DEVELOPMENT OF MONOCLONAL ANTIBODY-BASED ASSAYS FOR
DETECTION AND DIFFERENTIATION OF TRYPANOSOME SPECIES
IN THE TSETSE FLY (GLOSSINA SPP.)
A Thesis Presented to
The Board of Graduate Studies,
University of Ghana, Legon.
Ghana.
In fulfilment of the
Requirements for the Degree
of Doctor of Philosophy (Ph.D.)
(Animal Science),
By
KWABENA MANTE BOSOMPEM
BSc. (Hons.)
Department of Animal Science,
Faculty of Agriculture,
University of Ghana,
Legon, Accra. Ghana.
March, 1993.
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DECLARATION
I do hereby declare that except for references to other people's
investigations which have been duly acknowledged, this exercise is the result of my
own original research, and that this thesis, either in whole, or in part, has not been
presented for another degree elsewhere.
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D E D I C A T I O N
To Dr. J. E. Fletcher for the help in determining my
career, and to my wife Emestina and my children for their
understanding of the circumstances.
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ACKNOWLEDGEMENT
It is my first duty to acknowledge with pleasure, my indebtedness to all
the individuals, organisations and institutions that have contributed in various
ways to the formulation, execution and submission of the work described in
this thesis.
I will begin by expressing my sincere thanks to the Animal Science
Department, Faculty of Agriculture, University of Ghana, for making me the
beneficiary of the Research Fellowship awarded by the International
Laboratory for Research on Animal Diseases (ILRAD), and to my employers,
Noguchi Memorial Institute for Medical Research (NMIMR), University of
Ghana Legon, for granting me a study leave to undertake this study. I am also
grateful to the ILRAD Administration and the Training Department for
providing such excellent facilities and atmosphere under which this work was
carried out.
I am particularly indebted to Prof. Reginald K. G. Assoku and Dr.
Vinand Nantulya, my supervisors, not only for the guidance, encouragement
and stimulating discussions, but also for their unfailing courtesy and
cooperation. I also wish to express my deep gratitude to Dr. Rachael Masake,
for acting as my ILRAD supervisor during the absence of Dr. Nantulya. I am
particularly appreciative of the way in which Dr. Nantulya continued to find
time for this project, even after his departure from active service in ILRAD. I
am thankful to him.
I am extremely thankful to Dr. S. K. Moloo, head of the ILRAD tsetse
laboratory, for the help and encouragement he offered, and all his technicians,
particularly Messrs Joseph Muia, John Kabata and Clement Sabwa for their
unfailing cooperation and assistance in all the experiments involving the use of
laboratory-bred tsetse flies.
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I gratefully acknowledge the support granted to me by the Kenya
Trypanosomiasis Research Institute (KETRI) in making it possible to conduct
part of this work on the Galana Ranch, and the assistance received from that
institute from Dr. Elizabeth Opiyo. I am thankful to Dr. Chris Green for his
assistance in trapping tsetse flies, and Mr. T. Wanyama for helping me in both
trapping and dissection of tsetse at the Ranch.
I owe a special debt of gratitude to Dr. Ian Gumm and Dr. Ron
Kaminsky for supplying culture-derived trypanosomes for this project whilst
they were in ILRAD, and Mr. Francis Chuma of ILRAD for similar
assistance. Also, I remember Dr. Joe McNamara of the Tsetse Research
Laboratory, Bristol, England for supplying Trypanosoma grayi antigens for
this study and Dr. Andrew Peregrine of ILRAD for making this arrangement
possible.
The helpful advice and encouragement that was freely given by Dr.
Phelix Majiwa, Dr. M. Toure and Mr. Stephen Minja all of ILRAD, is greatly
appreciated.
I wish to thank Dr. M. K. Shaw for technical help in
immunolocalization studies; Henry Gathuo for introducing me to tissue culture
and immunofluorescence techniques; Messrs John Ngatti, James Thuo, Jackson
Makau, Benson Gichuki and Stephen Ngava for helping me to master the
various techniques described in this work; David Elsworth and J. Mwaura for
advice on preparation and presentation of illustrations, and Francis Shikhubari
for his expert assistance in photography.
Finally, I wish to thank Mr. Maxwell Appawu of the NMIMR, for the
immeasurable help he offered during my absence from Ghana.
V
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VI
TABLE OF CONTENTS
Page No.
TITLE PAGE .............................................................................................................................................. W
DECLARATION ........................................................................................................................................ (ii)
DEDICATION .............................................................................................................................................
4 and O.lmM KH2PO4 , pH 7.4). The molten agarose was poured
onto microscope slides and allowed to solidify. Wells were then cut into the
solid gel and each was filled with approximately 10/d of reagent. Antisera
were placed in a central well and test samples (culture supamatants
concentrated ten-fold by ammonium sulphate precipitation) were placed in the
surrounding wells. A precipitin line formed in-between a sample well and the
homologous antiserum in a central well. The precipitin reaction was allowed
to develop in up to 48 hr at room temperature in a wet chamber and observed
by viewing the gels against light. For preservation, agarose gels were
thoroughly washed with PBS, pH 7.4, followed by distilled water to remove
unprecipitated proteins, dried, and stained using Coomassie Brilliant blue
(Williams, 1971).
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4.3.10.2 Sodium dodecvl sulphate-polvacrvlamide gel electrophoresis (SDS-
PAGE)
Electrophoresis of trypanosome proteins was performed, using the
Bio Rad Protean II cell apparatus (Bio Rad, Italy) and following the SDS-Tris-
glycine discontinuous buffer system (Laemmli, 1970).
4.3.10.3 Assembly of slab gel apparatus, and preparation of resolution and
stacking gels
The gel casting apparatus consisted of four transparent glass plates
(16cm x 20cm), four 1.5mm thick plastic spacers, and four plastic clamps.
These were assembled such that the two glass plates wiped clean, using 70%
ethanol, were separated by the plastic spacers along the 16cm edges and
clamped together. The assembled glass plates were then secured vertically on
a gel casting platform so that the lower gap between each pair of plates was
sealed by a rubber gasket.
Resolution acrylamide gradient gels (7.5-15%) were prepared as follows:
Solution A. 7.5% resolution gel (one gel)
Deionised water 7.34ml
30% (w/v) acrylamide,
0.8% (w/v) N ' -methylene bis-acrylamide 3.75ml
1.5M,pH 8 .8 ,tris-(hydroxymethyl)
-aminomethane (Tris) 3.75ml
10% (w/v) sodium dodecyl sulphate (SDS) 0.3ml
N,N,N'-,N'-tetramethylethylenediamine (TEMED) 0.01ml
10%(w/v) ammonium persulphate (APS) 0.04ml
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Solution B. 15% resolution gel (one gel)
Deionised water 3.84ml
30%(w/v)acrylamide; 0.8%(w/v) bis-acrylamide 7.5ml
1.5M Tris, pH 8 . 8 3.75ml
10%(w/v) SDS 0.3ml
TEMED 0.01ml
10% APS 0.04ml
The acrylamide/bis-aerylamide solution and TEMED were stored in
brown bottles whilst 10% APS was prepared fresh and added to Solutions A
and B just before gel casting. All solutions were kept at 4°C, except 10% SDS
which was kept at room temperature.
A 7.5-15% resolution acrylamide gradient gel was prepared by
slowly mixing solution A and B using Bio-Rad Model 385 gradient former.
Each solution was swirled to mix and poured into one of the two separate
chambers of the gradient mixer. Solution B, with the highest acrylamide
concentration was placed in the chamber next to the outlet. The valve between
the two chambers was opened and a magnetic stirrer placed in solution B
started. A peristaltic pump (LKB, Sweden) set at a flow rate of 3ml/min was
used to deliver the gel mixture via rubber tubing into the space between the
two glass plates. The gel former apparatus was then immediately rinsed with
distilled water. The poured gel was overlaid with 500-1000^1 of water-
saturated butanol using a micropipette or pasteaur pipette and left for
approximately 1 hr to polymerize. After the resolution acrylamide gel
(separating gel) had set, the gel overlay was removed and the top of the gel
rinsed with distilled water. A stacking gel (Solution C) prepared as below was
then poured on top of the separating gel and a comb carefully inserted to cast
the desired wells for sample application.
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Solution C. 3% stacking gel (one gel)
Deionised water 7.5ml
30%(w/v) acrylamide; 0.8%(w/v) bis-acrylamide 1.5ml
0.5M Tris, pH 6 . 8 3.0ml
10%(w/v) SDS 0.125ml
TEMED 0.01ml
10% APS 0.05ml
The stacking gel was allowed 30 min to polymerize and the comb
removed. The cast gel units were then assembled in a Bio-Rad Protean II cell
electrophoresis apparatus. The upper electrophoretic chamber, at the cathode,
was filled with 0.4 litres of running-buffer (24.8mM Tris, 191.8mM Glycine
and 3.47mM SDS) and the lower chamber, at the anode, filled with 1.6 litres
of running-buffer diluted with 0.5 litres of deionised water.
4.3.10.4 Preparation of samples and electrophoresis run
The trypanosome crude extracts were adjusted for protein and
diluted with sample buffer [150mM Tris, pH 6 .8 , 104mM SDS, 3%(v/v)
mercaptoethanol, 30%(v/v) glycerol and 4%(v/v) bromophenol blue] at 2:1
sample to buffer ratio, to give a final protein concentration of approximately
lmg/ml. Standard high molecular weight markers (Rainbow Markers, MW
14,300 to 200,000; Amersham International pic, Amersham, UK) were diluted
1:1 with sample buffer without bromophenol blue. All the samples and
standard markers were boiled for 5 and 1 min, respectively, at 100°C in a
waterbath and centrifuged at 9,900 Xg for 5 min to remove particulate matter.
About 200/xg of the boiled trypanosome extracts or 5 to 10^1 of standard
molecular weight markers were loaded per lane of about 0.5cm width.
Electrophoresis was performed using the Bio-Rad protean II cell apparatus,
cooled to 10°C with a Lauda RC20 cooler (Bremen, Germany). A constant
voltage using electrophoresis power supply (EPS 500/400, Pharmacia Fine
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Chemicals) either at 50-70V/gel overnight, or at 300V/gel for 3-4 hr was
applied until the bromophenol blue tracer dye migrated almost to the end of the
separating gel. At the completion of the run, the assembled gel units were
removed from the electrophoresis chamber and dismantled.
4.3.10.5 Staining, destaining and western immunoblot
A vertical strip of the gel was cut using a surgical blade, and
transferred into a plastic tray containing staining solution [0.5%(w/v)
coomassie blue, 10%(v/v) acetic acid and 30 %(v/v) isopropyl] for 15 min.
The stained gel was then transferred to a destaining solution containing
10%(v/v) methanol and 7%(v/v) acetic acid on a gentle rotor (Red-Rotor
Model PR70, Hoeffer) with several changes of the solution until stained
protein bands were clearly visible in the gel (Weber and Osborn, 1969).
Separated trypanosome proteins were transferred electrophoretically from
unstained gels to nitrocellulose sheets, as described by Towbin, Staechelin and
Gordon (1979) and Burnette (1981). Briefly, 3mm Whatman chromatography
paper (Whatman, Maidstone, England) was soaked with transfer buffer [25mM
Tris, 192mM glycine, 0.1%(w/v) SDS and 20%(v/v) methanol] and placed on
top of a scouring pad (Scotch-Brite, Hoefer Scientific Instruments, USA)
wetted in the same buffer and supported by a stiff plastic grid. The gel was
then placed on top of the chromatography paper. A sheet of nitrocellulose
filter (0.45/an pore size, Schleicher and Schuell, Inc., Keen, NH, USA)
trimmed to fit the gel, was briefly wetted with transfer buffer and carefully
placed on top of the gel without trapping air bubbles. A second
chromatography paper and scouring pad, both soaked in the same buffer, and a
plastic grid were added in that order and clipped. The sandwiched gel was
then fitted in a Transphor Electrophoresis Unit, Model TE50 (Hoeffer
Scientific Instruments, San Francisco, USA) filled with transfer buffer.
Electrophoretic transfer was run at a constant voltage (either at 10V overnight
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or at 70V for 3 hr) with the nitrocellulose sheet facing the cathode. The
nitrocellulose was removed, cut into strips and immuno-assayed using the
method described for the detection of in vitro propagated tiypanosomes by dot-
ELISA (section 4.3.9.1).
4.3.10.6 Electro-elution of proteins from polyacrylamide gels
Individual coomassie-stained protein bands of interest were cut out
of polyacrylamide gels using a scalpel blade, and chopped into small pieces.
The two screw cups of the electrophoresis concentration chambers of the Ecu-
040 electrophoresis elution apparatus (CBS Scientific Company, Inc., USA),
were fitted with Spectra/Por dialysis membrane, molecular weight cut-off
3,500 (Spectrum Medical Industries, Inc., USA) and the cut gel placed in the
large wells. All the chambers of the apparatus were filled with elution buffer
(50mM ammonium bicarbonate, 0.97mM l,4'-Dithiothreitol and 0.1%(w/v)
SDS) to volumes recommended by the manufacturer. Protein elution was
performed at a constant current of 12mA/cell for 17-24 hr at room
temperature. The elution buffer was then carefully replaced with dialysis
buffer (lOmM NH3HCO3 and 0.02%(w/v) SDS) without disturbing the eluted
proteins concentrated in the small well of the concentration chamber. Dialysis
was performed using the same current for 2 hr. At the end of the run, the
dialysis buffer was carefully pipetted out of the concentration chambers and the
eluted proteins resuspended in a small volume of PBS, pH 7.4. These samples
were immediately used to immunize mice for the production of MoAbs, or
stored frozen at -20°C before use.
4.3.11 Determination of the biochemical nature of antigenic epitopes
4.3.11.1 Detection of MoAbs specific for carbohydrate epitopes
The micro-plate ELISA based periodate oxidation at acid pH
described by Woodward, Young and Bloodgood (1985) was used in
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determining whether the antigenic epitopes detected by the specific MoAbs
were carbohydrate in nature. Crude trypanosome extracts were diluted in
coating buffer (34.5mM NaHC03 and 15.1mM Na2C03) at dilutions
previously determined by titration, and dispensed (100/tl/well) into a 96-well
micro-plate (Immulon, Dynatech Laboratories, Chantilly, Virginia, USA) and
blocked overnight at 4°C. The plates were rinsed once with washing buffer
consisting of 0.05%(v/v) Tween 20 in PBS, pH 7.4, followed by a second
rinse using 50mM sodium acetate buffer, pH 4.5. Sets of wells were then
incubated with varying concentrations of periodate (0, 10, and 20mM) in
sodium acetate buffer (1 0 0 /xl/'well) for 1 hr at room temperature in the dark.
The plates were rinsed once with sodium acetate buffer, and incubated with
1% glycine, 100/d/well, for 30 min at room temperature, after which they
were rinsed five more times with washing buffer. The wells were incubated
with MoAbs of murine origin diluted appropriately, in washing buffer,
1 0 0 /d/well, for 1 hr at room temperature, and the plates washed five times
with washing buffer to get rid of excess unbound antibody. To each well was
then added 100/d of HRPO-conjugated goat anti-mouse antibodies diluted at
1:1000 in washing buffer. The plates were washed five times with washing
buffer and incubated with substrate solution [40mM 2,2'-azino bis-(3-
ethylbenz-thiazoline sulfonic acid) diammonium salt (ABTS) and 0.01%(v/v)
hydrogen peroxide in 50mM citric acid buffer, pH 4.0], The reaction was
allowed to proceed for 30 min and the plates read at a wavelength of 414nm
using a Titertek Multiskan micro-plate ELISA reader (MCC/340, Labsystems
and Flow Laboratories, Finland).
4.3.11.2 Detection of MoAbs specific for protein epitopes
Monoclonal antibodies (MoAbs) with specificity for protein
antigenic epitopes were detected using enzymatic digestion with proteinase-K
according to the methods described by Martin, Larose, Hamel, Lagac'e and
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Brodeur (1988) and Lussier et al. (1989) with some modifications. Fifty
micrograms of proteinase-K (Bethesda Research Laboratories, USA) diluted in
PBS, pH 7.4, was added to 100/zg of fresh trypanosome crude antigens
extracted in PBS by the freeze and thaw method. One hundred microgram
amounts of each antigen extract were pipetted into two different eppendorf
tubes. Fifty micrograms of proteinase-K in 50/xl PBS was added to one
sample, whilst the other sample was diluted with 50pd of plain PBS. Both
tubes were incubated at 37°C in a waterbath for 1 hr and 3/xl samples pipetted
onto nitrocellulose strips in dots. The strips were assayed as described under
section 4.3.9.1.
4.3.12 Micro-plate ELISA
Non-competitive ELISA techniques were used for the detection of
antibody, employing the double antibody sandwich method (Cheng, L.Y.,
1987; Beards and Bryden, 1981) and for the detection of antigen, using the
indirect-system (Sandwich-ELISA) as described by Nantulya et al. (1987) and
Nantulya (1989).
4.3.12.1 Coating microtitre plates with antigen or antibody
Trypanosome extracts or purified MoAbs were diluted in
carbonate-bicarbonate buffer consisting of 34.5mM NaHC03 and 15.1mM
Na2C0 3 , pH 9.6 (coating buffer). Flat-bottomed 96-well microtitre plates
were coated with 100jul/well of 10-15/xg of crude antigen or 2.5-5.0 jug/ml of
purified MoAb. The coating concentrations were determined by chequerboard
titrations as described by Voller, Bidwell and Bartlett (1980). The plates were
covered and the adsorption of antigen or antibody onto the polystyrene wells
achieved by overnight incubation at 4 °C.
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4.3.13 Micro-plate ELISA procedure
4.3.13.1 Antibody detection ELISA
Antibody detection ELISA was used for screening hybridoma
culture fluids for the selection of trypanosome species-specific MoAbs. This
method was also used for screening sera from immunized mice. In this assay,
micro-ELISA plates were coated with antigens of a particular trypanosome
species, and then rinsed once with washing buffer to remove excess unbound
antigen. Culture fluids and positive controls (prefusion sera taken from
immunized mice diluted, 1:500) and negative controls (normal mouse serum
diluted 1:500) or titrated sera from immunized mice, were transferred to a
micro-ELISA plate (100^1/well) and incubated for 15 min at 37°C. The
micro-ELISA plates were rinsed once with washing buffer to remove excess
unbound antibody, and all the wells incubated with 1 0 0 /zl/well goat anti-mouse
HRPO conjugate diluted at 1:1000 for 15 min at 37°C. The plates were then
washed 3 times, each by 10 min incubation with washing buffer to remove
excess unbound conjugate. The presence of bound conjugate was revealed by
the addition of substrate solution consisting of 40mM 2,2'- azino-bis (3-
ethylbenzthiazoline-6 -sulfonic acid) (ABTS) and 0.01%(v/v) hydrogen
peroxide in 50mM citric acid buffer, pH 4.0. The substrate was incubated for
30 min at room temperature. The colourless substrate solution changed to
green in wells with bound enzyme conjugates. The optical densities were read
at 414nm wavelength using a Titertek Multiskan micro-ELISA reader.
4.3.13.2 Antigen detection sandwich-ELISA
A simplified sandwich-ELISA using MoAb-coated polystyrene
micro-ELISA plates was used for antigen detection. The plates were coated
with 100/i/well of 2.5-5.0 jug/ml of purified MoAbs and rinsed once with
washing buffer to remove uncoated antibody. The plates were then incubated
for 15 min at 37°C with 100/xl/well of trypanosome antigen extracts titrated
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serially (using washing buffer as diluent) to give protein concentrations of 1 0 -
0.714 /ig/ml. Antigen molecules were captured specifically by the coating
MoAb. The plates were rinsed twice with washing buffer to remove
uncaptured antigen. This was followed by incubation with 100/il/well
horseradish peroxidase-labelled MoAb, diluted 1:500 in washing buffer at
37°C for 15 min. During this step, the conjugated MoAb reacted with the
antigen that had previously been captured by the coating MoAb. The plates
were washed, the substrate solution added, and the results read as described for
antibody detection-ELISA (section 4.3.13.1).
4.3 .13.3 Inhibition ELISA
Inhibition ELISA was used to study the relationship between
trypanosome species-specific MoAbs. By this method it was possible to
determine whether the binding of one antibody inhibited binding by another.
Micro-ELISA plates were coated with antigens of a particular trypanosome
species and rinsed once with washing buffer. Sets of wells were then
incubated for 15 min at 37°C with 100/xl/well serial dilutions of different
MoAbs specific for the coating trypanosome species. MoAbs with specificity
to different trypanosome species (non-related MoAbs) were titrated as above
and used as controls. A second control consisted of a set of wells that were
not incubated with any antibody. The plates were rinsed twice to remove
excess unbound antibody and then incubated as above with a uniform
concentration of MoAb-HRPO conjugate of one of the specific MoAbs used
earlier. The plates were washed three times (10 min/wash) to remove excess
antibody-conjugate. Substrate solution was added and the optical densities
read as described previously (section 4.3.13.1). The effect of the non-related
MoAbs on conjugate binding, was interpreted as protein to protein interactions
that were not due to specific inhibition. The conjugate activity in the control
wells that were not incubated with antibody, gave the level of conjugate
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binding without interference. The results of these inhibition experiments were
interpreted by two-way analysis of variance (Snedecor and Cochram, 1980).
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4.4.1 Selection of MoAbs from those produced previously
Experiments were carried out using the nitrocellulose membrane-based
dot-ELISA, the indirect immunofluorescent antibody test (IFAT) and the
micro-plate ELISA assays, to re-examine the specificities of the MoAbs
produced previously by Nantulya et al. (1987). Also, the sensitivity, in terms
of the minimum number of procyclics or epimastigotes that could be detected
by the extant MoAbs in the dot-ELISA, was studied. Following those
experiments, the MoAbs listed in Table 7 were selected for further studies.
The selected MoAbs reacted specifically with various trypanosome
species or subspecies as shown in Table 7. The minimum number of
trypanosomes that each of these MoAbs could detect, are however reported in
Chapter 5.
4.4.2 Immunizing Antigens and Antibody Responses in Immunized Mice
The BALB/c mice responded well to the various trypanosome antigen
preparations that were used in the immunizations. In general, high serum
antibody responses, with titres far beyond 1 :1 0 ,0 0 0 , were obtained against
homologous trypanosome antigens, as determined by the double-antibody
sandwich micro-plate ELISA. However, differences were found in the ability
of the three different trypanosome antigen preparations (namely,
formaldehyde-fixed whole trypanosomes, trypanosome crude-antigen extracts
or purified trypanosome antigens) to induce antibody responses that were
essentially species-specific.
Figure 9, illustrates the mean antibody responses of mice following
immunization with T. brucei procyclic crude antigen extract (BPCAE). The
individual curves in this figure show that the mice produced antibodies that
4.4 Results
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Table 7: Reactivity of selected extant MoAbs with procyclics or epimastigotes of
different trypanosome species/subspecies as determined by
dot-ELISA, IFAT and micro-plate ELISA
Monoclonal
Antibody Isotype
T. brucei
*
T. vivax
**
T. congolense
*
T. simiae
*
TR7/47.37.16 IgM + - - -
TV8/8.33.42 IgG3 - + - -
C2 IgGi - - + -
TC6/42.6.3 IgG, - - + -
TC40/30.15.40 IgM - - + -
TC39/30.25.95 IgM - - + -
TC16/5.12.33 IgGi - - + +
TC6/25.25.4 IgG3 - + +
* procyclics.
** epimastigotes.
+ = antibody reacts with trypanosomes.
- = antibody does not react with trypanosomes.
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1 0 9
Figure 9
Serum antibody response of BALB/c mice against antigens of
different trypanosome species following immunization with T.
brucei procyclic crude antigen extract. Each point represents the
mean of three test readings obtained for three different mice +
the standard error.
O.D. = Optical density.
T.b.Ag = Curve showing serum antibody response against T.
brucei antigen.
T.c.Ag = Curve showing serum antibody response against T.
congolense antigen.
T.v.Ag = Curve showing serum antibody response against T.
vivax antigen.
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®
oc
CO
S2u.o
V)
JQ
<
Q
o
2.00-1
1.50
1 .0 0 t
0.50
o.oo r ---------- r -------- r
100 200 400
- A — T.b. Ag
l-O
H
I | j |------------ T V
800 1600 3200 6400 12800 25600 51200
Reciprocal dilution
— T.c. Ag —O— T.v. Ag
Figure 9
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110
cross-reacted with equal concentrations of antigens derived from three different
trypanosome species (T. brucei, T. congolense and T. vivax). Even though the
mean antibody titre against immunizing T. brucei antigens was the highest, the
titres recorded against T. congolense or T. vivax were substantially high, with
both maintaining optical densities > 0 .5 for serum dilutions of up to 1:200.
On the other hand, the mean antibody response against T. brucei antigens was
maintained at optical densities > 1 .0 for serum dilutions of up to 1:6,400.
The mean antibody responses of other mice which were immunized
with purified T. brucei procyclic antigens (PBPA), are shown in Figure 10.
At a serum dilution of 1:100, the optical density of the mean response against
T. brucei antigens was >1 .0 whereas, that against T. congolense or T. vivax
was <0 .25 . At a serum dilution of 1:400, the mean antibody response against
T. brucei antigens still gave an optical density >1.0 , whereas, that against T.
congolense and T. vivax were reduced to zero. At a serum dilution of
1:12,800, the optical density of the reactivity against T. brucei antigens,
remained higher than that against T. congolense or T. vivax at 1:100 serum
dilution. This immunization with purified T. brucei procyclic antigens, thus
demonstrates antibody responses that were essentially species-specific.
The ability of purified trypanosome antigens to induce antibody
responses that were essentially species-specific, was also demonstrated for T.
vivax and T. simiae.
In the case of T. vivax, BALB/c mice were immunized with purified T.
vivax epimastigote antigens (PVEA), and screened for serum antibody response
against equal concentrations of T. vivax, T. brucei, T. congolense and T.
simiae antigens. The individual curves shown in Figure 11, illustrate the mean
antibody responses against the different antigens. At a serum dilution of
1:400, the mean optical density of serum antibody reactivity against T. vivax
antigens was > 1 .5 , whilst that against the other trypanosome antigens, was
< 0 .5 . The mean serum reactivity against T. vivax antigens maintained
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I l l
Figure 10
Serum antibody response of BALB/c mice against antigens of
different trypanosome species following immunization with
purified T. brucei procyclic antigens. Each point represents the
mean of three test readings obtained for three different mice +
the standard error.
O.D. = Optical density.
T.b.Ag = Curve showing serum antibody response against T.
brucei antigen.
T.c.Ag =Curve showing serum antibody response against T.
congolense antigen.
T.v.Ag = Curve showing serum antibody response against T.
vivax antigen.
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1.50n
100 200 400
“ A— T.b. Ag
f t ----------- ? ----------- 1 f ------------- t “ -------$
600 1600 3200 6400 12800 25600 51200
Reciprocal dilution
— T.c. Ag - O - T.v. Ag
Figure 10
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1 1 2
Figure 11
Serum antibody response of BALB/c mice against antigens of
different trypanosome species following immunization with
purified T. vivax epimastigote antigens. Each point represents
the mean of three test readings obtained for three different mice
+ the standard error.
O.D. = Optical density.
T.v.Ag = Curve showing serum antibody response against T.
vivax antigens.
T.b.Ag = Curve showing serum antibody response against T.
brucei antigens.
T.c.Ag = Curve showing serum antibody response against T.
congolense antigens.
T.s.Ag = Curve showing serum antibody response against T.
simiae antigens.
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O
.D
.
(A
bs
or
ba
nc
e)
Reciprocal dilution
—O— T.v. Ag —A— T.b. Ag — T.c. Ag — T.s. Ag
Figure 11
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113
an optical density of about 0.5 at a serum titre of 1:6,400, when reactivity
against antigens of the other trypanosome species were almost nonexistent
(Figure 11).
Serum antibody responses of mice immunized with purified T. simiae
procyclic antigens (PSPA) are shown in Figure 12. The individual curves
show the mean serum antibody responses against equal amounts of T. simiae,
T. brucei and T. vivax antigens. An elevated antibody response is clearly
shown against T. simiae antigens as compared with the responses against
antigens of the other trypanosome species. At a serum titre of 1:100, the mean
optical density of the reactivity against T. simiae antigens was >1.25,
whereas, that against antigens of T. brucei, T. congolense and T. vivax was
each below 0.5. Furthermore, for serum dilutions >1:3,200, the reactivity on
T. simiae antigens gave a mean optical density of about 0.75, whereas there
were no reactions at all against antigens of the other trypanosome species, thus
demonstrating specific reactivity with T. simiae.
Screening for serum antibody responses in immunized mice, was also
performed using the IFAT technique. Table 8 summarizes the results obtained
for serum antibody responses of one of the mice immunized with formaldehyde
fixed T. vivax epimastigotes (FFVE). To enable the selection of the best
responder mice for cell fusion, using this method of screening, the
fluorescence on test trypanosomes were graded from; negative (-); weak
positive (+); to strong positive (+ + + +). Antibodies produced in this mouse
reacted strongly with epimastigote antigens of East African T. vivax (EATV)
as well as those of West African T. vivax (WATV), with antibody titres of up
to 1:400 and 1:800 respectively (Table 8). Also the antibodies cross-reacted
weakly < (+ +) with procyclic antigens of T. brucei (TB), T. congolense
(TCK) and T. simiae (TS), with antibody titres ranging from 1:50 to 1:100.
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1 1 4
Figure 12
Serum antibody response of BALB/c mice against antigens of
different trypanosome species following immunization with
purified T. simiae procyclic antigens. Each point represents the
mean of three test readings obtained for three different mice +
the standard error.
O.D. = Optical density.
T.s.Ag = Curve showing serum antibody response against T.
simiae antigens.
T.c.Ag = Curve showing serum antibody response against T.
congolense antigens.
T.b.Ag = Curve showing serum antibody response against T.
brucei antigens.
T.v.Ag = Curve showing serum antibody response against T.
vivax antigens.
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■O
<
Q
o
0 .50 -
0 . 0 0
100 200 400
T.s. Ag
800 1600 3200 6400
Reciprocal dilution
— ♦ — T.c Ag —A— T.b. Ag
12800 25600 51200
—O— T.v. Ag
Figure 12
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1 15
Table 8
Antibody response of a BALB/c mouse following immunization with
formaldehyde fixed Trypanosoma vivax epimastigotes
Serum
dilution
Reactivity of serum with different
trypanosome species by IFAT
EATV WATV TB TCK TS
1/50 + + + + + + + + + + + +
1 / 1 0 0 + + + + + + + + +
1 / 2 0 0 + + + + + -
1/400 + + + - -
1/800 - + - -
EATV = East African T. vivax epimastigotes.
WATV = West African T. vivax epimastigotes.
TB - T. brucei procyclics.
TCK = T. congolense Kilifi type procyclics.
TS = T. simiae procyclics.
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116
Other mice immunized with FFVE produced serum antibodies that reacted
similarly as the one described above.
4.4.3 Cell Fusions and Selection for Hybridomas
Twenty eight independent cell fusions were made for the production of
trypanosome species-specific MoAbs. Of those fusions, 10, 8 and 10 were
made for the production of T. brucei, T. vivax and T. simiae specific MoAbs,
respectively. Antibody secreting hybridomas were cloned at least twice by
limiting dilution, and the class and subclass of the secreted MoAbs determined
by the Ouchterlony double immunodiffusion method (section 4.3.10.1).
4.4.3.1 Anti-T. brucei MoAb secreting hybridomas
The results of ten independent cell fusions made towards the production
of T. brucei specific MoAbs are summarized in Table 9. Four of these fusions
(TB39a, TB40a, TB40b and TB42) were carried out using spleen cells from
mice immunized with formaldehyde fixed T. brucei procyclics (FFBP). From
these fusions, only one hybridoma from TB39a had the desired specificity for
T. brucei. Another hybridoma obtained from TB40a secreted a MoAb that
reacted specifically with T. brucei antigens in the double antibody sandwich
ELISA. However that MoAb cross-reacted with antigens of T. congolense and
T. simiae when tested using the Western immunoblot technique (Table 9).
Cell fusions (TB40c, TB40d and TB41) were undertaken using spleen cells
from mice immunized with crude antigen extracts of T. brucei procyclics
(BPCAE) (Table 9). None of the hybridoma cells derived from those three
fusions secreted any MoAb that was T. brucei specific, despite a high number
of fusion wells with antibody activity (Table 9). The highest success in
deriving hybridomas that secreted T. brucei specific MoAbs was achieved from
fusions TB43 and TB44, both of which were carried out using spleen cells
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1 17
Table 9: Results of cell fusions made towards the production of T. brucei specific MoAbs
Fusion Origin o f
spleen
cells
Immunogen Myeloma
parent
Spleen cell
count for
fusion
Numbers o f
wells
showing
growth of
hybrids
Number (%)
of positive
wells a
Number o f
wells with
specific
reactivity^
Number o f
hybrids
cross-reacting
by other tests
Number o f
stable hybrids
secreting
specific
antibodys
TB39a BALB/c FFBP NSI/lAg4.1 3 .6 x l06 16/48 10(62%) 1 0 1
TB40a - 4 .1 x l0 6 48/48 41(85%) 1 l w 0
TB40b ' ■ 1 3.2x10® 42/48 31(74%) 0 n/a n/a
TB40c " BPCAE 2 .1 x l0 6 45/48 36(80%) 0 n/a n/a
TB40d ti - i 3 .2 x l0 5 48/48 47(98%) 0 n /a n /a
TB41 * « • 5 .2 x l07 20/48 10(50%) 0 n/a n/a
TB42 n FFBP n 8x l06 12/48 3(25%) 0 n/a n/a
TB43 « PBPA X63/AG8.653 6 .9x l07 42/48 16(38%) 4 0 3
TB44 - - 9 .4 x l0 6 40/48 6(15%) 4 0 2
TB45 n n 1 7 .9 x l0 7 48/48 48(100%) 3 3w 0
a Supernatants were tested in double antibody sandwich ELISA using T. brucei antigen coated micro-ELISA plates,
b Tested in double antibody sandwich ELISA using 4 different antigens (T. brucei, T. vivax, T. congolense and T. simiae).
s Hybridoma cells which secreted specific antibody into culture supernatants after two months o f continuous culture in vitro.
w Number o f hybridomas that secreted cross-reacting MoAbs when tested using the Western immunoblot technique.
073 not applicable.
FFBP = Formaldehyde fixed T. brucei procyclics.
BPCAE = T. brucei procyclic crude antigen extract.
PBPA = Purified T. brucei procyclic antigens.
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118
from mice immunized with a purified T. brucei procyclic antigen preparation
(PBPA). These two fusions yielded 5 T. brucei specific antibody-producing
hybridomas (Table 9). One other fusion which was undertaken using spleen
cells from a mouse that was immunized with PBPA produced three hybridomas
that secreted MoAbs that reacted specifically with T. brucei in the micro-plate
ELISA. However, those MoAbs were found to cross-react with T.
congolense, T. simiae and T. vivax in the Western immunoblot assay (Figure
13). Cell clones that were isolated from T. brucei specific antibody-secreting
hybridomas were found to be stable as determined by sustained MoAb
secretion in continuous in vitro culture for two months.
Figure 14 shows an example of the micro-plate ELISA results when
used for screening 45 out of 48 wells from the T. brucei cell fusion TB43.
The reactions in wells A(5&6) and F(9&10) occur on all three microtitre
plates, indicating that the hybridoma cells from the corresponding tissue
culture well secreted antibodies that cross-reacted with antigens from all the
three species of trypanosomes. On the other hand, the reactions in wells
B(l&2), C(5&6), D(5&6), E(5&6) and F(5&6) are only seen on the T. brucei
coated plate, demonstrating that the hybridoma cells from the corresponding
tissue culture wells were secreting antibodies that react specifically with only
T. brucei antigens.
4.4.3.2 Anti-T. vivax MoAb secreting hybridomas
Table 10 gives a summary of all the cell fusions performed with the
aim of producing T. vivax specific MoAbs. Five of these fusions (TV30,
TV31, TV32, TV33 and TV34) were made using spleen cells from mice
immunized with formaldehyde fixed T. vivax epimastigotes. Of these one
fusion (TV34) produced no wells with antibody activity even though two wells
had hybridoma cell colonies (Table 10), and two (TV30 and TV33) produced
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1 1 9
Figure 13
Western immunoblot cross-reactivity of a MoAb secreted by a hybridoma
which was produced by fusing a myeloma cell with a spleen lymphocyte
from a BALB/c mouse immunized with purified T. brucei procyclic
antigens. Strip (A) shows the reactivity with electrophoresed T. brucei
IL2616 antigens; (B) with T. congolense K/83/IL/97/2 antigens; (C) with T.
simiae KETRI 2431 antigens, and (D) with T. vivax IL1392 antigens.
Notice the weak cross-reactivity of the MoAb with a 58 kDa antigen.
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B C
cDa
58 -
Figure 13
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Figure 14
Screening for T. brucei specific MoAbs in culture supernatants from cell
fusion TB43 using micro-plate ELISA. The spleen cell donor BALB/c
mouse was immunized with purified T. brucei procyclic antigens. Plate I
was coated with T. brucei procyclic antigen; Plate II with T. congolense
procyclic antigen, and Plate III with T. vivax epimastigote antigen. Culture
supernatants from fusion wells were tested in duplicates in identical wells on
all three plates. Wells G(ll&12) were incubated with 1:100 dilution of
normal mouse serum as negative controls, and H(ll&12) were incubated
with 1:100 dilution of pre-fusion mouse serum as positive controls. Also,
wells A(l&2) was used to assess non-specific conjugate binding by omitting
the addition of samples.
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1 2 3 4 5 6 7 8 9 10 11 12
A r ' . r ’r ^ "S ^
B # ,< # r A A A A *S -S ^ -S
C
e 6 e A
F 4 • > '
G
1 2 3 4 5 6 7 8 9 10 11 12
o o V \ SA o U J \ j sJ \ j J J
V v V ■■ - ■' ^ J J
O 'V j .J vJ
K,yr. ■ _ ' s " . • ■ • -.j W ^ J
:'y y- y - - ’ -' V V ^ •'
V - ^ ^ J
\ - W
y » y ;y v v 1y iv ;V is / ,'VW
1 2 3 4 5 6 7 8 9 10 11 12
c. v ^ o o
1 I----------------- I L
Plate I Plate l l P late I I I
Figure 14
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121
Table 10: Results of cell fusions made towards the production of T. vivax specific MoAbs
Fusion Origin of
spleen
cells
Immunogen Myeloma
parent
Spleen cell
count for
fusion
Numbers o f
wells
showing
growth of
hybrids
Number (%)
o f positive
wells3
Number o f
wells with
specific
reactivity*3
Number o f
hybrids
cross-reacting
by other testsw
Number of
stable hybrid,
secreting
specific
antibodys
TV30 BALB/c FFVE NSI/lAg4.1 1 .25xl07 5/48 2(40%) 0 n/a n/a
TV31 ■ - 1 .65xl07 17/48 7(41%) ll 0 1
TV32 » " ■ 5 .8x l07 38/48 19(50%) 31 0 3
TV33 ' 8 .8 x l06 26/48 4(15%) 0 n/a n/a
TV34 - Tl Sp2/OAG14 6 .4 x l0 5 2/48 0(0%) 0 n/a n/a
TV35 " CVEAL 5x l0 6 15/48 5(33%) 0 n/a n/a
TV36 * X63/AG8.653 2 .4 x l0 6 45/48 30(67%) 0 n/a n/a
TV37 ■ PVEA 3 .2x l07 48/48 48(100%) 9d 0 9
a Supernatants were tested in double antibody sandwich ELISA using T. vivax antigen coated micro-ELISA plates,
b Tested in double antibody sandwich ELISA using 4 different antigens (T. brucei, T. vivax, T. congolense and T. simiae).
s Hybridoma cells which secreted specific antibody into culture supernatants after one month of continuous culture in vitro.
I Supernatants were tested in Indirect Fluorescent Antibody Test (IFAT) using 4 different antigens (T. vivax, T. brucei, T. congolense and T. simiae).
D Tested in dot enzyme immunoassay (dot-ELISA) using 4 different antigens (T. vivax, T. brucei, T. congolense and T. simiae).
w Tested for cross-reactivity using the Western immunoblot technique.
not applicable.
FFVE = Formaldehyde fixed T. vivax epimastigotes.
CVEAL = Crude T. vivax epimastigote antigen lysate.
PVEA = Purified T. vivax epimastigote antigens.
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1 22
wells with antibody activity, but none of them was specific for T. vivax. The
remaining two fusions (TV31 and TV32) produced four hybridomas of desired
specificity for T. vivax as determined by IFAT. All the positive clones derived
from those wells were stable (Table 10).
None of two fusions (TV35 and TV36) made with spleen cells from
mice immunized with crude T. vivax epimastigote antigen lysate (CVEAL)
produced wells with specific activity against T. vivax, although both fusions
had wells with antibody activity against trypanosome antigens. Cell fusion
(TV37) was made using spleen cells from mouse MTV32 immunized with a
purified T. vivax epimastigote antigen (see Figure 11). The products from this
cell fusion were screened by dot-ELISA (Figure 15). All the 48 fusion wells
showed antibody activity against the T. vivax epimastigote antigen (Figure 15).
Of these, wells (1, 4, 19, 32, 33, 34, 35, 42 and 43) contained antibodies that
reacted specifically with the T. vivax antigen. The cells from wells 19, 33 and
34 were selected for cloning based on the stronger reactivity of the secreted
antibodies and the relatively fewer cells that were present in those wells.
The hybridoma (KD37/19.3) derived from well 19 was selected for
further studies.
4.4.3.3 Anti-T. simiae MoAb secreting hybridomas
Of ten cell fusions carried out with the aim of producing T. simiae
specific MoAbs, four were made using spleen cells from mice previously
immunized with formaldehyde fixed T. simiae procyclics (FFSP). All these
four fusions (TS1, TS2, TS3 and TS4) produced hybridomas which secreted
antibodies to trypanosome antigens (Table 11). However, only two of those
fusions (TS3 and TS4) yielded hybridomas with antibodies specific for either
T. simiae or the Nannomonas subgenus. TS3 had one well with hybrids that
secreted T. simiae specific antibodies. These hybrids were, however, not
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123
Figure 15
Screening for T. vivax specific MoAbs in culture supernatants from wells of
cell fusion TV37 using dot-ELISA. The spleen cell donor BALB/c mouse
was immunized with purified T. vivax epimastigote antigens. Culture
supernatant from each of the 48 fusion wells was incubated with one strip of
NC membrane which was previously "dotted" with lxlO 5 T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431
(TS) cultured procyclics, and lxlO5 T. vivax IL1392 (TV) cultured
epimastigotes. (a.) represents culture supernatants that contained antibodies
that reacted specifically with T. vivax epimastigotes; (■) represents culture
supernatants that contained antibodies that cross-reacted with all the four
trypanosome species that were tested.
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25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48
Figure 15
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124
Table 11: Results of cell fusions made towards the production of T. simiae specific MoAbs
Fusion Origin of
spleen
cells
Immunogen Myeloma
parent
Spleen cell
count for
fusion
Numbers of
wells
showing
growth o f
hybrids
Number (%)
o f positive
wellsa
Number o f
wells with
specific
reactivity
Number o f
hybrids
cross-reacting
by other testsw
Number of
stable hybrids
secreting
specific
antibodys
TS1 BALB/c FFSP NSI/lAg401 1 .2x l07 11/48 6(54%) 0 n/a n /a
TS2 n " 6.8x10® 9/48 7(78%) 0 n/a n/a
TS3 n " 2 .3 x l0 5 8/48 4(50%) l 1 0 0
TS4 7.1x10® 10/48 8(80%) I * I 0 1
TS5 n CSPAL Sp20AG14 3.8x10® 16/48 12(75%) 2D;11*D 0 1
TS6 t " 4 .4 x l0 7 48/48 47(98%) 0 n/a n/a
TS7 " PSPA X63/AG8.653 7 .2 x l0 7 48/48 48(100%) 1D 0 0
TS8 " (41.7-43.6)kDa** 6 .9x l07 8/48 2(25%) 0 n/a n/a
TS9 ■ 75 kDa** 8 .9x l07 13/48 6(46%) 0 n/a n/a
TS10 " 107 kDa** " l . lx lO 7 18/48 10(56%) 0 n/a n/a
a Supernatants were tested in double antibody sandwich ELISA using T. sim iae antigen coated micro-ELISA plates.
s Hybridoma cells which secreted specific antibody into culture supernatants after one month o f continuous culture in vitro.
I Supernatants were tested in Indirect Fluorescent Antibody Test (IFAT) using 4 different antigens (T. simiae, T. congolense, T. brucei and T. vivax).
D Tested in dot enzyme immunoassay (dot-ELISA) using 4 different antigens (T. simiae, T. congolense, T. brucei and T. vivax).
w Tested for cross-reactivity by the Western blot technique.
H^ a Not applicable.
FFSP = Formaldehyde fixed T. simiae procyclics.
CSPAL = Crude T. simiae procyclic antigen lysate.
PSP A = Purified T. simiae procyclic antigens.
* Hybridoma secreting Nannomonas species-specific monoclonal antibody.
** Antigen band electro-eluted from polyacrylamide gels.
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1 25
stable as they stopped antibody secretion when maintained in continuous
culture in vitro. As a result, the hybrid was lost during cloning. The fusion
(TS4) had one well with specificity for the Nannomonas subgenus. This
hybrid was cloned successfully.
Two fusions (TS5 and TS6) were made using spleen cells from mice
immunized with crude T. simiae procyclic antigen lysate (CSPAL). One of
these fusions (TS5) produced one hybridoma with specific antibodies to the
Nannomonas subgenus (Table 11). However, none of the hybridomas from
TS6 secreted antibodies that were specific for either T. simiae or the
Nannomonas subgenus. The fusions (TS8, TS9 and TS10) were made using
spleen cells from mice immunized with T. simiae antigen bands of varying
molecular weights that had been electro-eluted from polyacrylamide gels
(Table 11, Figure 16). These bands were selected based on the following
rationale. T. simiae and T. congolense procyclic extracts were electrophoresed
side by side on polyacrylamide gels and the resolved bands studied for
differences in molecular weight (MW). All T. simiae antigen bands that occur
at MW where there were no corresponding T. congolense bands, were pin
pointed. Reasoning that some of the T. simiae unique bands may contain
antigens that define T. simiae specificity, the bands were separately electro
eluted and used for immunizing BALB/c mice. Though each of die three
fusions made with spleen cells from mice immunized with electro-eluted
antigen bands produced hybridomas with antibody activity, none of them was
specific for T. simiae or the Nannomonas subgenus.
The fusion (TS7) which was made using spleen cells from the mouse
MTS7 immunized with a purified T. simiae procyclic antigen produced the
most promising results (Figure 17). Figure 17 shows the result of this cell
fusion as screened by dot-ELISA. All the wells from this fusion had colonies
of hybrid cells that were secreting antibodies to trypanosome antigens. Of
these, 11 wells had antibodies specific to the Nannomonas subgenus, whereas 2
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126
Figure 16
Comparison of coomassie stained polyacrylamide gel electrophoresed T.
simiae (KETRI 2431) and T. congolense (K/83/IL/97/2) antigens. Lane 'C'
shows the staining pattern of T. simiae antigens; Lane 'B' the staining
pattern of T. congolense antigens; and lane 'A ', the molecular weight
markers. T. simiae antigen bands without corresponding T. congolense
bands of identical molecular weights were numbered 1 to 8 .
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A
i------- 1
92 .5—
69 -
46 - *
30 - +>
21 .5 - *
14 .3 - |
2 0 0 -
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1 2 7
Figure 17
Screening for T. simiae specific MoAbs in culture supernatants from wells
of cell fusion TS7 using dot-ELISA. The spleen cell donor BALB/c mouse
was immunized with purified T. simiae procyclic antigens. Culture
supernatant from each of the 48 fusion wells was incubated with one strip of
NC membrane which was previously "dotted" with lxlO5 T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431
(TS) cultured procyclics, and lxlO5 T. vivax IL1392 (TV) cultured
epimastigotes. (a ) represents culture supernatants that contained antibodies
that reacted mainly with T. simiae procyclics; ( □ ) represents culture
supernatants that contained antibodies that reacted specifically with
trypanosomes of the Nannomonas subgenus; ( o ) represents culture
supernatants that contained antibodies that cross-reacted with all the four
trypanosome species that were tested.
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Figure 17
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128
wells (14 and 44) had activity confined mainly to the T. simiae antigen. The
antibodies from well 14 reacted strongly with the T. simiae antigen dot and
very weakly with the T. congolense antigen dot, but not at all with the dots
representing T. brucei or T. vivax. Likewise, the antibodies from well 44
reacted strongly with the T. simiae antigen dot, but showed weak reactivity
with both the T. congolense and the T. brucei antigen dots. It also did not
react with the dot representing the T. vivax antigen. Based on this reactivity,
the cells from those two wells were extensively cloned.
Of the first clones originating out of well 14, only 4 out of 200 tested
positive and all were specific to T. simiae when screened by dot-ELISA
(Figure 18). The clones marked 1, 2 and 3 were selected for further cloning
on the basis of their stronger reactivity. Screening of the re-clones revealed
that only about 1% of the cells continued to secrete the T. simiae specific
MoAb, suggesting that the hybridoma was unstable. It was, therefore, decided
to explore the possibility of isolating some stable hybrids by re-cloning positive
clones several times over. Unfortunately, after several re-cloning attempts, the
trend remained unchanged. As a result, continuous culturing of these cells was
not possible. However, culture supernatants obtained from the earlier cultures
were concentrated by ammonium sulphate precipitation and dialysed. This
fraction was tested by dot-ELISA and found to be active, and used for further
characterization of the antibody and antigen. Some cells from the original well
14 as well as cells from the first and second positive clones were cryopreserved
in liquid nitrogen.
Two hundred first clones were derived from TS7 fusion well 44, but
none of these tested positive when screened by dot-ELISA. Hence, only two
hybrids (one from fusion TS3 and the other from fusion TS7) secreting
antibodies with specific reactivity to T. simiae were ever produced, and none
of these hybrids was stable.
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1 29
Figure 18
Dot-ELISA reactivity of MoAbs secreted by four hybridoma cell clones
obtained from well 14 of cell fusion TS7. Culture supernatant from each
clone was tested for antibody reactivity by incubating with a strip of NC
membrane that was previously "dotted" with lxlO 5 T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431
(TS) cultured procyclics, and lxlO5 T. vivax IL1392 (TV) cultured
epimastigotes. Strips 1, 2, 3 and 4 (Group I) shows the specific reactivity
of the MoAbs secreted by the four hybrid clones, with T. simiae parasites.
The strips shown in Group II illustrate specific reactivity of control MoAbs
in the same test: T. brucei specific MoAb (KT39a); T. vivax specific MoAb
(KD32); Nannomonas specific MoAb (KN4); and T. congolense specific
MoAb (TC6 ).
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1 2 3 4
TCK —
TB -
TS -
T V -
I
Group I
Figure
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K
T
3
9
a
CM
CO CD
Group II
18
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1 30
4.4.4 Reactivity of the New MoAbs Produced
From the 28 fusions that were made, 8 additional hybridomas each of
which secreted a trypanosome species or subspecies specific MoAb were
derived. The specificity of each of the MoAbs was confirmed by testing for
cross-reactivity using the more sensitive Enzyme-linked Immunoelectrotransfer
Blot Technique (Western immunoblot) analysis. The isotypes and reactivity
patterns of the 8 additional MoAbs are listed in Table 12. Three of these
MoAbs [KT39a/18.17 (IgM), KT43/33.32 (IgGj) and KT43/27.32 (IgG2a)]
were T. brucei specific; two [KD32/48.17 (IgGj) and KD37/19.3 (IgGj)] were
T. vivax specific; one [KNS7/14.X(IgG1)] was T. simiae specific; and two
[KN4/13.9(IgG3) and KN5/6.15(IgGj)] were Nannomonas subgenus-specific.
4.4.5 Characterization of MoAbs and the Antigens that they Detect
The remaining sections of this Chapter record the results of the
characterization studies of the MoAbs listed in (Tables 7 and 12), and the
specific antigens that they detected. For purposes of convenience, abbreviated
names of those MoAbs will henceforth be used in the text. Table 13 lists the
full names of the MoAbs and their abbreviated forms.
4.4.6 Immunolocalization of the Species-specific Antigens bound bv the
MoAbs
Immunolocalization studies made by IFAT, revealed that some
trypanosome species-specific antigens bound by the MoAbs were located on
the surface membrane of procyclics or epimastigotes (Figures 19a, 19b and
19c) whilst others were intracytoplasmic (Figure 19d). Table 14 summarizes
the results on the localization of the specific antigens bound by all the MoAbs
as determined by IFAT. Three out of four T. brucei specific antigens localize
to the surface membrane of T. brucei procyclics, whereas one is
intracytoplasmic. Likewise, two out of three T. vivax specific antigens
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1 31
Table 12
Reactivity of the new MoAbs against procyclics or epimastigotes
of different trypanosome species
Monoclonal
Antibody Isotype
T. brucei
*
T. vivax
**
T. congolense
*
T. simiae
*
KT39a/18.17 IgM + - - -
KT43/33.32 IgGi + -
KT43/27.32 I§G2a + -
KD32/48.17 IgGi - + - -
KD37/19.3 IgGj “ +
KNS7/14.X IgGj - - +
KN4/13.9 IgG3 - - + +
KN5/6.15 IgGi - - + +
* procyclics.
** epimastigotes.
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
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Table 13
Abbreviated forms of the names of selected MoAbs
Monoclonal
Antibody
(FULL NAME)
Abbreviated
name Isotype Specificity
TR7/47.37.16 TR7 IgM T. brucei
KT39a/18.17 KT39a IgM T. brucei
KT43/33.32 KT43/33 IgGi T. brucei
KT43/27.32 KT43/27 IgG2a T. brucei
TV8/8.33.42 TV8 IgG3 T. vivax
KD32/48.17 KD32 IgGj T. vivax
KD37/19.3 KD37 IgGi T. vivax
C2 C2 IgGi T. congolense
TC6/42.6.3 TC6 IgGj T. congolense
TC40/30.15.40 TC40 IgM T. congolense
TC39/30.25.95 TC39 IgM T. congolense
KNS7/14.X KNS7 IgGi T. simiae
TC16/5.12.33 TC16 IgGi Nannomonas
TC6/25.25.4 TC6/25 IgG3 Nannomonas
KN4/13.9 KN4 IgG3 Nannomonas
KN5/6.15 KN5 IgGi Nannomonas
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1 33
Figure 19a
Light micrograph of Trypanosoma simiae (KETRI 2431)
procyclics showing surface membrane fluorescence following
incubation with KN4 and anti-mouse-FITC. Photographed at
xlOO magnification.
f = flagella.
m - membrane.
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V * * " '
m
Figure 19a
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1 3 4
Figure 19b
Light micrograph of Trypanosoma vivax (IL1392) epimastigotes
showing surface membrane fluorescence following incubafjfp
with KD32 and anti-mouse-FITC.
Photographed at x 100 magnification.
f = flagella.
m — membrane.
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Figure 19b
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13 5
Figure 19c
Light micrograph of Trypanosoma brucei (IL2616) procyclics
showing surface membrane fluorescence following incubation
with KT39a and anti-mouse-FITC.
Photographed at xlOO magnification.
f — flagella.
m = membrane.
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Figure
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119c
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136
Figure 19d
Light micrograph of Trypanosoma brucei procyclics showing
cytoplasmic staining following incubated with KT43/27 and anti-
mouse-FITC. Photographed at xlOO (A) without and (B) with
fluorescence.
m = membrane,
n - nucleus.
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Figure 19d
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1 37
Table 14
Immunolocalization of the trypanosome species-specific antigens
by indirect fluorescent antibody test (IFAT)
Monoclonal
Antibody Isotype Specificity
Membrane
staining
Cytoplasmic
staining
TR7 IgM T. brucei +
KT39a IgM T. brucei +
KT43/33 IgGj T. brucei +
KT43/27 IgG2a T. brucei +
TV8 IgG3 T. vivax +
KD32 IgGi T. vivax + -
KD37 IgG! T. vivax +
C2 IgGi T. congolense +
TC6 IgGj T. congolense +
TC40 IgM T. congolense +
TC39 IgM T. congolense +
KNS7 IgGi T. simiae - +
TC16 IgGi Nannomonas +
TC6/25 IgG3 Nannomonas +
KN4 IgG3 Nannomonas + -
KN5 IgGi Nannomonas + -
+ = stained.
= not stained.
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1 38
are surface membrane antigens of epimastigotes, and one is intracytoplasmic.
All the T. congolense specific antigens are located within the cytoplasm of
procyclic organisms. The T. simiae specific antigen is also located in the
cytoplasm of procyclics. Unlike the T. congolense specific MoAbs, all the
Nannomonas subgenus-specific antigens are located on the surface membranes
of procyclics.
IFAT analysis, using live trypanosomes, showed that three T. brucei
specific MoAbs (TR7, KT39a and KT43/33); four Nannomonas specific
MoAbs (TC16, TC6/25, KN4 and KN5), and one T. vivax specific MoAb
(KD32) bound antigens on the surface of living trypanosomes.
Characterization of the specific antigens by the Western immunoblot
technique revealed that some of the MoAbs could not work in this assay (Table
15). Each trypanosome species-specific MoAb was assayed on SDS-PAGE
separated antigens of four different trypanosome species (T. brucei, T. vivax,
T. congolense and T. simiae). Of the four T. brucei specific MoAbs, TR7 (an
IgM antibody) bound three protein bands of MW between 21 and 27 kDa
whilst KT43/33 (an IgGj antibody) bound multiple bands ranging between 21
and 47 kDa (Figure 20). The third T. brucei antibody, KT39a, an IgM
isotype, bound a 90 kDa protein band whilst the fourth, KT43/27, an IgG2 a,
did not work in this assay.
The T. vivax specific MoAbs TV8 (IgG3), KD32 (IgG^ and KD37
(IgGj) did not bind any bands in electrophoresed T. vivax bloodstream form or
epimastigote lysates.
C2 and TC6 , both T. congolense specific and of IgGj isotype, bound
protein bands within the same molecular weight range (30-40) kDa. C2 bound
a doublet of protein bands at 30 and 31 kDa and another doublet at 38 and 40
kDa, whilst TC6 bound only one band at 30 kDa. The T. simiae specific
MoAb, KNS7 (IgGj), did not work in the Western immunoblot assay. Also,
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Table 15
The molecular weights of the antigens detected by the
trypanosome species-specific MoAbs as determined
by Western inununoblot analysis
Monoclonal
Antibody Isotype Specificity
Molecular
weight (kDa)
TR7 IgM T. brucei (21, 24, 27)
KT39a IgM T. brucei (90)
KT43 IgG! T. brucei (21 - 47)
KT43/27 !gG2 a T. brucei —
TV8 IgG3 T. vivax _
KD32 IgGi T. vivax --
KD37 IgGi T. vivax --
C2 IgGi T. congolense (30 - 40)
TC6 IgGi T. congolense (30)
TC40 IgM T. congolense (51, 60, 85)
TC39 IgM T. congolense (21 30)
KNS7 IgGi T. simiae —
TC16 IgGj Nannomonas (18, 89)tck (31)ts
TC6/25 IgG3 Nannomonas --
KN4 IgG3 Nannomonas --
KN5 IgGj Nannomonas --
— = antibody does not bind any antigens.
TCK= T. congolense Kilifi type procyclic lysate.
TS = T. simiae procyclic lysate.
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1 4 0
Figure 20
Specific reactivity of the MoAb KT43/33 in the Western immunoblot assay
and the molecular weights of the antigens that it bound. Strip 'A' shows the
reactivity of KT43/33 with antigens in electrophoresed T. brucei IL2616
procyclic lysate. Strips B, C and D contained respectively, electrophoresed
T. congolense, T. simiae and T. vivax antigens. KT43/33 reacted
specifically with T. brucei antigen peptides of molecular weights ranging
between 21 and 47 kDa.
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1 41
three of the four Nannomonas specific MoAbs did not work. However, TC16,
also Nannomonas specific, bound antigens in electrophoresed T. congolense
and T. simiae procyclic extracts at 18, 89 kDa and 31 kDa, respectively (Table
15).
4.4.7 The Biochemical Nature of the Trypanosome Species-specific Antigenic
Determinants
Periodate oxidation of carbohydrate residues and proteinase-K
modification of polypeptide residues were used to study the biochemical nature
of the specific antigenic determinants bound by the MoAbs.
Binding by three of the four T. brucei specific MoAbs was totally
abrogated by treatment with proteinase-K (Table 16). This result suggests that
the antigenic determinants involved are protein in nature. The fourth T. brucei
specific MoAb (KT39a) was only partially affected by proteinase-K digestion,
but not by sodium periodate oxidation, indicating that the antigenic
determinant involved is partly protein and partly either a carbohydrate or a
lipid (Table 16).
Two of the three T. vivax specific MoAbs bound a proteinase-K
sensitive antigenic determinant, whilst the remaining one (TV8 ) was insensitive
to both periodate oxidation and proteinase-K digestion.
All the four Nannomonas as well as the T. simiae specific MoAbs
detected periodate sensitive antigenic determinants in glycoprotein or
glycolipid antigens. In contrast, all the T. congolense specific MoAbs detected
protein antigenic epitopes, as evidenced by their sensitivity to proteinase-K and
insensitivity to periodate oxidation (Table 16).
4.4.8 Distribution of the Specific Antigenic Determinants fEnitones't on
Antigens
The antigen detection sandwich-ELISA was used to study the
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Figure 20
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142
Table 16
The nature of the antigens detected by the trypanosome
species-specific MoAbs as determined by periodate
and proteinase-K digestion
Monoclonal
Antibody Isotype Specificity
Sensitivity to Nature of antigenic
epitopePeriodate Proteinase-K
TR7 IgM T. brucei - + P
KT39a IgM T. brucei - + /- P, C?, L?
KT43 IgGi T. brucei + P
KT43/27 IgG2a T. brucei + P
TV8 IgG3 T. vivax _ _ C?, L?
KD32 IgGj T. vivax - + P
KD37 IgGi T. vivax - + P
C2 IgGi T. congolense - + P
TC6 IgGi T. congolense + P
TC40 IgM T. congolense + P
TC39 IgM T. congolense + P
KNS7 IgGi T. simiae + - C
TC16 IgGi Nannomonas + _ C
TC6/25 IgG3 Nannomonas + - C
KN4 IgG3 Nannomonas + C
KN5 IgGj Nannomonas + C
+ = sensitivity to periodate or proteinase-K.
- = insensitivity to periodate or proteinase-K.
+ = partial sensitivity to proteinase-K.
P = protein antigenic determinant.
C = carbohydrate antigenic determinant.
L = lipid antigenic determinant.
? = not certain.
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143
distribution of trypanosome species-specific antigenic epitopes on antigens.
In these experiments, MoAbs specific to each trypanosome species or
subgenus were placed into separate groups. Each antibody in a group was
used to trap the antigen(s) on which its specific epitope is expressed. The
trapped antigen(s) was then revealed by HRPO conjugate of each antibody in
the group in separate experiments.
The results obtained for the T. brucei specific MoAbs are shown in
Table 17a. When the MoAb TR7 was used to capture the antigen(s) on
which its specific epitope is expressed, it was possible to reveal the captured
antigen(s) using the conjugates of all the T. brucei specific MoAbs,
including the homologous conjugate of TR7 (Table 17a). This meant that
the TR7 specific antigenic epitope is repeated on the captured antigen(s), so
that when the antigen(s) was trapped by TR7 the same antigen(s) could be
revealed by that MoAb's conjugate. Also, the result suggested that the
antigen(s) captured by TR7 expressed all the antigenic epitopes bound by the
other T. brucei specific MoAbs. Similar results were recorded when KT39a
was used as capture antibody (Table 17a). The results also showed that the
IgM MoAbs were better capture antibodies compared with the IgG's. This
was clearly shown by the strong reactivity of the conjugate of
KT43/33(IgGi) with the antigen(s) captured by KT39a(IgM), and yet the
absence of reactivity when the conjugate of KT39a was used to reveal the
antigen(s) captured by KT43/33 (Table 17a). Furthermore, it was evident
from the pattern of reactivity that KT43/33 was the best antibody for
revealing captured antigen (Table 17a).
Each T. congolense MoAb captured antigen(s) that could be revealed
by conjugates of all the others including that of the capture MoAb (Table
17b). This result suggested that the antigen(s) captured by these MoAbs is
likely to be the same. Also, the ability of the MoAbs to capture their
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144
Table 17a
Relationship between the T. brucei specific
MoAbs as revealed by sandwich-ELISA
Reveal antibody conjugate
Capture -----------------------------------------------------------------
antibody TR7 KT39a KT43/33 KT43/27
TR7(IgM) + + + + + + + + +
KT39a(IgM) + + + + + + + +
KT43/33(IgG!) + - + +
KT43/27(IgG2a) +
+ = ability of MoAb conjugate to reveal captured antigen.
- = MoAb conjugate unable to reveal captured antigen.
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Table 17b
Relationship between the T. congolense specific MoAbs as
revealed by sandwich-ELISA
Capture
antibody
Reveal antibody conjugate
C2 TC6 TC40 TC39
C2 + + + + +
TC6 + + + + +
TC40 + + + + + +
TC39 + + + + + + + +
+ = ability of MoAb conjugate to reveal captured antigen.
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146
respective antigens and reveal them by their own conjugates, indicated that the
antigenic determinants are repeated on the antigen(s).
As shown in Table 17c, the Nannomonas subgenus-specific MoAb
TC6/25 captured antigen(s) that could be detected by conjugates of itself, KN4
and KN5 but not TC16. Likewise, the antigen(s) captured by TC16 could not
be revealed by any of the conjugates other than that of TC16 itself. These
results indicate that the antigenic epitope bound by TCI6 is on a different
antigen. It is also seen from Table 17c that both KN4 and KN5 captured
antigen(s) that could not be revealed by their own conjugates. This
observation suggests that the epitopes bound by these MoAbs (KN4 and KN5)
are not significantly repetitive on the respective antigens.
The T. vivax MoAb, TV8 , captured antigen(s) that could be revealed
by conjugates of each of the three T. vivax MoAbs (Table 17d), suggesting that
the antigenic determinants bound by all these MoAbs are distributed on the
same antigen(s). KD32 captured antigen(s) that could be revealed by its own
conjugate, but weakly by conjugates of TVS or KD37, yet the same KD32
conjugate could reveal very well the antigen(s) captured by TVS. This
suggests that the weak reactivity of the TV8 conjugate may be due to altered
epitope accessibility due to conformational changes in the antigen, brought
about by the binding to KD32.
4.4.9 Inhibition ELISA
To further elucidate the relationship between the specific epitopes
bound by the different MoAbs (section 4.4.8), experiments were conducted to
examine the effect of the binding of one MoAb on binding by another, using
micro-plate-based inhibition ELISA.
The results obtained showed that the T. brucei specific MoAbs,
KT43/33 and KT43/27 could not inhibit each other, showing that the two
epitopes were different. However, two other T. brucei specific MoAbs
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Table 17c
Relationship between the Nannomonas specific MoAbs as
revealed by sandwich-ELISA
Capture
antibody
Reveal antibody conjugate
TC6/25 TCI 6 KN4 KN5
TC6/25 + - + +
TC16 - + -
KN4 + - - +
KN5 + +
+ = ability of MoAb conjugate to reveal captured antigen.
- = MoAb conjugate unable to reveal captured antigen.
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Table 17d
Relationship between the T. vivax specific MoAbs as revealed by
sandwich-ELISA
Capture
antibody
Reveal antibody conjugate
TV8 KD32 KD37
TV8 + + + + +
KD32 + + ±
KD37 + +
+ = ability of MoAb conjugate to reveal captured antigen.
= MoAb conjugate unable to reveal captured antigen.
± = very weak reactivity.
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(KT39a and TR7) inhibited each others binding, suggesting that the two
MoAbs are directed at the same epitope.
Each of the four T. congolense specific MoAbs (C2, TC6 , TC39 and
TC40) was able to inhibit the binding of the others.
4.4.10 Reactivity of the Various MoAbs with Different Trypanosome Stocks
and Clones
The aim of the experiments described here was to determine the
suitability of the trypanosome species-specific MoAbs as diagnostic reagents.
This assessment was based on their ability to react with trypanosomes from
different geographical areas.
All the trypanosome stocks and clones used in the present study, are
listed, together with their places of origin, in Table 18.
With the exception of KT43/27, the T. brucei specific MoAbs detected
all the different developmental stages of T. brucei organisms that were tested
(Table 19). The reactivity patterns indicate that KT43/27 was able to detect all
the in vitro propagated T. brucei procyclic organisms. However, the same
MoAb could not detect T. brucei bloodstream forms or insect forms from
tsetse gut or salivary glands.
Studies with the T. vivax specific MoAbs showed that TV8 and KD37
could detect all the epimastigotes and blood stream forms tested (Table 20).
Thus, in addition to East and West African T. vivax, these two MoAbs
detected IL3841 which originated from Colombia, South America. These
MoAbs also detected T. vivax insect forms of IL3096 from tsetse mouthparts.
In contrast, KD32 which was derived against epimastigotes of West African T.
vivax (IL1392), was unable to detect bloodstream forms of IL1392, IL2160
and IL3841, even though the same MoAb detected bloodstream forms of
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l aoie 18: Trypanosom e stocks and clones from d ifferen t geographical a rea s used in determ in ing
th e range o f reactiv ity o f the trypanosom e species-specific M oAbs
: ■’ , 150
Species Trypanosome
stock/clone
Origin
T. congolense *K/83/IL/97/2 Kilifi, Kenya (K)
K/82/IL/60/1 Kilifi, Kenya (K)
IL3779 Nguruman, Kenya (S)
CP81 Taita, Kenya (S)
*ILC49 Transmara, Kenya (S)
*IL13-E3 Busoga, Uganda (S)
*IL2079 Serengeti, Tanzania (S)
*IL1180 Serengeti, Tanzania (S)
IL3900 Bobodioulasso, Burkina Faso (R)
*IL3274 Banankeledaga, Burkina Faso (R)
MSUS/LR/77/TSW103 Duoplay, L iberia (K)
MOVS/KE/81/WG84 Matuga, Kenya (R)
MBOI/NG/60/1-148 Donga Valley, N igeria (S)
T. simiae KETRI 2431 Ukunda, Kenya
*TS1 Ukunda, Kenya
*TS4 Ukunda, Kenya
IL3815 Ukunda, Kenya
T. vivax IL3895 Kipini, Kenya
IL2005 Teso, Uganda
IL1392 Zaria, Nigeria
IL2160 Zaria, Nigeria
IL3096 Zaria, Nigeria
*ILDat 1.9 Zaria, N igeria
*IL3841 Lorica, Colombia
T. b. brucei CP 2137 Nairobi, Kenya
M iTat 1.2 Lugala, Uganda
CP 547/R Jilib, Somalia
IL2616 Serengeti, Tanzania
IL375 Serengeti, Tanzania
IL3579 Serengeti, Tanzania
T. b. gambiense TREU 1442 Nigeria
Th-17/78 E(020) Cote d 'Ivoire
T. b. rhodesiense IL1984 Lugala, Uganda
IL1478 Lambwe Valley, Kenya
T. grayi GPAG/GM/88/BAN1 Bansang, The Gambia
* = clone.
K = K ilifi type.
S = savannah type.
R = riverine-forest type.
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1 5 1
Table 19: Reactivity of the T. brucei specific MoAbs with different stocks and clones
of T. brucei as defined by dot-ELISA
Monoclonal
antibody
IL2616
(Proc)
Th-17/87
(Proc)
TREU-1442
(Proc)
M iT atl.2
(Proc)
IL1984
(Proc)
IL1478
(Proc)
CP2137
(b/d)
CP547/R
(b/d)
IL375
(i/f)G
IL375
(i/f)SG
IL3579
(i/f)G
IL3579
(i/f)SG
TR7 + + + + + + + + + + + +
KT39a + + + + + + + + + + + +
KT43/33 + + + + + + + + + + + +
KT43/27 + + + + + - - - - - - -
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
(Proc) = procyclic forms propagated in vitro.
(b/d) = bloodstream forms propagated in vivo.
(i/f)G = insect forms from the gut.
(i/f)SG = insect forms from the salivary glands.
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Table 20: Reactivity of the T. vivax specific MoAbs with different stocks and clones
of T. vivax as defined by dot-ELISA
Monoclonal
antibody
IL1392
(Epis)
IL1392
(b/d)
IL3895
(Epis)
ILDatl.9
(Epis)
IL2160
(b/d)
IL2005
(b/d)
IL3841
(b/d)
IL3096
(i/f)MP
TVS + + + + + + + +
KD32 + - + + - + - +
KD37 + + + + + + + n.t.
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
(Epis) = epimastigote forms propagated in vitro.
(b/d) = bloodstream forms propagated in vivo.
(i/f)MP = insect forms from the mouthparts.
n.t =not tested.
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IL2005 (Table 20), indicating a differential expression of the epitope involved
in insect stages of the parasite, and in bloodstream forms of some stocks
(KD37 was not tested against the insect forms of IL3096 because the MoAb
was derived late in the course of these studies).
Each of the four T. congolense specific MoAbs detected all the
different stocks and clones of T. congolense that were tested, regardless of the
developmental stages of the organism (Table 21).
The reactivity of the Nannomonas specific MoAbs is given in Table 22.
The four specific MoAbs detected all the epimastigote and tsetse gut forms of
T. congolense, as well as the procyclics of T. congolense and T. simiae. The
reactivity of these MoAbs with bloodstream forms, however, presented a
different picture. Whilst KN5 detected all the T. congolense bloodstream
forms that were tested, TC6/25, TC16 and KN4 were unable to detect the
bloodstream forms of IL2079, and CP81. Yet, the same MoAbs (TC6/25,
TC16 and KN4) could detect bloodstream forms of IL1180, IL3779 and
IL3900, suggesting that the antigenic epitopes detected by these MoAbs were
not expressed in the bloodstream forms of all the different stocks of T.
congolense organisms.
All the specific MoAbs were screened against T. grayi procyclics. The
object of this exercise was to determine whether any of the MoAbs would
cross-react with T. grayi, since it also infects tsetse flies. None of the MoAbs
reacted with the T. grayi parasites when tested with the dot-ELISA (Figure
21). The results of the screening of TC6/25, KN4, TC6/42, KT39a and KD32
on T. grayi, and T. congolense (savannah type, riverine/forest type and Kilifi
type) are summarized in Figure 21. As it is indicated, the T. congolense
MoAb (TC6 ) and Nannomonas MoAbs (TC6/25 and KN4) detected all the
different types of T. congolense that were tested.
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Table 21: Reactivity of the T. congolense specific monoclonal antibodies with different stocks and clones
of T. congolense as defined by dot-ELISA
Monoclonal
antibody
IL/60/1
(Proc)
IL/97/2
(Proc)
IL2079
(Epis)
IL3900
(b/d)
IL2079
(b/d)
ELC49
(b/d)
CP81
(Epis)
CP81
(b/d)*
CP81
(i/f)G
IL1180
(b/d)
IL1180
(i/f)G
EL13-E3
(i/f)G
IL3274
(i/f)G
IL3779
(i/f)G
MOVS
(Proc)
MBOI
(Proc)
MSUS
(Proc)
C2 + + + + + + + + + + + + + + + + +
TC39 + + + + + + + + + + + + + + + + +
TC40 + + + + + + + + + + + + + + + + +
TC6 + + + + + + + + + + + + + + + + +
+ = antibody reacts with tiypanosomes.
IL/60/1 = K/82/IL/60/1.
IL/97/2 = K/83/IL/97/2.
(Proc) = procyclic forms propagated in vitro.
(Epis) = epimastigote forms propagated in vitro.
(b/d)* = bloodstream forms propagated in vitro.
(b/d) = bloodstream forms propagated in vivo.
(i/f)G - insect forms from the gut.
MOVS = MOVS/KE/81/WG84.
MBOI = MBOI/NG/60/1-148.
MSUS = MSUS/LR/77/TSW103.
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1 55
Table 22: Reactivity of the Nannomonas specific MoAbs with different stocks and clones
of T. congolense and T. simiae as defined by dot-ELISA
Monoclonal
antibody
IL/97/2
(Proc)
IL/60/2
(Proc)
TScl
(Proc)
TSc4
(Proc)
IL2079
(Epis)
IL2079
(b/d)*
CP81
(Epis)
CP81
(b/d)*
CP81
(i/f)G
IL1180
(b/d)
IL1180
(i/f)G
IL3779
(b/d)
IL3779
(i/f)G
IL3900
(b/d)
CP813
(i/f)G
IL3274
(i/f)G
MOVS
(Proc)
MBOI
(Proc)
MSUS
(Proc)
TC6/25 + + •+ + + - + - + + + + + + + + + + +
TC16 + + + + + - + - + + + + + + + + + + +
KN4 + + + + + - + - + + + + + + + + + + +
KN5 + + + + + + + + + + + + + + + + + + +
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
IL/60/1 = K/82/IL/60/1.
IL/97/2 = K/83/IL/97/2.
(Proc) = procyclic forms propagated in vitro.
(Epis) = epimastigote forms propagated in vitro.
(b/d)* = bloodstream forms propagated in vitro.
(b/d) = bloodstream forms propagated in vivo.
(i/f)G = insect forms from the gut.
(i/f)SG = insect forms from the salivary glands.
MOVS = MOVS/KE/81/WG84.
MBOI = MBOI/NG/60/1-148.
MSUS = MSUS/LR/77/TSW103.
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Figure 21
Reactivity of some trypanosome species-specific MoAbs against lxlO4
parasites/dot of Trypanosoma grayi (TG), and T. congolense savannah type
(TCST), K ilifi type (TCK7) anci 3X103 forest type (K T 1) in the dot-ELISA.
The control antigens consisted of lxlO 5 parasites per dot of T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431
(TS) cultured procyclics, and lxlO5 T. vivax IL1392 (TV) cultured
epimastigotes. Strip 'C' was a conjugate control; not incubated with
specific MoAb. KD32 and KT39a were respectively, T. vivax and T. brucei
specific MoAbs. TC6/25 and KN4 were Nannomonas subgenus-specific,
and TC6 was a T. congolense specific MoAb. Note that none of the MoAbs
reacted with T. grayi.
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T.G
T.C ST
T.C FT
T.CKT
TB -|
TS
TV -
T C K - •
o
TC
62
5
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COo
H
CO
0 5
CO
\—
*
CM
CO
D
*
Figure 21
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1 5 7
The main aim of this study was to obtain trypanosome species-specific
MoAbs that could be useful in developing a field applicable assay for detecting
and differentiating trypanosome species in the vector (Glossina spp.).
It had been previously shown that T. brucei, T. vivax, T. congolense
and the Nannomonas subgenus, possess species-specific and/or subgenus
specific antigens (Parish, Morrison and Pearson 1985, Richardson et al., 1986;
Nantulya et al., 1987).
The initial step, therefore, was to re-examine the specificity and
sensitivity of the extant trypanosome species-specific MoAbs that were
available at ILRAD, to select some for further study and then to produce
additional MoAbs, if necessary, for eventual detection and differentiation of
vector-borne trypanosome species. These studies were made using IFAT,
micro-plate ELISA, dot-ELISA and Western immunoblot analysis, and the
selection criteria were as follows: (1 ) specificity as determined in all the assay
systems, (2 ) sensitivity in terms of the minimum number of insect form
trypanosomes that can be detected in the dot-ELISA and (3) the ability of a
MoAb to bind antigens in the Western immunoblot assay. A series of MoAbs
were also produced against insect forms of T. brucei, T. vivax, T. simiae and
the Nannomonas subgenus as indicated, and each of these MoAbs was screened
using IFAT, micro-plate ELISA, dot-ELISA and Western immunoblot assays,
and their specific reactivity with the trypanosome species against which they
were derived established.
Data presented in this Chapter shows that immunization of BALB/c
mice with trypanosome antigens purified according to the method described by
(Ijagbone et al., 1989) increased the fusion success rate as well as the chances
of obtaining hybridomas that secreted trypanosome species-specific MoAbs.
4.5 Discussion
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Although this method of antigen purification was originally described for the
purpose of improving serological diagnosis of trypanosomiasis, it has
successfully been used in this study to produce T. brucei specific MoAbs
(KT43/33, KT43/27), T. vivax specific MoAb (KD37) and T. simiae specific
MoAb (KNS7). It has also been demonstrated in this study that the dot-ELISA
procedure is suitable for screening the products of cell fusions, especially
where it is desired to screen MoAb against a large number of different antigens
simultaneously. This suggestion is in agreement with the findings of Hawkes,
Niday and Gordon (1982), that the NC membrane-based dot-ELISA was well
suited for screening of MoAbs.
Two different hybridomas that secreted T. simiae specific MoAb were
derived. However, both hybridomas were not stable since the ability to secrete
the specific MoAb was lost when grown in continuous culture. This
phenomenon has indeed been reported by Pearson, Pinder, Raelants, Kar,
Lundin, Mayor-Withey and Hewett (1980), the underlying reason having been
attributed to the loss of chromosome chains (Goding, 1980). Hybrid cells are
unstable and tend to lose chromosomes especially during the early cell
divisions following fusion (Goding, 1980). It is, therefore, possible for hybrid
cells to lose one or more of the chromosomes that encode the genes for the
expression of immunoglobulins. The stability of the cells increases with
chromosome loss, and eventually the cells become relatively stable.
Consequently, it has been established that recloning hybrid cells should
produce higher cloning efficiency and increase numbers of active cells. This
was, however, not the case with the T. simiae hybridomas reported here. This
observation may be explained by the fact that the chances of a hybrid cell
losing immunoglobulin genes never really ceases. Conditions necessary to
minimise the occurrence of unstable hybrid cells include; a suitable
immunization schedule; the state of health of the cells used in cell fusion; rapid
identification of MoAb secreting cells; early cell cloning and the use of feeder
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cells; and the choice of FBS used in the preparation of medium (reviewed by
Goding, 1980). Though these conditions were closely followed, the two T.
simiae specific MoAb secreting hybridomas were not stable. This occurrence
is, however, not the first, since it has been reported that some hybrids are
inherently more stable than others. Hence even with intensive care and
repeated cloning, some hybrid cells will lose production (Goding, 1980). The
results, however, show that T. simiae specific antigens exist at least in the
procyclic stage of that species, and that these antigens are sufficiently
immunogenic and can be utilized in traditional cell fusion methods for the
production of T. simiae specific MoAbs. This is very useful information since
no T. simiae specific MoAb has been reported in the literature. The low
frequency in occurrence of MoAbs that are specific for T. simiae compared
with T. congolense may be attributed to fewer or less immunogenic T. simiae
specific antigens.
IFAT studies carried out to immunolocalize the antigens detected by the
MoAbs, revealed that antigens that define T. brucei specificity were not
restricted to the cell membrane. Thus, the MoAb KT43/27 was also shown to
bind antigens located in the cytoplasm of T. brucei procyclics, and membrane
bound T. brucei specific antigens have been reported earlier (Nantulya et al.,
1987). Despite the obvious differences in location, it was not possible to
determine whether the antigenic molecule bound by KT43/27 was different
from that bound by any of the other T. brucei specific MoAbs.
Parish, Morrison and Pearson (1985) reported the identification of an
antigen specific to T. congolense using MoAbs. This MoAb, TC6/42.6.4, was
shown to bind a membrane antigen that was made accessible to the antibody
following treatment of bloodstream trypanosomes with acetone. In this study,
it was shown using IFAT, that the four T. congolense specific MoAbs tested
did not bind to live procyclic trypanosomes, unlike the Nannomonas subgenus-
specific MoAbs which all bound to live procyclic trypanosome membranes. It
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has also^sliown using IFAT that the T. simiae specific MoAb did not bind to
live T. simiae procyclics.
All the MoAbs produced reacted specifically with the trypanosome
species against which they were derived when tested in the IFAT, micro-plate
ELISA and the dot-ELISA. However, not all of them bound their respective
antigens with the Western immunoblot analysis, whether as MoAb in culture
supernatants or as purified fractions. This, perhaps, was not surprising, since
in SDS-PAGE analysis, antigen samples were heated to 100°C in SDS in the
presence of a reducing agent, a process that could lead to the denaturation of
antigem (Su and Prestwood, 1990). Also, the conformation of the antigens
after they are transferred to NC membrane is not known. Moreover, it had
been reported that the reactivity of immune serum made against native antigens
is usually much weaker when tested against denatured antigens (Amon, 1973).
Chaicumpa, Ruangkunapom, Kalambaheti, Limavongpranee, Kitikoon,
Khusmith, Pungpak, Cbongsa-Nguan and Sommani (1991) had also pointed
out that antisera against native proteins normally contain some clonal products
which recognize the denatured antigens, allowing the Western immunoblot to
function. In contrast, MoAbs against native antigens may or may not bind the
denatured products. It is therefore expected that many clones of MoAb may
fail to bind denatured antigens (Goding, 1983), which could explain why the
T. simiae KNS7 failed to bind any antigens with the Western immunoblot
assay. This inability of KNS7 to bind the specific antigens, did not allow
purification of that antigen by electro-elution. As a result, it would have been
necessary to resort to immunoaffinity or immuno-precipitation techniques for
isolation of the antigen. However, time did not permit such a study to be
conducted.
The T. brucei MoAbs TR7 and KT43/33; T. congolense MoAbs (C2,
TC39 and TC40); and Nannomonas MoAb TC16, reacted with multiple bands
in the Western immunoblot assay. This observation is not new, since, it has
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been reported that certain MoAbs often show variable staining intensities or
multiple band staining (Braun, Pereira, Norrid and Roizman, 1983; Mandrell
and Zollinger, 1984; Steinemann, Fenner, Binz and Parish, 1984; Turner,
1983). The case of TR7 and KT39a may be explained by the findings obtained
from micro-plate based antigen capture studies, which indicated that the two T.
brucei specific MoAbs bound repeated determinants which possibly were
located in multiple peptide bands. It has indeed been reported that the usual
treatment of antigens with a reducing agent (sodium dodecyl sulphate) and heat
in the Western immunoblot assay, leads to the breakdown of antigens into
several peptides (Chung, 1987). Moreover, autodegradation of the antigens
could produce a similar effect. Both of these processes could lead to the
distribution of the antigenic epitopes detected by MoAbs on several peptides of
varying molecular weights, and thus lead to multiple band staining (Chaicumpa
et al. , 1991). It has also been argued that MoAbs that reveal multiple bands in
the Western immunoblot assay may be binding common sequences or repeated
determinants (Bers and Garfin, 1985; Chaicumpa, Thin-inta, Khusmith,
Tapchaisri, Echeverria, Kalamba-heti and Chongsa-Nguan, 1988) in different
polypeptide chains produced by denaturing conditions.
The studies described in this Chapter also showed that each of the four
T. congolense specific MoAbs captured antigen molecules that could be
revealed by conjugates of all the others. These results thus suggest that the
antigenic epitopes for those MoAbs were located on the same antigen
molecule(s). Furthermore, inhibition ELISA studies which showed that each
of those T. congolense specific MoAbs could inhibit binding by any of the
others, suggested two possibilities: (1 ) that the antigenic epitope(s) recognised
by all those four MoAbs was the same, or (2) that the antigenic epitopes
detected by these MoAbs were not necessarily the same, instead they might be
located so close to one another in a way that binding by one MoAb led to
interference in the binding of another MoAb.
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Proteinase-K digestion of peptide residues and periodate oxidation of
carbohydrate residues have been described and used by several workers in the
characterization of the antigens detected by MoAbs (Bright, Chen, Flebbe, Lei
and Morrison, 1990; Woodward et al., 1985). Investigations of the
biochemical nature of the epitope specificities of the MoAbs produced had
revealed that three of the T. brucei MoAbs bound protein specific antigenic
determinants, since their binding was completely abrogated by proteolysis.
Binding by the fourth T. brucei MoAb KT39a was, however, only partially
affected by proteolysis, suggesting that the antigenic determinant was at least
partly protein in nature. Binding by that same antibody was not affected by
periodate oxidation of carbohydrate residues. It was, however, difficult to rule
out any part played by carbohydrate. This is because according to Woodward
et al. (1985), antigenic determinants affected by periodate oxidation are
carbohydrates in glycoprotein or glycolipids, yet some carbohydrate residues
are insensitive to periodate oxidation. It is, therefore, likely that KT39a bound
a glycoprotein or a lipoprotein. The studies also showed that the four T.
congolense MoAbs bound protein antigenic determinants, whilst the four
Nannomonas subgenus-specific MoAbs were directed at carbohydrate antigenic
determinants.
The only Nannomonas specific MoAb (TC16) that bound antigens with
the Western immunoblot assay, was also shown to bind an antigenic
determinant which was different from the common determinant bound by the
other three Nannomonas MoAbs. This meant that there were at least two
different antigenic determinants that defined Nannomonas species specificity,
both of which were of carbohydrate nature.
Although none of the T. vivax specific MoAbs could bind antigens in
the Western immunoblot assay, the results obtained using micro-plate ELISA
revealed that the antigenic determinant bound by TV8 was different from that
bound by KD32. This observation is supported by the finding that TV8
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reacted with the bloodstream forms of the South American T. vivax IL3841,
whilst KD32 could not. Also, the determinant bound by TV8 was insensitive
to proteinase-K digestion whilst that bound by KD32 was sensitive to that
treatment. It may be further argued that the antigenic determinants bound by
TV8 was different from that bound by KD37. This is because unlike TV8 , the
KD37 epitope was sensitive to proteolysis, and yet both MoAbs detected the
bloodstream forms of IL3841. These findings could mean that there were at
least three different antigenic determinants that express T. vivax species
specificity, two of which were proteins and the other of carbohydrate or lipid
nature.
Studies on the reactivity of the trypanosome species-specific MoAbs
with trypanosome stocks isolated from different geographical areas, have
clearly shown that the reactivity of some of the MoAbs was indeed broad. The
studies showed that two of the T. vivax specific MoAbs, TV8 and KD37, were
capable of detecting T. vivax originating from East and West Africa, as well as
from South America. All the T. congolense species-specific and Nannomonas
subgenus-specific MoAbs were also shown to be capable of detecting the three
different types of T. congolense (savannah, riverine-forest and Kilifi types)
tested. In the application of DNA probes for the differentiation of
trypanosome species, the absence of a probe that could hybridize with all the
different types of T. congolense has been a major limitation (Kukla et al.,
1987). It is important to mention here, though, that the recently identified
Tsavo type T. congolense was not tested in this study because of failure to
obtain suitable samples.
Another important observation was that some MoAbs showed a stage
specificity in their reactivity. Of the Nannomonas specific MoAbs, for
instance, only KN5 detected all the different T. congolense bloodstream forms
tested. The others could not react with the bloodstream stages of two T.
congolense stocks even though they reacted with the insect stages of the same
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stocks. It was also shown that unlike TV8 and KD37, the T. vivax specific
MoAb KD32 reacted with the vector stages but not the bloodstream forms of
the parasite. These observations were not unusual since MoAbs that were
specific to the procyclic stages of trypanosomes had been reported earlier
(Richardson et al., 1986). A second point was that one of the T. brucei
specific MoAbs, KT43/27, failed to react with some in vitro propagated T.
brucei procyclics and insect forms from the gut and the salivary glands of
tsetse infected with some T. brucei stocks. Moreover, KT43/27 could not
react with bloodstream forms isolated from laboratory rodents (mice and rats)
infected with two different T. brucei stocks. This observation suggests that the
antigenic epitope bound by KT43/27 might not be expressed in the procyclic as
well as other stages of some T. brucei stocks. However, it should be noted
that of the four T. brucei MoAbs, only KT43/27 could bind cytoplasmic
antigens; and this was the only T. brucei specific MoAb that did not bind any
antigens with the Western immunoblot assay. The internal localization of the
antigen detected by KT43/27 suggested that, of all the T. brucei specific
MoAbs, it was the one that would most likely be affected by degradative
substances such as proteases and lysozymes from the parasites during sample
preparation. It is also likely that the dot-ELISA technique was not suitable for
detecting the antigen targeted by KT43/27, possibly because when applied to
NC membrane, the antigen could bind in such a way that the epitope detected
by KT43/27 was concealed.
These findings indicated that, apart from KT43/27, the MoAbs
included in this study were likely to be useful in the development of MoAb-
based assays for the detection and differentiation of procyclic forms of African
trypanosomes, propagated in vitro as well as those in the vector (Glossina
spp.). In addition, some of the newly derived MoAbs could be useful in
studies aimed at diagnosing trypanosomiasis in the vertebrate host. The
usefulness of the MoAbs as diagnostic reagents in detecting and differentiating
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between culture derived vector stage trypanosome species, would be the
subject of investigation in the next Chapter, as a prelude to the diagnosis of
infections in the vector.
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CHAPTER 5
166
DIFFERENTIATION BETWEEN IN VITRO PROPAGATED
INSECT-STAGE TRYPANOSOME SPECIES
USING DOT-ELISA
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A sensitive and specific nitrocellulose (NC) membrane-based dot-
ELISA, utilizing a panel of monoclonal antibodies (MoAbs), was developed
for differentiation between in vitro derived procyclic forms of Trypanosoma
brucei, T. congolense and T. simiae, and epimastigotes of T. vivax.
Trypanosomes were applied onto NC membrane in dots and probed with
unlabelled trypanosome species-specific MoAb. Bound MoAb was revealed by
enzyme labelled anti-mouse IgG and precipitable chromogenic substrate. The
assay detected the afore-mentioned trypanosome species in both single and
artificially mixed preparations. Six T. brucei, four T. vivax, seven T.
congolense and three T. simiae procyclic stocks and clones from different
geographical areas were tested and identified using the specific MoAbs in the
dot-ELISA which had a specificity greater than 99.9%. Some of the T.
brucei, T. congolense and Nannomonas specific MoAbs could detect as low as
10 trypanosomes per dot, whilst one T. vivax MoAb was able to detect a
minimum of 100 trypanosomes per dot in mono-species preparations. A
concentration of lxlO4 trypanosomes//xl/dot was eventually determined as ideal
for testing in the dot-ELISA. Antigen dots made from the different
trypanosome species, and stored at 4°C under desiccated conditions did not
show any loss in activity in up to 90 days. However, when stored under
similar conditions at room temperature (17-26°C), the T. congolense specific
antigen remained unaffected up to 60 days, and then showed decreased activity
when tested on day 90. The ability of the dot-ELISA to distinguish between
the various stocks and clones of trypanosomes that were used, and the ability
to identify the constituent species in mixed trypanosome preparations, indicated
that this test might prove useful as a laboratory tool for the determination of
the identity of in vitro derived procyclic trypanosomes. Also, the dot-ELISA
5.1 Summary
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developed could be a useful first step in the development of a field applicable
MoAb-based assay for diagnosis of trypanosome infections in the tsetse fly.
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In the studies described in this Chapter, the trypanosome species and
subgenus-specific MoAbs derived against in vitro propagated procyclics of T.
brucei, T. congolense and T. simiae, and epimastigotes of T. vivax, were
employed in the development and standardization of a simple, sensitive and
specific NC membrane-based dot-ELISA for the differentiation of readily
available in vitro cultivated forms of those trypanosome species.
It was intended to ultimately apply the assay to the diagnosis of
trypanosome infections in infected tsetse flies. The feasibility of this approach
stems from the finding that procyclic tsetse midgut forms and culture forms of
the African trypanosomes express similar antigens (Richardson et al., 1986;
Pearson, Moloo and Jenni, 1987). The NC membrane-based dot-ELISA was
selected for this application for two reasons. Firstly, it offered the best
opportunity for the development of a diagnostic test that is simple and easy to
perform, in addition to being both sensitive and specific. Secondly, such an
assay could be easily modified for field diagnosis of trypanosome infections in
the tsetse fly (Glossina spp.).
Furthermore, the introduction of a simple, specific and sensitive assay
capable of detecting and differentiating between in vitro propagated
trypanosome species, would facilitate other studies. For example, the search
for a solution to the trypanosomiasis problem has necessitated extensive studies
into the biology, biochemistry, response to chemotherapy, antigenic
constitution, as well as characterization of the causative organisms. To
facilitate these studies, techniques have been developed for in vitro culture of
various developmental stages of the parasite. Thus the procyclic,
epimastigote, metacyclic and the bloodstream forms of trypanosomes can be
propagated in large numbers in artificial cultures in vitro (Hirumi, Doyle and
Hirumi, 1977; Ross, Gray, Taylor and Luckins, 1985; Zweygarth, Gumm,
5.2 Introduction
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Gray, Cheruiyot, Webster and Kaminsky, 1989; Hirumi, Nelson and Hirumi,
1983; Baltz, Baltz, Giroud and Crocket, 1985; Bran and Schonenberger,
1979). This has made it possible to conduct trypanosome drug sensitivity
analysis in vitro (Kaminsky and Zweygarth, 1989; Kaminsky, Chuma and
Zweygarth, 1989; Ross and Taylor, 1990). Moreover, in vitro culturing of
trypanosomes has made possible, the isolation of the parasites from various
organs of infected tsetse flies into artificial cultures (Cunningham, 1977;
Trager, 1959; Gumm, 1991; Gray, Cunningham, Gardiner, Taylor and
Luckins, 1981).
This unlimited opportunity to grow freshly isolated trypanosomes in
culture, and the ability to cryopreserve samples of such organisms, calls for
the availability of simple reliable techniques for ascertaining the species of
trypanosomes present in in vitro cultures. Two diagnostic techniques, DNA
hybridization analysis and isoenzyme characterization, are currently used for
this purpose (Gashumba, Gibson and Opiyo, 1986; Kukla et al., 1987). These
methods are, however, not simple enough and cannot be performed in most
laboratories. The ability of a simple MoAb-based dot-ELISA to detect and
differentiate between culture derived procyclic trypanosomes, is reported.
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5.3.1 In vitro cultivation of trypanosomes
5.3.1.1 Cultivation of procyclic forms
Procyclic trypanosomes were cultivated in culture using complete-
(SM) medium filtered through 0.2 to 0.45/xm membrane bottle filter (Costar).
Cryopreserved T. brucei, T. congolense and T. simiae procyclic trypanosomes
were resuscitated into culture medium and the cultures initiated as described
earlier (section 3.2.1). The trypanosomes were allowed to multiply until the
trypanosome density reached approximately lx l0 7 /ml. The T. brucei IL2616
procyclics were well adapted to culture. Maintenance of this trypanosome
stock was achieved by removal of all but 1ml of the lx l 0 7/ml trypanosome
suspension from a culture flask and replacement with fresh medium in
quantities of up to 20 times the residual volume. However, the T. congolense
clone K/83/IL/97/2 and T. simiae clones TS1 and TS4 procyclics were poorly
adapted to culture. These were maintained by removal of half of the lx l0 7/ml
procyclic suspension and replacement with an equal volume of new medium
usually thrice weekly. The trypanosomes were grown in 15-20ml volumes in
75cm2 flasks (Costar; Falcon). The cultures were gassed whenever the flasks
were opened. Flasks were closed tightly soon after gassing and incubated at
27°C. Old flasks that had been used for maintaining over six passages were
replaced with new ones.
5.3.1.2 Cultivation of epimastigote forms
In vitro propagation of T. vivax epimastigotes, East African (EA)
stock IL2337 and West African (WA) stock IL1392 were achieved by
transformation of freshly isolated bloodstream forms into epimastigotes at
27°C in Iscove's modified Dulbecco's minimum essential medium (M-
DMEM,; Flow Laboratories, Irvine, Scotland, UK) that had transferrin,
5.3 Materials and methods
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soybean lecithin, and bovine serum albumin incorporated in it (Iscove and
Melchers, 1978). Foetal bovine serum (FBS), purchased from Hyclone
Laboratories Inc., was heat inactivated at 56°C for 30 min, and used at
20%(v/v) final concentration. This medium was modified again by the
addition of 0.3% (w/v) sodium bicarbonate and adjusting the pH to 7.0 (It will
henceforth be referred to as "complete-(M-DMEM) medium").
Mice were infected by intraperitoneal injection of lxlO 5
trypanosomes in 0.5ml of PSG, pH 7.4. Blood taken from the tail veins of
infected mice was examined microscopically, at x400 magnification, for
trypanosomes as described by Herbert and Lumsden (1976). Mice with peak
parasitaemia of more than lxlO9 trypanosomes/ml were killed by terminal
anaesthesia with diethy 1-ether and immediately sterilized by immersion in 70%
ethanol. Infected blood was drawn aseptically by cardiac puncture, using a 22
gauge hypodermic needle, into heparinized syringes containing 5IU
heparin/ml. Five microlitre volumes of infected blood were slowly deposited
by pipette at the bottom, close to the edges of three of the wells in a six well
plate (Costar, USA) containing 1ml of complete-(M-DMEM) medium each.
The culture plate was then incubated at 27°C for 90 min. During this
incubation, bloodstream form trypanosomes migrated from the infected blood
into the medium. Five hundred microlitres of medium, containing the
trypanosomes, were pipetted away from the deposited blood from each of the
three wells and transferred to the three remaining wells containing 1ml of
complete-(M-DMEM) medium each. The three new wells were incubated for
another 90 min, after which 1ml volumes of medium, containing
trypanosomes, were pipetted from each well away from the site of deposition
and pooled (3ml) into a 25cm2 culture flask. The flask was capped tightly and
incubated at 27°C. No attempt was made to change or add medium to the
culture for at least five days, and even then only if an increase in trypanosome
numbers and a decrease in pH were observed. Thereafter, up to 50% of the
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medium was changed over 2 to 3 days. Subculture of the EA IL2337 and WA
IL1392 were made when colonies of epimastigote forms covered at least 75%
of the plastic surface (Gumm, 1991). Epimastigote colonies were scraped off,
using disposable cell scrapers (Costar). Half of the medium containing
epimastigotes was transferred from one flask to a new one, and an equal
volume of fresh medium added.
5.3.1.3 Transformation of bloodstream form trypanosomes into procyclics
Transformation of T. brucei and T. congolense bloodstream
trypomastigotes into procyclics was initiated at 27°C in complete-(SM)
medium. Infected parasitaemic mice were killed by terminal anaesthesia as
usual and immediately dipped into 70% ethanol. Infected blood was drawn
aseptically into a heparinised syringe by cardiac puncture as previously
described. The blood was washed two times in complete-(SM) medium by
centrifugation at 400 Xg for 10 min. The pelleted blood cells and
trypanosomes were resuspended in complete-(SM) medium to a final
concentration of Ix l0 6 - lx l0 7 red bloodcells/ml and 4ml volumes pipetted into
25cm2 sterile culture flasks (Costar). The flasks were gassed with 5% CO2 in
air for 10-20 seconds, tightly closed and incubated at 27°C. Each flask was
examined daily, using an inverted microscope (Nikon, 46212, Japan) under
x200 magnification. When the trypanosome density reached approximately
lx l 0 7 /ml, half of the medium was removed and replaced by an equal volume
of fresh medium. This process was repeated until all blood cells were
eliminated from the culture. The cultures were then expanded by two fold
volume increases and transferred to larger (75cm2) culture flasks (Costar).
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5.3.2 Sample Preparation for Dot-ELISA
5.3.2.1 Preparation of trypanosomes for dot-ELISA
Procyclic forms of T. brucei and T. congolense, as well as
epimastigote forms of T. vivax were propagated in culture as described under
sections 5,3.1.1 and 5.3.1.2. Trypanosomes were harvested from in vitro
cultures and washed 2 times in PBS, pH 7.4, PSG, pH 8.0 or normal saline,
by centrifugation at 1000 Xg for 5 min each. The trypanosome pellets were
resuspended in small volumes of the appropriate buffer and counted, using an
Improved Neubauer counting chamber.
To allow for the proper estimation of the minimum number of
trypanosomes detected, the trypanosome suspensions were adjusted to lxlO 8
trypanosomes/ml and ten-fold serial dilutions made down to lxlOJ
trypanosomes/ml. 1 /xl samples were then pipetted from those tubes and placed
in dots onto strips of NC membrane, pore size 0.45/mi. Trypanosome
numbers ranging between lxlO5 trypanosomes/dot and 0 trypanosomes/dot
were thus obtained. Each sample was dotted onto several strips so that strips
with the same samples could be tested against different trypanosome species-
specific MoAbs. Also, procyclic T. congolense (savannah, riverine/forest and
Kilifi types) and T. grayi, each suspended in normal saline and dotted onto NC
filters (lxlO4 or 7xl03) per dot, were prepared and donated by Dr. J.
McNamara of the Tsetse Research Laboratory, Bristol, England.
The ability of the MoAbs to identify mixed trypanosome
populations was also studied. Trypanosome mixtures, each consisting of equal
numbers of two different species from the group (T. brucei, T. congolense, T.
simiae and T. vivax), were made in all possible combinations. Each mixed
sample was titrated in PBS (pH 7.4) to give lxlO5, lxlO4, lxlO3, lxlO2,
lxlO 1 and 0 trypanosomes per microlitre, and 1/xl volumes dotted onto NC
membrane strips. Trypanosomes were also lysed by suspension in distilled
water, and the lysed suspensions titrated to determine the effect of lysis on
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17 5
specificity and sensitivity of the MoAbs. The antigen "dotted" NC membrane
strips were left to dry at room temperature (17-26°C) for 15 min before they
were assayed.
The suitability of some other membrane supports, namely, 0.45/jm
pore size hybridization transfer membranes, Hybond-C (Cat. RPN.203C,
Lot. 18425), Hybond-N (Cat. RPN.303N, Lot.20849) both from Amersham,
and 0.45/xm pore size immuno-affinity membrane (Pall Immunodyne
Lot. 141743; Pall Bio Support Division, East Hills, NY, USA), was also
investigated.
5.3.3 Dot-ELISA Procedure
5.3.3.1 Detection of in vitro propagated trypanosomes by dot-ELISA
In vitro derived trypanosomes were suspended in buffer and applied
in dots onto NC membrane filters, and tested as described previously (Chapter
4, section 4.3.9).
5.3.3.2 Titration of specific MoAbs and enzyme conjugated antibody
Trypanosome species-specific MoAbs were tested in the dot-ELISA
to determine the optimal working dilution and time of incubation. MoAb in
culture supernatants were tested in four-fold dilutions, starting with a dilution
of 1:2. Ammonium sulphate concentrated MoAb fractions were tested in two
fold dilutions (starting with 1:5 dilution), and affinity purified MoAb fractions
were tested in two-fold dilutions, starting from 1:250. All MoAb dilutions
were also tested for optimum time of incubation, namely 30 min, Ihr, and 3hr.
Enzyme-conjugated antibody was also tested in two-fold dilutions from 1:250
to 1:2,000. The dilution and time of incubation at which an antibody reacted
specifically and gave the highest intensity of colour development were selected
and tested against various conjugate incubation times (15 min, 30 min and lhr)
for optimisation.
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1 76
5.4.1 Optimal working dilution and incubation period for MoAbs and
enzvme-coniugate
Investigations into the influence of period of incubation on the
reactivity of the specific MoAbs, indicated that a 3hr incubation period was
suitable for all the MoAbs. In contrast, different MoAb dilutions were
determined to be ideal, depending on the source of MoAb and the purification
method used (Table 23). Figure 22 shows the results obtained when purified
fractions of KT43/33 and KN4 were tested to determine the optimal working
dilutions. Both MoAbs reacted specifically at all the dilutions tested. The
intensity of the positive colour reactions remained virtually unchanged from
1:250 to 1:1,000 and decreased at 1:2,000. A working dilution of 1:1,000
was selected for both MoAbs.
One hour incubation of enzyme-conjugate was found to give better
reactions when compared to 30 min or 15 min incubations (Figure 23).
5.4.2 Specificity of the dot-ELISA in identifying trypanosomes in mono
species preparations
The ability of a panel of trypanosome species-specific MoAbs to
differentiate between in vitro derived procyclics of T. brucei, T. congolense
and T. simiae and epimastigotes of T. vivax, was investigated with the dot-
ELISA. Figure 24 summarizes the reactivity of two of the T. brucei specific
MoAbs (TR7 and KT39a) in this assay. It was observed that both TR7 and
KT39a reacted with the dot containing T. brucei antigen, and neither of them
reacted with the antigen dots representing T. congolense, T. simiae or T. vivax.
At 1:5 dilution, the culture supernatant containing KT39a MoAb, clearly left
negative impressions on the T. congolense and T. simiae dots, thereby
5.4 Results
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1 77
Table 23
Working dilution of the specific MoAbs used in the dot-ELISA
Monoclonal
Antibody Isotype Specificity
Source of
antibody
Dot-ELISA
titre
TR7/47.37.16 IgM T. brucei A.S. ppt 1 : 2 0
KT39a/18.17 IgM T. brucei C.S. 1:50
KT43/33.32 IgGj T. brucei Purified 1 :1 , 0 0 0
KT43/27.32 IgG2 a T. brucei Purified 1 :1 , 0 0 0
TV8/8.33.42 Ig°3 T. vivax Purified 1 :1 , 0 0 0
KD32/48.17 IgGi T. vivax Purified 1 :1 , 0 0 0
KD37/11.1 IgGi T. vivax A.S. ppt 1:50
C2 IgGi T. congolense Purified 1:500
TC6/42.6.3 IgGj T. congolense A.S. ppt 1 : 2 0
TC40/30.15.40 IgM T. congolense Purified 1 :2 , 0 0 0
TC39/30.25.95 IgM T. congolense Purified 1 :2 , 0 0 0
KNS7/14.X IgGi T. simiae A.S. ppt 1 : 2 0
TC16/5.12.33 IgGj Nannomonas Purified 1 :1 , 0 0 0
TC6/25.25.4 IgG3 Nannomonas Purified 1 :1 , 0 0 0
KN4/13.9 IgG3 Nannomonas Purified 1 :1 , 0 0 0
KN5/6.15 IgGi Nannomonas A.S. ppt 1 : 2 0
A.S. ppt= x20 concentration of culture supernatant by ammonium sulphate
precipitation.
C.S. = culture supernatant.
Purified = purified MoAb fraction.
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1 7 8
Figure 22
Titration of purified fractions of KT43/33 (Tb ruce i species-specific) and
KN4 (Nannomonas subgenus-specific) MoAbs to determine the optimal
dilution of antibody for use in the dot-ELISA. Each strip of NC membrane
was applied with varying concentrations of trypanosomes per dot
(Tryps/dot) of T. congolense K/83/IL/97/2 (TCK), T. brucei IL2616 (TB)
and T. simiae KETRI 2431 (TS) cultured procyclics. MoAbs were tested at
several dilutions as shown.
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CO
CO
— ,
CO
5r
• • , •
i U
« •
—
o o o o o
W O l f l O O
CM 10 N- O O ±1 - “ T- CM
z
*
i r
• • •
• • •
* ! ♦ i • *
l Tryps/dot
1x10®
1 x 1 0 4
1x10
1x10"
3
O O O O O^ o ^ o o MoAb.
CM 10 Is- O O ... .
^ ^ ^ r . dilution
Figure 22
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Figure 23
Titration of goat anti-mouse horseradish peroxidase conjugate to determine
optimal incubation time for reactions in the dot-ELISA. Each strip of NC
membrane was applied with varying concentrations of trypanosomes per dot
(Tryps/dot) of T. congolense K/83/IL/97/2 (TCK), T. brucei IL2616 (TB)
and T. simiae KETRI 2431 (TS) cultured procyclics. Strip 'C represents a
conjugate control, that was not incubated with specific MoAb.
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— Tryps/dot
1 x 1 0 5
1x104
1x103
1x102
1x101
0
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180
Figure 24
An illustration of the specific reactivity of two Trypanosoma brucei specific
MoAbs (TR7 and KT39a) in the dot-ELISA. Each strip shown was applied
with various concentrations of trypanosomes per dot (Tryps/dot) of either T.
vivax IL1392 cultured epimastigotes (TV) or procyclics of T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2331 (TS).
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KT39a
MoAb
^ ^ dilution
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181
illustrating clear T. brucei specificity (Figure 24). Figures 25, 26 and 27
illustrate respectively, the specificity of two T. vivax specific MoAbs (TV8 and
KD32), four T. congolense specific MoAbs (C2, TC6 , TC40 and TC39), and
four Nannomonas subgenus-specific MoAbs (TC16, TC6/25, KN4 and KN5).
These specific reactions remained unaltered even at trypanosome
concentrations of lxlO5 trypanosomes/dot in 1 pci volumes. The reactivity
pattern of the entire panel of MoAbs, as determined by dot-ELISA, is shown
in (Table 24).
5.4.3 Specificity of the dot-ELISA in identification of the constituent
trypanosome species in artificially mixed preparations
Mixtures consisting of two different trypanosome species each,
were made in all possible combinations, using T. brucei, T. vivax, T.
congolense and T. simiae organisms. The mixed trypanosome suspensions
were doted onto NC membrane and tested to determine the ability of the
various MoAbs to differentiate the constituent species. Figure 28 illustrates
the ability of the T. brucei specific MoAb (KT39a) to detect T. brucei in
brucei/congolense and brucei/simiae mixtures. In the same experiment,
KT39a did not react with the congolense/simiae mixture. Also, Figure 28
shows the specific detection of T. congolense by C2, TC6 , TC40 and TC39 in
congolense/brucei and congolense/simiae mixtures. The absence of a reaction
on the brucei/simiae dot, clearly showed that those MoAbs were indeed T.
congolense specific. TVS and KD32, both T. vivax specific, had been shown
not to react with antigen mixtures of brucei/congolense, brucei/simiae and
congolense/simiae (Figure 29). Yet, the Nannomonas specific MoAbs (TC16,
TC6/25, KN4 and KN5) are shown to detect their target species (T. congolense
and T. simiae) in those mixtures.
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182
Figure 25
Reactivity of Trypanosoma vivax specific MoAbs (TV8 and KD32) in the dot-
ELISA. Each strip shown was applied with various concentrations of
trypanosomes per dot (Tryps/dot) of either T. vivax IL1392 cultured
epimastigotes (TV) or procyclics of T. congolense K/83/IL/97/2 (TCK), T.
brucei IL2616 (TB) and T. simiae KETRI 2431 (TS).
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0 0
>
CM
CO
o
*
— ■
Tryps/dot
TV 1x105
1x104
1x103
1 x 1 0 2
1x101
1x10°
00
>
TCK
TB
TS
Figure 25
K
D
32
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183
Figure 26
Reactivity of Trypanosoma congolense specific MoAbs (C2, TC6 , TC40 and
TC39) in the dot-ELISA. Each strip shown was applied with various
concentrations of trypanosomes per dot (Tryps/dot) of either T. vivax IL1392
cultured epimastigotes (TV) or procyclics of T. congolense K/83/IL/97/2
(TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431 (TS).
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CM
o
O CD
CO CO
o o o
I— H- I—
CD
CM Q
O I-
L_
Tryps/dot
TS
5 ^
1 x 1 0
Figure 26
TC
40
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1 8 4
Figure 27
Reactivity of Nannomonas subgenus-specific MoAbs (TC16, TC6/25, KN4
and KN5) in the dot-ELISA. Each strip shown was applied with various
concentrations of trypanosomes per dot (Tryps/dot) of either T. vivax IL1392
cultured epimastigotes (TV) or procyclics of T. congolense K/83/EL/97/2
(TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431 (TS).
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- TV
Tryps/dot y B
^ T S
1x105
1x104
1 x 103
1 x 1 0 2
1 x 1 0 1
1x10
Figure 27
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1 85
Table 24
The specificity of the MoAbs as determined by their reactivity with procyclics and
epimastigotes of different trypanosome species in the dot-ELISA
Monoclonal
Antibody Isotype
T. brucei
*
T. vivax
**
T. congolense
*
T. simiae
*
TR7/47.37.16 IgM +
KT39a/18.17 IgM +
KT43/33.32 IgGi + - -
KT43/27.32 IgG2 a + - -
TV8/8.33.42 IgG3 - + - -
KD32/48.17 IgGi + -
KD37/11.1 IgGj - + -
C2 IgGi - +
TC6/42.6.3 IgGi - - +
TC40/30.15.40 IgM - +
TC39/30.25.95 IgM +
KNS7/14.X IgGi - - +
TC16/5.12.33 IgGi + +
TC6/25.25.4 IgG3 + +
KN4/13.9 IgG3 - + +
KN5/6.15 IgGi - + +
* procyclics.
** epimastigotes.
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
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Figure 28
Reactivity of T. brucei species-specific MoAbs (TR7 and KT39a) and T.
congolense specific MoAbs (C2, TC6 , TC40 and TC39) with mixtures of
cultured trypanosome procyclics in the dot-ELISA. Each NC membrane strip
was applied with varying concentrations of trypanosome mixtures per dot
(Tryps/dot/spp.). The trypanosome species used were: T. brucei IL2616 (TB),
T. congolense K/83/IL/97/2 (TCK) and T. simiae KETRI 2431 cultured
procyclics. ( a ) indicates NC membrane strips which were "dotted" with
trypanosome antigens prepared by suspending whole organisms in deionised
water, ( a ) indicates NC membrane strips which were "dotted" with whole
trypanosomes suspended in phosphate buffered saline (PBS) pH 7.4.
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K
QC
1-
TB TCK —
TB TS -
TCK TS —
K
T3
9a
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9
01
O O)
^ COo oI— I—
1 i 1 T ryps/dot/spp.
r p i j - - r a
5x104
5x103
5x102
5x101
5
0
A A A A A A A A
Figure 28
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1 8 7
Figure 29
Reactivity of T. vivax specific MoAbs (TV8 and KD32) and Nannomonas
subgenus-specific MoAbs (TC16, TC6/25, KN4 and KN5) with mixtures of
cultured trypanosome procyclics in the dot-ELISA. Each NC membrane strip
was applied with varying concentrations of trypanosome mixtures per dot
(Tryps/dot/spp.). The trypanosome species used were: T. brucei IL2616 (TB),
T. congolense K/83/IL/97/2 (TCK) and T. simiae KETRI 2431 cultured ,
procyclics. ( a ) indicates NC membrane strips which were "dotted" with
trypanosome antigens prepared by suspending whole organisms in deionised
water, (a ) indicates NC membrane strips which were "dotted" with whole
trypanosomes suspended in phosphate buffered saline (PBS) pH 7.4.
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Figure 29
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1 Tryps/dot/spp.
5x104
5x103
5x102
5x101
5
0
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188
Suspending mixed trypanosomes in PBS and dotting them as whole
organisms or lysing the mixed organisms in deionised water before applying
the samples in dots onto NC membrane, gave similar results (Figure 28, 29).
On the whole, it was found that each of the MoAbs could detect it's target
trypanosome species, irrespective of which other species were present (Table
25). Also, the MoAbs were tested against trypanosome stocks or clones from
different geographical areas and shown to detect specifically all the different
isolates (Table 26).
5.4.4 The suitability of ascites as a source of MoAb for the dot-ELISA
The use of ascitic fluid as a source of specific MoAb for the dot-ELISA
presented some problems. Most ascites fractions cross-reacted extensively
with all the different trypanosome species when used at dilutions lower than
1:100. At higher dilutions, specific reactions were usually obtained, but this
was normally at the expense of sensitivity. Figure 30 shows the results
obtained from the titration of ascites containing the T. congolense specific
MoAb TC39. The trend clearly illustrates the decreasing sensitivity as specific
reactivity on the T. congolense antigen dot (TCK) was being achieved. This
loss in sensitivity was unreasonably high when compared to MoAb purified
from culture supernatants, and remained unchanged even when ascites was
purified. It was, therefore, decided to discontinue the use of ascites as a
source of specific MoAb for the dot-ELISA in favour of direct use of culture
supernatants or purified fractions thereof.
5.4.5 Cross-reactivitv in the dot-ELISA
Cross-reactivity due to factors such as the source of MoAb and
concentrations of MoAb or conjugate or antigen, was encountered in the dot-
ELISA, prior to standardization of the assay. High concentrations of purified
MoAb or HRPO-conjugated antibody, increased the non-specific reactivity,
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1 8 9
Table 25: Ability of the specific MoAbs to identify trypanosome species in
artificial mixtures of cultured insect stages of the parasites
Reactivity of MoAbs with trypanosome mixtures tested
T. brucei T. brucei T. brucei T. congolenseT. congolense T. simiae
Monoclonal & & & & & &
Antibody Isotype Specificity T. congolense T. simiae T. vivax T. simiae T. vivax T. vivax
TR7/47.37.16 IgM T. brucei + + + ~ ~
KT39a/18.17 IgM T. brucei + + + - - -
KT43/33.32 IgGi T. brucei + + + - - -
KT43/27.32 !SG2 a T. brucei + + + - - -
TV8/8.33.42 IgG3 T. vivax - + - + +
KD32/48.17 IgGi T. vivax - - + - + +
KD37/11.1 IgGx T. vivax - - + - + +
C2 IgGi T. congolense + - - + + _
TC6/42.6.3 IgGi T. congolense + - - + + -
TC40/30.15.40 IgM T. congolense + - - + + -
TC39/30.25.95 IgM T. congolense + - - + + -
KNS7/14.X IgGi T. simiae - + - + - +
TC16/5.12.33 IgGj Nannomonas + + _ + + +
TC6/25.25.4 IgG3 Nannomonas + + - + + +
KN4/13.9 IgG3 Nannomonas + + - + + +
KN5/6.15 IgGi Nannomonas + + - + + +
+ = antibody reacts with trypanosomes.
- = antibody does not react with trypanosomes.
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1 90
Table 26: Reactivity of the specific MoAbs with different stocks and clones of T. brucei, T. vivax, T. congolense and T. simiae as defined by dot-ELISA
Reactivity of the monoclonal antibodies with uncoated procyclic or epimastigote trypanosomes of:
T. brucei T. vivax T. congolense T. simiae
Monoclonal IL2616 Th-17/87TREU-1442MiTatl .2 IL1984 IL1478 IL1392 IL3895 ILDatl .9 CP2331 IL/60/1 IL/97/2 1L2079 CP81 MOVS MBOI MSUS TS1 TS4 KETRI243
antibody (Proc) (Proc) (Proc) (Proc) (Proc) (Proc) (Epis) (Epis) (Epis) (Epis) (Proc) (Proc) (Proc) (Proc) (Proc) (Proc) (Proc) (Proc) (Proc) (Proc)
TR7 + + + + + + _ _ . - _ _ _ _ _ _ _
KT43/33 + + + + + + - - - - - - - - - - - - - -
KT39a + + + + + + - - - - - - - - - - - - - -
KT43/27 + + + + + + - - - - - - - - - - - - - -
TV8 - - - - - - + + + + - - - - - - - - - -
KD32 - - - - - - + + + + - - - - - - - - - -
KD37 - - - - - - + + + + - - - - - - - - - -
C2 - ■ - - - - ■ - - + + + + + + + - - -
TC6 - - - - - - - - - - + + + + + + + - - -
TC40 - - - - - - - - - - + + + + + + + - - -
TC39 - - - - - - - - - - + + + + + + + - - -
KNS7 - - - - - - - KNS7 - - - - - - - - - - - -
TC16 - - - - - - - - - - + + + + + + + + +
TC6/25 - - - - - - - - - - + + + + + + + + + +
KN4 - - - - - - - - - - + + + + + + + + + + n- m-
KN5 - - - - - - - - - - + + + + + + + + + +
+ = antibody reacts with trypanosomes.
= antibody does not react with trypanosomes.
EL/60/1 = K/82/IL/60/1
EL/97/2 = K/83/IL/97/2
MSUS = MSUS/LR/77/TSW103
(Proc) = procyclic forms propagated in vitro
(Epis) = epimastigote forms propagated in vitro
MOVS = MOVS/KE/81/WG84
MBOI = MBQI/NG/60/1-148
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1 9 1
Figure 30
Reactivity of ascitic fluid containing the T. congolense species-specific MoAb
(TC39) with T. congolense K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and
T. simiae KETRI 2431 cultured procyclics. Trypanosomes were titrated
tenfold from lxlO5 to 0 trypanosomes per dot (Tryps/dot). Note the
decreasing sensitivity as the ascites was diluted further in order to achieve
specificity.
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TC39
TCK
TB
TS
o
Q
‘ ©
o
©
o Oj
O -
I ®
CM 00 CM " t 00
^ " CO CD CM
Tryps/do t
1x105
1 x 1 0
1x10"
1x10*
1x10
1x10
1
Ascites
dilution
Figure 30
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1 92
even though culture supernatants, or higher dilutions of the same MoAbs
fractions, reacted specifically. Similarly, it was found that excess antigen
( > l x l 0 8 trypanosomes/dot//K.l) induced non-specific reactions, although the
observed reaction intensities were generally low.
All cross-reactions were, however, abolished following standardization
of the assay.
5.4.6 Sensitivity of the dot-ELISA
Application of the dot-ELISA in identification of trypanosomes in
mono-species cultures revealed that, some MoAb fractions of TR7, KT39a,
TC40, TC6/25 and KN4 were capable of detecting a minimum of 10
trypanosomes per dot, but one of the T. vivax specific MoAbs (KD37) detected
a minimum of 100 organism per dot. Table 27 summarizes the results of the
sensitivity in terms of the minimum number of trypanosomes detectable in
mono-species culture preparations by the dot-ELISA, using the panel of
MoAbs prepared.
The minimum number of trypanosomes that could be detected in
the dot-ELISA increased by a factor of 50, when the assay was applied for the
specific identification of trypanosomes in artificially mixed preparations.
Thus, a MoAb fraction that detected a minimum of 100 trypanosomes per dot
in the mono-species preparations, now would detect a minimum of 100 x 50
(5,000) trypanosomes per dot in the mixed preparations. Table 28 summarizes
the sensitivity in terms of the minimum number of trypanosomes that could be
detected by the various MoAbs in the dot-ELISA when applied for the
differentiation of artificially mixed trypanosomes. This drop in sensitivity
could be due to competition between antigens of the mixed trypanosome
species for the binding sites on the NC membrane.
Analysis of the data on sensitivity in terms of the minimum number of
trypanosomes that could be detected in mono-species trypanosome cultures,
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193
Table 27: Sensitivity in terms of the minimum number of trypanosomes detected in mono-species preparations by the dot-ELISA
Specific monoclonal antibodies
raiaMLc
number
detected TR7
T. brucei
KT39a KT43/33 KT43/27
T. vivax
TV8 KD32 KD37 C2
T. congolense
TC6 TC40 TC39
T. simiae
KNS7 TC16
Nannomonas
TC6/25 KN4 KN5
1 0 5 + + + + + + + + + + + + + + + +
1 0 4 + + + + + + + + + + + + + + + +
1 0 3 + + + - + + - + + + + - + + + +
1 0 2 + + - - + - + + + + - - + + -
1 0 1 + + - - - - - - + _ _ _ + + _
1 0 ° - - - - - - - - - - - - - - -
0 - - - - - - - - - - - - - -
+ = visible reactions observed with that number of trypanosomes in a dot.
- = visible reaction not observed with that number of trypanosomes in a dot.
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194
Table 28: Sensitivity in terms of the minimum number of trypanosomes detected in mixed trypanosome preparations by the dot-ELISA
Parasite
number
detected
Specific monoclonal antibodies
TR7
T. brucei
KT39a KT43/33 KT43/27 TV8
T. vivax
KD32 KD37 C2
T. congolense
TC6 TC40 TC39
T. simiae
KNS7 TC16
Nannomonas
TC6/25 KN4 KN5
5xl04
5xl03
5xl02
5X101
5
+
+
+
+
+
+
+
'
1
1
+
+ +
+
+ + +
+
+
+
+
+
+ +
+
+
+
+
+
i
i
i
+
+
1
0 - - - - - - - - - - - - - - - -
+ = visible reactions observed with that number of trypanosomes in a dot.
- = visible reaction not observed with that number of trypanosomes in a dot.
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195
revealed that this sensitivity varied between different assays as well as between
different fractions of the same MoAb. Thus, using the most active fractions,
some of the MoAbs could detect as low as 10 trypanosomes per dot.
However, the repeatability of the assay was better when higher trypanosome
numbers were used. It was found that all the MoAbs could detect 5xl03
trypanosomes/spp./dot, and this was 1 0 0 % reproducible, compared with 60%
reproducibility obtained with 1 0 organisms/dot.
Based on these results, and the intensity of the positive colour reactions
obtained, lxlO4 trypanosomes/dot was considered to be the most suitable
parasite number for use in identifying trypanosome cultures with the dot-
ELISA.
5.4.7 Stability of dotted antigens
NC membrane strips with trypanosomes deposited as dots were stored
under desiccated conditions at 4°C, and at room temperature (17-26°C), and
tested for antigenic reactivity at intervals of 30 days using the panel of MoAbs.
No significant loss in assay reactivity was observed for periods of up to 60
days, regardless of whether the strips were blocked with 5% skimmed-milk
diluted in TBS before storage or not. However, after 90 days of storage at
room temperature, the T. congolense specific MoAbs showed reduced
reactivity, with a loss in sensitivity from lxlO2 to lxlO4 trypanosomes/dot,
irrespective of whether the strips were pre-blocked or not. Again, no change
in reactivity was observed in strips stored at 4°C for up to 90 days.
5.4.8 Use of different immuno-affinitv membranes
The effects of different brands of immuno-affinity membranes (NC
membrane, Hybond-C, Hybond-N and Pall Immunodyne) on the dot-ELISA
reactions, were also investigated. No differences in either specificity or
sensitivity were observed with regard to the NC membrane, Hybond-C and
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Hybond-N. The Pall Immunodyne membrane, however, gave less satisfactory
results when compared with the other three membranes. There was loss of
sensitivity of the order of xlO magnitude, from lxlO3 to lxlO4
trypanosomes/dot. This drop in sensitivity was attributed to a tendency for
samples to diffuse into the Pall Immunodyne membrane, leading to lack of
clearly defined positive staining reaction zones.
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In order to develop a MoAb-based assay for the differentiation of
in vitro propagated insect stage trypanosome species, emphasis was placed on
the utilization of an existing technique that offered the best opportunity to
develop an assay which would be simple and easy to perform, in addition to
being both sensitive and specific. It was anticipated that such an assay could
easily be modified for use in the field in the diagnosis of trypanosome
infections in infected tsetse flies (Glossina spp.).
Of the existing techniques namely, dot-ELISA, micro-plate ELISA
and radio-immunoassay, the assay that could best be developed for purposes of
this study, was the NC membrane-based dot-ELISA. The dot-ELISA is a
highly versatile, solid-phase immunoassay useful for both antibody or antigen
detection. The technique is rapid, easy to perform and interpret, reagent
conservative, cost effective and field portable (Pappas, 1988a).
The dot-ELISA described in this Chapter was successfully applied
to the identification of in vitro derived vector stages of T. brucei, T.
congolense, T. simiae and T. vivax. The assay could correctly identify the
trypanosome species involved in mono-species preparations as well as in
artificial mixtures of trypanosome species. This assay was also able to identify
the various stocks and clones of the different trypanosome species isolated
from different geographical areas. This broad application of the dot-ELISA is
a distinct advantage over the DNA hybridization technique which at present
employs probes that are intra-species specific (Gardiner, 1989) and, therefore,
are known to fail to identify new genotypes (McNamara et al., 1991; Majiwa
etal., 1993).
Some of the MoAbs detected as low as 10 trypanosomes/dot with
the dot-ELISA. This high sensitivity, in terms of the minimum number of
trypanosomes detected, was not surprising, since it had been reported that NC
5.5 Discussion
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membrane avidly binds a wide variety of parasite antigen preparations (Pappas
et al., 1983; Pappas et al., 1986; Zimmerman, Nelson and Clark, 1985;
Boctor et al., 1987; Whelen, Richardson and Wikel, 1986). Furthermore,
unlike. plate-ELISA in which adsorption of soluble antigens to well surface had
been reported to vary significantly (Burt, Carter, and Kricka, 1979; Kricka,
Carter, Burt, Kennedy, Holder, Holliday, Telford and Wisdom, 1980), with
the dot-ELISA technique the entire antigen applied is immobilized on the NC
membrane, which has a large surface area as a result of its porosity, and thus
increases the sensitivity of the assay (McFarlane, Tolley, Major, McFarlane
and Williams, 1983; Kumar, Band, Samantaray, Dang and Talwar, 1985).
However, in this work, it was found that the smaller the number of
trypanosomes dotted onto NC membrane (ie,, at least 100 or less) the less
reproducible was the assay results. This reduced reproducibility is believed to
be due to small variations in the test conditions which may affect MoAb
binding; some of these conditions were temperature, pH, concentrations of
buffers and washing. This finding therefore suggested that the dot-ELISA
would not be suitable, especially under field conditions if such low numbers of
trypanosomes were to be detected. However, the finding that at least 1,000 or
more trypanosomes/dot could produce 1 0 0 % reproducible results, indicated
that at higher antigen concentrations, this dot-ELISA method could be robust
and suitable for use in the field.
Using the dot-ELISA method, Pappas and colleagues (1983) had
shown that as little as 2.5xl04 parasites/dot gave sensitive, specific and
reproducible results. In this study, lxlO4 trypanosomes/dot, applied in 1 fi\
volumes, was established to give satisfactory results, and this was therefore
recommended for use in the dot-ELISA for subsequent studies. The
application of antigen in small volumes was shown to give better results, since
the intensity of the colour that developed was more dependent on the density,
than on the amount of antigen in a dot (Towbin and Gordon, 1984), Volumes
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as small as 0.1 /xl/dot (Hawkes, Niday and Gordon, 1982) and 1 /xl/dot
(Pappas, Hajkowski and Hockmeyer, 1983) had been used previously.
In this dot-ELISA method, the use of whole ascites or
immunoglobulin fractions was found unsuitable, as they cross-reacted
extensively. Ascitic fluids contain antibodies secreted by hybridoma cells, as
well as some of the animal's own immunoglobulins. Consequently,
immunoglobulins, purified from this source are not monospecific (Boeye,
1986). Hence, depending on the type of work, the contaminating antibodies in
ascites may be more or less a nuisance.
Pappas, Hajkowski and Hockmeyer (1984) attributed the decreased
reactivity of antigen in dotted samples stored on NC membrane to oxidation of
adsorbed antigen by nitro groups present in the NC membrane matrix. This
phenomenon is likely to be, in part, the cause of the deterioration of the T.
congolense specific antigen when dotted samples were stored at room
temperature (17-26°C) for more than 60 days. Another likely cause of
decreased reactivity was epitope sensitivity to temperature variations. It has
been reported that other types of membrane, for example cellulose membrane
(Londner, Rosen, Sintov and Spira, 1987) and opaque, white plastics (Lin and
Halbert, 1986) could be used in dot-ELISA. In this study, it was found that
some brands of membrane supports were more suitable than others in the dot-
ELISA.
Positive results obtained with the dot-ELISA method were easily
observed visually as brown dots on white NC filter paper, and the assay did
not require a high level of technical expertise to perform or interpret. The
potential of this procedure for diagnosis of trypanosome infections in the
vector (Glossina spp.) of the African trypanosomes was noted, and this was
indeed the subject of investigation in the studies described in the next chapter.
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CHAPTER 6
2 0 0
DETECTION AND DIFFERENTIATION BETWEEN
TRYPANOSOMES IN EXPERIMENTALLY-INFECTED TSETSE
FLIES (GLOSSINA SPP'.) USING DOT-ELISA
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A modification of the NC membrane-based dot-ELISA
developed in Chapter 5, was successfully used to detect and differentiate
between T. brucei, T. congolense and T. simiae procyclics in the midguts of
experimentally infected tsetse flies. The modification of the assay consisted of
(a) the lysis of T. congolense or T. simiae in NC membrane applied sample
dots using Triton X-114, and (b) a hydrogen peroxide destaining step, in which
stains made on NC membrane strips by applied sample dots were removed.
The afore-mentioned trypanosome species were specifically detected and
differentiated without any cross-reactivity. In these assays, T. brucei and T.
congolense parasites were detected directly using MoAbs specific to each of
them, whereas T. simiae parasites were detected by exclusion using a T.
congolense specific and Nannomonas subgenus-specific MoAb. The sensitivity
of the assay was 90.5% in detecting T. brucei infections, 85.4% in detecting
T. congolense infections and 94.4% in detecting T. simiae infections. The
sample preparation from the gut of each tsetse fly could be replicated in 15
different dots, allowing some samples to be stored for testing at a later date.
Sample dots stored at room temperature (19-26°C) under desiccated conditions
did not show any loss in activity in 90 days. However, after seven days of
storage, a ring-pattem reaction appeared on most sample dots that were tested
with the T. brucei specific MoAb, irrespective of whether T. brucei antigens
were present or not. These ring reactions, however, did not interfere with the
correct interpretation of the assay results.
Substitution of the PBS or PSG sample buffers used in the
original dot-ELISA described in Chapter 5 for Na2EDTA buffer, led to the
detection of T. brucei parasites in the salivary glands of infected tsetse flies
using a T. brucei specific MoAb. This dot ELISA had a specificity greater
than 99.9% and a sensitivity of 90%. Also, a dot-ELISA employing T. vivax
6.1 Summary
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and T. congolense specific MoAbs and utilizing the biotin-streptavidin reaction
amplification technique, was successfully used to detect T. vivax and T.
congolense in the mouthparts of infected tsetse flies. The specificity of the
assays were as good as for detecting T. brucei in infected tsetse salivary
glands, but the sensitivity was lower, 43.8% in detecting T. vivax and 55.6%
in the case of T. congolense.
The successful modification and application of the dot-ELISA in
detecting and differentiating between trypanosome species in the midguts,
salivary glands and mouthparts of experimentally infected tsetse flies, is the
best indication that the assays developed may be capable of specific
identification of trypanosome species in naturally infected Glossina species.
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Earlier studies of the life-cycle of trypanosomes in the vector
established that each trypanosome subgenus characteristically develops in a
particular organ of the tsetse fly (Lloyd and Johnson, 1924). As a result, the
standard method for diagnosis of trypanosome infections in tsetse, has been by
dissection and microscopy. By this method, infections in the gut and salivary
glands have been deemed to be due to the Trypanozoon subgenus, whereas,
infections in the midgut and proboscis have been assigned to the Nannomonas
subgenus. Infections confined to the midgut are classified as immature
Nannomonas or Trypanozoon, whilst those confined to the proboscis have been
ascribed to the Duttonella subgenus. It is, however, not possible by these
criteria to differentiate between the recognised species within the various
subgenera, since all species within a subgenus have identical cycles of
development in the vector (Hoare, 1972). The differential diagnosis is further
complicated when mixed infections occur in the vector (Godfrey, 1966).
Besides, Trypanosoma grayi and T. suis are known to reside in the midgut and
salivary glands of infected tsetse, respectively (Hoare, 1972), and their
presence, therefore, could lead to a misdiagnosis.
Currently, a recombinant DNA-based technique, first applied to
trypanosome identification by Kukla et al. (1987), provides the best known
alternative for the detection of, and differentiation between trypanosome
species in the Glossina species. This technique has subsequently been used for
the identification of Nannomonas species (Gibson et al., 1988), differentiation
between T. congolense and T. simiae (Majiwa and Webster, 1987; McNamara,
Dukes, Snow and Gibson, 1989; Majiwa and Otieno, 1990; McNamara and
Snow, 1991) and identification of T. brucei and T. vivax (Kukla et al., 1987;
Dicken and Gibson, 1989) in infected tsetse flies. However, this method also
has some disadvantages. The most important disadvantage is that the existing
6.2 Introduction
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DNA probes employed in the technique are intra-species specific (Majiwa et
al., 1993). As a result, the probes have shown that there are five types of T.
congolense (Kilifi type, West African riverine-forest type, Savannah type,
Godfrey type and Tsavo type) recognised by five different probes. The most
recent discovery, the Tsavo type, was established following failure of the four
previously existing T. congolense probes to hybridize to a new Nannomonas
isolate from Tsavo, Kenya. It is also quite likely that other T. congolense
populations exist which would not react with any of the five probes developed,
so that a negative result would not necessarily indicate that a given
Nannomonas trypanosome population does not belong to the T. congolense
species. Another, disadvantage is that the technique is not simple enough, and
therefore cannot be performed in most laboratories. The development of a test
which is simple, rapid, sensitive and specific and applicable under both
laboratory and field conditions is, therefore, highly desirable.
In the studies described in the previous chapter, a nitrocellulose
(NC) membrane based dot-ELISA that utilizes trypanosome species-specific
MoAbs was developed for identification and differentiation between in vitro
derived trypanosome species. In the study reported here, the dot-ELISA thus
developed, was successfully modified and used to detect and differentiate
between T. brucei, T. congolense and T. simiae procyclics in the midgut, T.
brucei in the salivary glands, and T. congolense and T. vivax in the mouthparts
of experimentally infected Glossina species.
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6.3.1 Experimental animals
6.3.1.1 Goats
Adult male castrated goats (crossbreeds between East African
Masai and Galla), aged 8-10 months and weighing between 20 and 25Kg, were
used in this study. They were purchased from farms in the Kumanchu
location, Laikipia district of Kenya, an area known to be free from tsetse flies
and trypanosomiasis. The goats were quarantined in fly-proof housing for one
month, after being dipped and treated with long-acting tetracycline,
coccidiostats and anthelmintics on arrival. Prior to being used, they were
confirmed to be uninfected with trypanosomes, using the thick, thin and wet
blood films as well as by the darkground/phase contrast buffy coat technique
described by Murray, Murray and McIntyre (1977).
6.3.1.2 Pigs
Male and female, 6 -month old, Large-white pigs were bred at the
Veterinary Research Laboratory, Kabete, Kenya, an area known to be free
from tsetse and trypanosomiasis. Those which were purchased for this study,
came from herds kept in the area.
The animals were kept in fly-proof quarters and screened for
trypanosomiasis, using the haematocrit centrifugation technique as well as the
thick, thin and wet blood film microscopy method.
6.3.2 Tsetse flies
6.3.2.1 Laboratory bred tsetse flies
The tsetse flies used came from the ILRAD laboratory-reared
Glossina morsitans centralis which had previously been obtained from the East
African Trypanosomiasis Research Organisation (EATRO), Tororo, Uganda in
6.3 Materials and methods
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1979 (Moloo, Kutuza, Bakakimpa, Kamunya, Desai and Pereira, 1985). This
colony was first initiated in 1969 at EATRO, with adults which had emerged
from pupae collected in the field at Singida, mainland Tanzania (Moloo and
Kutuza, 1969). The Glossina pallidipes flies used had originated from
Nguiuman and Shimba Hills in Kenya, and were also part of the ILRAD tsetse
colony collection.
6.3.3 Infection of goats, pigs and tsetse flies
6.3.3.1 Infection of goats
Seven goats were each infected with one of the following 7
trypanosome stocks or clones: T. brucei stock IL375; T. vivax stocks IL3096
and IL2337; T. congolense stock IL3779 and clones, IL1180, IL3274, and
IL13-E3. Each goat was infected by the intramuscular route with about lxlO 7
trypanosomes, diluted in 3ml of phosphate-buffered saline-glucose (PSG), pH
8.0 (Lanham and Godfrey, 1970). To monitor parasitaemia, each goat was
bled daily from a marginal ear vein, and the blood examined for the presence
of trypanosomes, using the wet blood film phase contrast microscopy at x400
magnification or the microhaematocrit/dark ground technique (Murray et al. ,
1977).
6.3.3.2 Infection of pigs
Three pigs were each infected subcutaneously in the neck region
with either T. simiae stock CP11(IL3879) or IL3815. To monitor
parasitaemia, peripheral blood was drawn daily from either an ear or tail vein
and examined for trypanosomes as described for goats above.
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6.3.3.3 Infection, maintenance and identification o f infected tsetse flies
T. brucei, T. vivax and T. congolense parasites were transmitted to
G. m. centralis flies from infected goats and T. simiae to G. pallidipes from
infected pigs, by fly feeding.
Five days after infections had become patent in goats, and 1 day
afterwards in pigs, teneral tsetse were allowed to feed on the shaven flanks of
an infected goat for a period of 30 days in the case of T. brucei and 25 days
for T. vivax and T. congolense. Thereafter, the flies were starved for two days
and those with mature infections identified by the warm-slide probe method of
Burtt (1946). With regard to T. simiae, teneral tsetse were fed once only on
infected pigs, after which the flies were maintained by feeding on rabbits for
25 days and starved for 2 days prior to probing. All tsetse flies confirmed to
be infected by the extrusion of metacyclics were maintained by feeding on
rabbits.
6.3.4 Preparation of samples for dot-ELISA
6.3.4.1 Dissection of tsetse and extraction of midgut tissue
Tsetse flies were killed by crushing the thorax with gentle pressure
exerted with a finger or by anaesthesia using chloroform, and the wings and
legs pulled off. Several ways of dissection and preparation of the midgut
samples were examined:
6.3.4.1.1 The fly was placed on a microscope slide under a dissecting
microscope (Wild M5A binocular; Wild, Heerbrugg, Switzerland) at
xl20 magnification and about 30/d of PBS (pH 7.4) or PSG (pH
8.0) added. The abdomen of the fly was then tom open at the
ventral surface, using a pair of forceps and a dissecting pin. The gut
was pulled into the buffer on the slide and the midgut cut out and
covered with a coverslip and examined for trypanosomes using a
compound microscope (Leitz larlux; Leitz Wetzlar, Germany) at
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x320 magnification. The examined tissues were then transferred
with forceps into an Eppendorf tube containing 50/d of the
appropriate buffer.
6.3.4.1.2 Alternatively, the tsetse gut was dissected out onto a slide as above,
and cut below the proventriculus and above the rectum. The whole
gut, including the foregut, midgut and hindgut, was examined
microscopically for the presence of trypanosomes and then
transferred into 50/d of either PBS or PSG.
6.3.4.1.3 In the last method tried, the distal quarter of the abdomen of tsetse
was excised with a pair of dissecting scissors and discarded (Kukla et
al., 1987). The whole abdominal contents were then squeezed out
by applying firm pressure in a rolling motion, from the anterior
portion toward the posterior end of the abdomen. The protruding
gut was then tom apart with forceps and transferred into 50/d of
buffer.
6.3.4.2 Preparation and application of tsetse midgut suspensions onto NC
membrane
Tsetse gut tissue dissected out as indicated variously above, and
suspended in either PBS or PSG, were treated again in three
different ways before applying sample dots onto NC membrane
strips for testing: (1) Suspended tsetse gut samples were agitated to
release trypanosomes into the buffer, by tapping the base of the tube
gently with a finger. The samples were then allowed to stand for up
to 1 hr, and agitated once more before pipetting out 3 /d samples
onto NC membrane strips in dots. (2) The gut suspensions were
mixed gently by pipetting the fluid up and down a few times, using a
50/d micropipette, and 3/d samples dotted soon after. (3)
Trypanosomes in suspended gut tissues were released by physical
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maceration, using the tip of a 50/u.l micropipette, together with
vigorous pipetting up and down about 10 times, before 3/xl sample
volumes were applied in dots onto NC membrane strips for testing.
As controls, lxlO5 T. brucei, T. congolense and T. simiae
procyclics, and epimastigotes of T, vivax obtained from in vitro
cultures were separately applied in dots onto each NC membrane
strip.
6.3.4.3 Preparation of touch blots
Tsetse abdomen was slit open as above (section 6 .3.4.1.3). The
abdomen was squeezed several times and the protruding gut touch-
blotted by pressing gently onto NC membrane. Alternatively, the
protruding gut was cut with a scalpel blade before touch-blotting.
6.3.4.4 Preparation of dot-blots using lvsed trypanosomes
Attempts were made to lyse gut forms of T. congolense and T.
simiae so as to expose internal trypanosome species-specific antigens
for uptimum reactivity in the dot-ELISA.
6.3.4.4.1 Lvsis of T. consolense or T. simiae in infected tsetse gut samples in
suspension
Several detergents, namely, Nonidet P-4Q (NP-40), Saponin,
Sodium dodecyl sulphate (SDS), all from (Sigma, England); and Triton X-114
(Fluka Chemie AG, Switzerland), were tested in experiments intended to lyse
T. congolense or T. simiae procyclic midgut forms in infected tsetse gut
samples. Each of the detergents was used to prepare a "lysis-buffer" which
consisted of 0.05, 0,1, 0.2, 0.3, 0.4 or 0.5% detergent, and lOjug/ml
Leupeptin and E-64 in either PBS or PSG. Fifty microlitre aliquots of each
concentration of lysis-buffer were pipetted into Eppendorf tubes, and infected
tsetse midguts dissected out and suspended in them. Trypanosomes were
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released into the sample lysis buffers by gently pipetting the fluid up and down
a few times, using a 50/xl pipette. The samples were allowed to stand for 30
min, and mixed once again before 3/d volumes were pipetted out and applied
onto NC membrane strips in dots.
6.3.4.4.2 Lvsis of T. comolense or T. simiae gut forms in sample dotted NC
membrane strips
NC membrane strips were "dotted" with experimentally-infected T.
congolense or T. simiae tsetse gut samples, as previously described. The
sample dotted strips were then incubated in different concentrations of
detergent solutions for varying time periods (either 30 min, lhr or 2hr, at
room temperature of 19-25°C) without shaking. The detergents used were
either: NP-40, Saponin, SDS or Triton X-114. Each was tested at six different
concentrations (0.05, 0.1, 0.2, 0.3, 0.4, or 0.5%), diluted in blocking solution
which consisted of 5% (w/v) skimmed milk in Tris-buffered saline
(TBS)(50mM Tris and 150mM NaCl, pH 8.0).
6.3.4.5 Preparation of tsetse salivary glands for dot-ELISA
Tsetse salivary glands were dissected out in one of two ways:
6.3.4.5.1 Each fly was placed on a microscope slide, ventral surface up, and
30/d of PSG added onto the head region. The thorax was then
pinned down with a dissecting needle close to the base of one wing,
and the head grasped with fine forceps and pulled gently, but
steadily, away from the thorax in a straight line, under a dissection
microscope at xl20 magnification. The glands were pulled out
whilst immersed in the buffer until they were out of the thorax.
When a gland broke, it was seized with forceps and pulled out.
6.3.4.5.2 A fly was placed on a slide as above, and 30/d of buffer added to
the abdominal area. The abdomen was then torn open at the anterior
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end close to the thorax and the elastic tissue pulled backwards
towards the posterior end. The exposed gut was pulled back and a
drop of PSG added into the cavity. The tissues at the anterior most
part of the exposed abdominal cavity were grasped with a pair of
fine forceps and pulled into the buffer on the slide. The two salivary
glands were easily located by this method.
The isolated salivary glands were transferred, using forceps, into
lOjul of 5mM Na2EDTA buffer. The suspended glands were pipetted up and
down several times, using a 1 0 /d micro-pipette, before 3/zl volumes were
pipetted onto NC membrane strips in dots.
6.3.4.6 Preparation of tsetse proboscides for dot-ELISA
Several ways of dissection and preparation of tsetse mouthparts were
explored:
6.3.4.6.1 The proboscis of a tsetse fly was cut a third of the way down from
the thecal bulb, with a pair of scissors. The thorax was then
squeezed gently to expel a drop of fluid through the cut proboscis
and gently touch-blotted onto a demarcated spot on NC membrane.
6.3.4.6.2 The head of a tsetse fly was placed on a microscope slide, ventral
surface up. The posterior base of the thecal bulb, close to the head,
was pressed gently but firmly with a dissecting needle placed almost
parallel to the slide surface, and pulled away from the head. The
labrum and hypopharynx were then examined under a light
microscope (Leitz labrlux; Leitz Wetzlar, Germany) at x320
magnification, for the presence of trypanosomes. The separated
proboscis was then transferred into about 1 0 /xl of distilled water,
under a dissection microscope at xl80 magnification, and the
labrum, labium and hypopharynx separated, using two dissecting
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needles, before they were transferred into about 1 0 /xl of distilled
water in an Eppendorf tube. The sample was left to stand for about
lhr before pipetting up and down about ten times using a 5/A
micropipette, and five microlitres transferred onto a spot on NC
membrane. The sample was air dried at room temperature and the
remaining 5/xl pipetted onto the same spot.
6.3.4.6.3 Tsetse proboscis was separated from the head and dissected as
described above, in about 7/xl of distilled water, PBS or PSG or
5mM Na2EDTA buffer, in the wells of a teflon coated multitest
immunofluorescence slide. The dissected labrum and hypopharynx
were then cut into pieces in the wells with a small knife, and the
suspension transferred from the well directly onto NC membrane in
a dot.
6.3.4.6.4 The sample preparation, as previously described (section 6 .3.4.6 .3)
was repeated using silicon coated multitest slides.
6.3.4.6.5 The proboscis was separated from the head of tsetse and cut at the
base of the thecal bulb. The mouth parts were then transferred into
an Eppendorf tube containing about 7^1 of distilled water, PBS,
PSG, or 5mM Na2EDTA buffer. The sample was left to stand for at
least 1 hr, after which the proboscis was broken up into small pieces
with the tip of a micropipette. The sample was pipetted up and
down about 5 times and the whole volume transferred onto a NC
membrane in a dot.
6.3.5 Estimation of trypanosome numbers in midgut suspensions
Tsetse midgut suspensions were prepared and mixed as described
earlier, and large particulate tissue matter removed and discarded.
A small volume was then pipetted out of each sample preparation
and dropped onto a microscope slide, and covered with coverslip.
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The number of trypanosomes per millilitre in each sample was then
estimated using the "rapid matching method" of Herbert and
Lumsden (1976).
6.3.6 Monoclonal antibodies
The panel of trypanosome species, and subgenus-specific MoAbs
used in this study were produced and selected as described in Chapter 4.
6.3.7 Dot-ELISA procedure
6.3.7.1 Detection of T. brucei in midguts of infected tsetse flies bv a
modified dot-ELISA I
All incubations and washings in this assay were performed at room
temperature on a gentle rocker. Each tsetse sample was applied in dots onto
several strips so that every sample could be assayed for reactivity with various
trypanosome species-specific MoAbs. The strips were first destained by
incubating for 1 hr in a "destaining solution" containing 5%(v/v) H2O2 in
blocking solution. They were then washed three times, 10 min each, with TBS
pH 8.0, and then incubated for 3 hr with specific MoAbs, diluted in a blocking
solution. This was followed by two washes (10 min/wash) with the same
buffer. The strips were then incubated for 1 hr with goat anti-mouse
immunoglobulins labelled with horseradish peroxidase (HRPO) (Sigma, USA)
and diluted in a blocking solution. They were washed two times, after which
they were immersed for three minutes in a substrate solution containing
0.15%(v/v) hydrogen peroxide (H2 0 2) and 0.05%(w/v) 3,3'-diaminobenzidine
(DAB) in phosphate-Na2EDTA buffer (lOmM NaH2P04, lOmM Na2HP0 4
and lOmM Na2 EDTA). The strips were then rinsed two times in deionised
water and the substrate reaction stopped as described earlier (Chapter 4 ,
section 4.3.8.1). The results were read visually. Positive reactions appeared
as brown dots, whereas negative results remained colourless. A control
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section on each strip was applied with lxlO5 trypanosomes/dot of T. brucei, T.
congolense and T. simiae. These were used to assess the performance of the
specific MoAbs. The conjugate control strips dotted with all the test samples
were assayed omitting the step in which specific MoAb was added. Any
reactions on these trips therefore gave a measure of non-specific background
reactivity.
6.3.7.2 Detection of T. coneolense and T. simiae in the midguts of infected
tsetse flies bv a modified dot-ELISA II
NC membrane strips applied with sample dots were first incubated
for I hr with 0.1%(v/v) Triton X-114 dissolved in blocking solution, and
washed three times (10 min/wash) with Tris-buffered saline pH 8.0. The
Triton X-114 was used to lyse whole trypanosomes in the dotted samples so as
to expose internal trypanosome antigens. The rest of the procedure was the
same as described previously for the detection of T. brucei in infected tsetse
midgut.
6.3.7.3 Detection of T. brucei in the salivary glands of infected tsetse flies
bv dot-ELISA
Salivary gland samples were prepared as described earlier and dotted
onto NC membrane strips in triplicates. All the steps in this assay were
performed at room temperature. Also, all incubations and washings were done
on a gentle rocker. The strips were first blocked by incubation in blocking
solution for 1 hr. The blocking solution was discarded and the strips further
incubated for 3 hr with trypanosome species-specific MoAbs diluted in
blocking solution. They were then washed three times (10 min/wash) with
TBS and incubated for 1 hr with HRPO-conjugated goat anti-mouse
immunoglobulins diluted in blocking solution. They were washed as above
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and then incubated with substrate solution for 3 min. The substrate reaction
was stopped and the results read as before.
6.3.7.4 Detection of T. vivax and T. consolense in the mouthparts of
infected tsetse flies bv dot-ELISA
Each tsetse proboscide sample was placed onto a NC membrane strip
in a single dot. The sample dotted strips were assayed either following the
procedure described earlier for the detection of T. brucei in the salivary glands
or following the modified procedure briefly described here under: Briefly,
after washing off excess monoclonal antibody, the strips were incubated for 1
hr with biotinylated sheep anti-mouse immunoglobulins, diluted in Tris-
buffered saline pH 8.0 and containing l%(w/v) bovine serum albumin. The
strips were washed three times as usual to remove excess unbound biotinylated
antibody and then incubated for 1 hr with streptavidin-conjugated horseradish
peroxidase (diluted in blocking solution). This was followed by washing as
described above, before incubating with the substrate. As usual, a control
section was incorporated into the system, consisting of four dots containing,
respectively, lxlO5 trypanosomes/dot of T. vivax, T. congolense, T. brucei
and T. simiae. (There were no controls with the conjugate since tsetse
proboscide samples were not replicated).
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6.4.1 Detection of trypanosomes in the midgut of experimentally infected
tsetse flies, using the standardized dot-ELISA developed for
differentiating between in vitro derived insect stage trypanosomes
Gut samples prepared from laboratory-reared tsetse flies and
applied in dots onto white NC membrane, were found to stain the membrane
with varying coloration and intensity. The stains were predominantly either,
reddish, reddish-brown, brown or blackish-brown to black, and occasionally
greenish to almost colourless, depending on the stage of digestion in the fly.
The strip labelled "P" in Figure 31 shows the stains made on NC membrane by
"dotted" tsetse gut samples from five T. congolense infected flies, five
uninfected flies, and in vitro derived procyclic T. congolense, T. brucei and T.
simiae. Two important observations were evident. Firstly, midgut samples
from both infected and uninfected tsetse flies stained the membrane.
Secondly, sample dots consisting of in vitro derived trypanosomes did not stain
the membrane.
Figure 31 shows an example of the results of direct application of
the dot-ELISA developed and standardized in Chapter 5 when applied for the
detection of T. congolense in the midgut of experimentally infected G. m.
centralis. The Nannomonas subgenus-specific MoAb (TC6/25) and the T.
congolense specific MoAb (TC6 ) reacted with samples from the T. congolense
infected flies as expected (Figure 31). However, these MoAbs also reacted
with samples from all the uninfected flies. The reactions with the control
trypanosome dots on the strips incubated with these two MoAbs, showed
cross-reactivity with other trypanosome species to which they were known not
to react (Chapter 5). Furthermore, both the T. brucei (KT39a) and T. vivax
(KD32) specific MoAbs, reacted with samples from all the T. congolense
6.4 Results
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infected as well as all the uninfected flies. These false reactions were also seen
on samples that were tested as conjugate controls (without incubation with
specific MoAbs), suggesting that the reactions were not the result of non
specific binding of the MoAbs. Comparison of the staining on the preserved
NC membrane strip P with those on the tested strips, revealed that the staining
intensity of the sample from uninfected fly UF5 was amplified by the dot-
ELISA (Figure 31).
6.4.1.1 Removal of high background activity from the dot-ELISA
The high background encountered was assumed to be due to two
causes: (1) persistent staining of the NC membrane due to the physical
coloration of the test samples, and (2 ) non-specific reactivity due to
interference by haem. To remove the background, investigations were
conducted into several alternatives. These were: (1) testing only flies with
very low amount of undigested blood meal (2 ) changing the handling of
samples prior to dotting, such as using the touch blot technique (3) changing
the enzyme substrate chromogen system so that positive reactions are
distinguishable from the background (4) reducing the amount of biological
debris in the tsetse gut samples, such as by partial isolation of trypanosomes
(5) removing the background without destroying the diagnostic antigens such
as by a destaining process, and (6 ) developing an alternative assay in which
background originating from tsetse gut samples present no problems. The
findings on each of these investigations are presented serially here under:
6.4.1.1.1 Testing flies with very low amounts of undigested blood msal
The suitability of the option to test only flies with m in im a l
amounts of residual blood meal clearly depended on the proportion of flies that
could be tested using that selection criterion. To determine this proportion in
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218
Figure 31
Dot-ELISA of midgut samples from five T. congolense (IL1180) infected
tsetse flies (IF1 to IF5) and five uninfected control flies (UF1 to UF5), The
sample from each fly was dotted across in a row, one replicate dot on each
strip. A control sector at the lower section of each strip was applied with
1x10s trypanosomes per dot of in vitro propagated T. congolense K/83/IL/97/2
(TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431 (TS). The antigen
"dotted" strips were tested using Nannomonas subgenus-specific MoAb
(TC6/25), a T. brucei species-specific MoAb (KT39a), a T. congolense
specific MoAb (TC6 ) and a T. vivax specific MoAb (KD32). Strip 'C' was a
conjugate control, and strip 'P ' was preserved without processing through the
dot-ELISA. Note the sample stains shown on strip 'P '.
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CM COO) CO CM/VSCD
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2 1 9
the case of laboratory reared tsetse flies, an experiment was first conducted
using newly emerged and 8 -week old G. m. centralis.
Figure 32a shows the staining pattern obtained from midgut
samples prepared from newly emerged male and female G. m. centralis from 1
hr after feeding (day 0) through day 1, 2, 3 to 4 after feeding. Non-specific
staining was observed with samples obtained up to 4 days post-feeding.
Samples prepared and dotted on day 0, 3 and 4 after feeding presented less
staining problems, compared with the samples prepared and dotted on days 1
and 2 after feeding. Analysis of the results obtained from the experiments
conducted showed that <10% of male, and <5% of female flies could be
tested 1 hr after feeding. The flies that were most suitable for testing were
those that did not fully engorge. None of the flies from either sex could be
tested on day 1 and 2 after feeding, though the female flies presented more
intense staining problems. By day 3 and 4 after feeding, about 10% of the
flies from either sex could be tested, and there appeared to be no differences in
the intensity of staining with reference to sex.
The pattern of staining from dotted gut samples of the eight week
old G. m. centralis flies is shown in Figure 32b. It was evident that gut
samples from male flies stained NC membrane less intensely when compared
with samples from female flies. Whilst about 10% of male flies could be
tested 1 hr after feeding and 35% could be tested on day 3 or 4 after feeding,
less than 2% of female flies could be tested on day 3 and 4 post-feeding
combined.
6.4.1.1.2 Use of different sample application techniques
Efforts were made to reduce non-specific staining by reducing
the amount of undigested material that was applied onto NC membrane for
testing. Investigations were conducted into the suitability of use of the tsetse
abdominal touch blot technique previously described by Kukla et al. (1987).
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Figure 32a, b
The staining pattern obtained on NC membrane following application of
midgut samples prepared from male (0 ") and female (9) G. morsitans centralis
from 1 hr after feeding (day 0) through days 1 to 4 after feeding, (a) staining
pattern from young flies that have fed only once; (b) staining pattern from 8 -
week old adult flies. Midgut samples were prepared from four randomly
selected flies from each of the two sex groups on days 0, 1, 2, 3 and 4 after
feeding, and applied in dots onto NC membrane. The strips were tested in the
dot-ELISA without incubating with specific MoAbs, but with conjugate and
substrate, so as to determine non-specific background.
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.• m •
Midgut contents of
l * _ •
• v.
randomly selected1 — ----- ----- — -----
tsetse flies • *1 m t— ---- ----1
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Figure 32a
Midgut contents of
randomly selected
tsetse fSes
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• •
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Days after feeding
• 9
Figure 32b
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2 2 1
The results showed that touch blotted samples left very little or no stains on
NC membrane. However, the sensitivity of the dot-ELISA was so much
lowered that less than 5% of T. brucei midgut infections could be detected.
6.4.1.1.3 Use of different enzymes and chromogenic substrates
It was thought likely that the false reactions could be the result
of oxidation of the chromogenic substrate [3,3'-diaminobenzidine (DAB)] by
H2 0 2 through catalysis by haem which acted as a peroxidase (Saunders,
Holmes-Siedle and Staak, 1964). To abolish those non-specific reactions, the
HRPO enzyme used in the dot-ELISA was replaced with glucose oxidase
which generates H2 0 2 by its action on glucose (Decker, 1977), thereby
permitting the omission of H2 0 2 in the substrate solution. The presence of
haem without glucose oxidase, therefore, would result in no false reactions
since H2 0 2 would be absent. Figure 33 summarizes the results of a
comparison of HRPO-conjugate and glucose oxidase-conjugated antibodies in
the detection of T. congolense (IL1180) in the midguts of experimentally
infected Glossina. The results showed that the glucose oxidase-conjugate was
not able to eliminate the background. It was also found that the glucose
oxidase-conjugate gave a higher assay background compared to HRPO. The
chromogenic substrate 4-Chloro-l-Naphthol (4C1N) which normally gives a
blue reaction, was compared with the brown reaction given by DAB so as to
determine whether it was possible to distinguish positive reactions from the
background by colour. The results obtained showed that neither the blue
reaction of 4C1N nor the brown reaction of DAB could allow clear distinction
of positive reactions from the background in the dot-ELISA.
6.4.1.1.4 Removal of background activity bv destaining
A destaining step involving the use of hydrogen peroxide
(H2 0 2) was introduced into the dot-ELISA and investigated to establish
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2 2 2
Figure 33
Comparison of HRPO-conjugated and glucose oxidase-conjugated antibodies in
the detection of T. congolense (IL1180) in the midguts of experimentally-
infected G. morsitans centralis using dot-ELISA. Each strip was "dotted" with
samples from ten infected flies (IF1 to IF10) and three uninfected control flies
(UF1 to UF3). The strips marked '1' were tested using HRPO-conjugate, and
those marked '2' with glucose oxidase-conjugate. The MoAbs used were:
TC6 , T. congolense specific; TC6/25, Nannomonas subgenus-specific; TR7
andKT39a, T. brucei species-specific; and KD32, T. vivax specific. Strip 'P'
was preserved without processing through the dot-ELISA.
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CO
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Figure 33
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22 3
whether it could remove the non-specific stains. Figure 34 shows the results
of an experiment in which the stains made by gut samples from T. brucei
infected flies as well as uninfected flies were removed by the destaining
method. Strip P which was not subjected to any testing, shows the stains made
by the original dotted samples. Strip C was run through the already
established dot-ELISA as conjugate control (without incubation with specific
MoAbs). This strip showed the non-specific reactions and stains described
earlier. The third strip Cm was run through a modified dot-ELISA that
included an H2O2 destaining step, also as a conjugate control. The removal of
all the non-specific stains in the sample dots on strip Cm are clearly shown. It
is important to mention, however, that the H2O2 treatment at this dilution
appeared to be harsh, considering the manner in which the sample dots
foamed, and pieces of debris broke loose and floated. Two important
questions, therefore, arose from this experiment. These were: (1) the effect of
H2O2 on the diagnostic antigens detected by the MoAbs, and (2) the stability
of those antigens on the NC membrane during treatment with H2O2 . These
questions were subsequently addressed in the following experiments.
6.4.1.2 The effect of hydrogen peroxide on the trypanosome species-
specific antigens detected bv the MoAbs
Figure 35 shows the effect of a 1 hr incubation of varying
concentrations of H2 0 2 on the T. brucei specific antigenic epitope detected by
KT43/27. The reactions on the control strip (incubated with 0% H2 0 2) and
those on strips incubated with 0.5-30% H2 0 2 showed that both the specificity
and sensitivity of the MoAb were unaffected by this treatment. In a similar
experiment illustrated in Figure 36, the Nannomonas subgenus-specific MoAb
KN4 was shown to react specifically with H2 0 2 treated T. congolense and T.
simiae parasites without any noticeable changes in sensitivity.
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2 2 4
Figure 34
Removal of non-specific stains from NC membrane strips "dotted" with G.
morsitans centralis midgut samples from five T. brucei infected flies (IF1 to
IF5) and five uninfected control flies (UF1 to UF5), using H2O2 in the dot-
ELISA. The sample from each fly was dotted across in a row, one replicate
dot on each strip. 'P ' was a preserved strip that was not subjected to any
testing. It shows the original stains made on NC membrane by the applied gut
samples. 'C ' was a strip processed through the dot-ELISA as conjugate
control, without incubation with specific MoAb, and strip 'Cm ' was processed
through a modified dot-ELISA that included an H2O2 destaining step.
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P c cm
IF 1 • •
IF2
IF3 O o
IF4
IF5 o o
UF1
■
UF2 I
UF3 '
UF4
UF5
Figure 34
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225
Figure 35
The effect of H2 0 2 on the T. brucei species-specific antigenic epitope
detected by KT43/27. In vitro derived T. congolense K/83/IL/97/2 (TCK),
T. brucei IL2616 (TB) and T. simiae KETRI 2431 (TS) were applied onto
NC membrane strips starting from lxlO 5 trypanosomes per dot to I
trypanosome per dot for each species.
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TCK—
TB —
TS -
n
Tryps /do t
1 x 10 '
1 x 10
* 1x1CT
1 x 1 0 '
1 x 101
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I
o i O r i n N i o W ^ i n i f l i o i c s a i o i o i o o i n o
6 OJ CO T t lO t- i - CM
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Figure 41
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2 3 7
reacted very weakly with the infected samples. This inability to strongly
detect clearly, the T. congolense IL1180 midgut infections was found to be the
case for all the T. congolense specific MoAbs. On the contrary, each of the
Nannomonas subgenus-specific MoAbs was able to detect those infections with
strong positive reactions.
6.4.3.1 Improved detection of T. consolense in the midguts of
experimentally infected tsetse flies using the modified dot-
ELISA
Attempts were made to improve the accessibility of the T,
congolense species-specific internal antigens (Chapter 4) for reactivity in the
dot-ELISA, by lysis of the trypanosomes in gut suspensions before applying
samples onto NC membrane for testing. The results, however, showed an
abolition of the weak reactivity of the T. congolense specific MoAbs, and a
decreased reactivity of the Nannomonas subgenus-specific MoAbs. It was
assumed that the decreased binding of the Nannomonas specific MoAbs, could
be due to increased competition for binding to NC membrane between the
trypanosome species-specific antigens and the mass of debris released by
midgut contents. Figure 42 shows a light micrograph of T. congolense midgut
procyclic forms together with the characteristic mass of biological debris
usually present in the tsetse gut samples. To circumvent this problem, it was
decided to first dot the gut samples onto NC membrane, before lysing the
bound trypanosomes.
Preliminary investigations showed that each of the detergents
used (NP-40, Saponin, SDS and Triton X-114), was capable of enhancing the
reactivity of the T. congolense specific MoAbs. Triton X-114 was, however,
selected due to its superior ability to give stronger reactions. Figure 43 shows
the results of an experiment in which T. congolense (IL1180) in the midguts of
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238
Figure 42
Light micrograph of a trypanosome infected tsetse midgut sample showing
biological debris and T. congolense parasites (t).
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Figure 43
Detection of T. congolense IL1180 in the midguts of experimentally infected
G. morsitans centralis using a modified dot-ELISA. Each of the NC
membrane strips was "dotted" with midgut sample preparations from, five
infected flies (IF1 to IF5), and five uninfected control flies (UF1 to UF5). A
control sector at the lower section of each strip was applied with lxlO5
trypanosomes per dot of in vitro propagated T. congolense K/83/IL/97/2
(TCK), T. brucei IL2616 (TB) and T. simiae KETRI 2431 (TS). The antigen
"dotted" strips were tested using Nannomonas subgenus-specific MoAb (KN4),
T. congolense specific MoAb (TC6) and T. brucei species-specific MoAb
(KT39a). Strip 'C' was tested as a conjugate control.
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•'t
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IF 1
IF2
IF3
IF4
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TB —
TS —
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Figure 43
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240
experimentally infected G. m. centralis were detected following lysis of
trypanosomes in sample bound NC membrane strips using 0.1% Triton X-114.
Both the Nannomonas subgenus-specific MoAb (KN4) and the T. congolense
specific MoAb (TC6) elicited stronger reactions and detected clearly, 4 out of
the five infected flies. Samples from all the uninfected flies tested negative,
and the reactions on the control trypanosome dots showed that both MoAbs
reacted specifically. The T. brucei specific MoAb KT39a reacted with the T.
brucei control parasite dot and detected none of the flies tested, thus,
demonstrating the specificity of the test.
6.4.4 Detection of T. simiae in the midguts of experimentally infected
tsetse flies using the modified dot-ELISA
The dot-ELISA described for detection of T. congolense in
infected tsetse guts was used for the detection of T. simiae in the same organ.
Figure 44 summarizes the results of an experiment in which T. simiae parasites
were detected and differentiated from T. congolense using the modified dot-
ELISA. The preserved strip P, which was not run through the assay, shows
the original staining of NC membrane by the gut samples. The conjugate
control strip C, which was not tested with specific MoAb shows no reactions,
confirming that the non-specific stains were removed. As seen on the strip
tested with the T. brucei specific MoAb (KT39a), none of the tested tsetse
samples reacted with this MoAb even though the specific reactivity of the
antibody was clearly illustrated by its reaction with the T. brucei control. Both
the Nannomonas and T. congolense specific MoAbs (KN4 and TC6) reacted
specifically in the assay as shown by their reactivity with the control T.
congolense and T. simiae parasite dots. Yet it was clearly shown that, whereas
KN4 detected all the five infected flies, TC6 did not, thus indicating that the
infections were due to T. simiae. T. simiae infections were successfully
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2 4 1
Figure 44
Detection of T. simiae CP11 in the midguts of experimentally infected G.
morsitans centralis using a modified dot-ELISA. Each of the NC membrane
strips was "dotted" with midgut sample preparations from, five infected flies
(IF1 to IF5), and five uninfected control flies (UF1 to UF5). A control sector
at the lower section of each strip was applied with lxlO5 trypanosomes per dot
of in vitro propagated T. congolense K/83/IL/97/2 (TCK), T. brucei IL2616
(TB) and T. simiae KETRI 2431 (TS). The antigen applied strips were tested
using Nannomonas subgenus-specific MoAb (KN4), T. congolense specific
MoAb (TC6) and T. brucei species-specific MoAb (KT39a). Strip 'C' was
tested as a conjugate control, and strip 'P ' was preserved without processing
through the dot-ELISA. Note the successful removal of sample stains shown
on strip 'P '.
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Figure 44
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24 2
detected in males and females of both experimentally infected G. m. centralis
and G. pallidipes.
6.4.5 Selected method of dissecting out tsetse gut tissue, choice of
sample buffer, and method of gut sample preparation
Dot-ELISA assays performed using gut tissue dissected out as
described in the materials and methods, indicated that, infecting trypanosome
species in tsetse gut could be detected using any of the gut sections.
In the preparation of tsetse gut for testing, no significant
differences were found between the use of PBS or PSG as sample buffers.
The release of trypanosomes from suspended tsetse gut tissue by
mixing through gentle pipetting and application of samples onto NC membrane
was found to be the best method. Using this method, positive reactions were
strong and easily seen. The release of trypanosomes by complete disruption of
gut tissue gave the strongest positive reactions. However, the method also
gave high background on negative sample dots, thereby making interpretation
of the results of the dot-ELISA difficult.
6.4.6 MoAbs selected for use in the modified dot-ELISA
Of the four T. brucei specific MoAbs tested in the modified dot-
ELISA, KT43/27 (IgG2 a) was found to be unsuitable, since it could not detect
T. brucei infections in the midguts of experimentally infected Glossina. The
other three MoAbs [TR7 (IgM), KT43/33 (IgGj) and KT39a (IgM)] were able
to detect those infections. KT39a was selected for routine use in the detection
of T. brucei in infected tsetse guts on the basis of its ability to strongly react
with this parasite species in that organ
Four T. congolense specific MoAbs [TC6 (IgGj), C2 (IgGj),
TC39 (IgM) and TC40 (IgM)] were tested in the modified dot-ELISA for the
detection of T. congolense in the midguts of infected tsetse flies. TC6, TC39
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243
and TC40 reacted more strongly with infected samples compared to C2.
Though TC6, TC39 and TC40 did equally well, TC6 was selected for use in
the modified dot-ELISA.
From the four Nannomonas subgenus-specific MoAbs tested,
the two IgG3 MoAbs (KN4 and TC6/25) reacted more strongly with positive
samples compared to the two IgGj (TC16 and KN5). Both KN4 and TC6/25
were found to be suitable for the identification of T. congolense and T. simiae
infections in the midguts of infected Glossina.
6.4.7 Specificity of the modified dot-ELISA
As reported under section 6.4.2.1 and 6.4.2.2, a ring-pattem
reaction occurred round some uninfected samples when tested in the modified
dot-ELISA using the T. brucei specific MoAb KT39a. Since the ring reactions
could be differentiated from specific reactions, they did not lead to difficulty in
the interpretation of the results. Hence, none of the 315 uninfected tsetse flies
that were tested using the T. brucei specific MoAb KT39a gave false positive
reactions in the modified dot-ELISA.
Of one hundred and ten (110) uninfected flies tested using the
Nannomonas subgenus-specific MoAb (KN4) and the T. congolense specific
MoAb (TC6), none reacted positively in the dot-ELISA.
6.4.8 Sensitivity of the modified dot-ELISA
The ability of the modified dot-ELISA to detect trypanosomes in
the midguts of experimentally infected tsetse flies was 91.6% (Table 29).
Further breakdown of this sensitivity into the ability to detect T. brucei, T.
congolense or T. simiae are also provided in the same table. Of 95 T. brucei,
130 T. congolense and 90 T. simiae infected flies tested, 86, 111 and 85 were
detected, giving sensitivities of 90.5, 85.5 and 94.4% respectively.
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244
Table 29
Detection of trypanosomes in the midguts of experimentally infected
Glossina by a modified dot-ELISA
Trypanosome
species
Number of
infected flies
tested
Number of flies
positive
% positive
(sensitivity)
T. brucei 95 86 90.5
T. congolense 130 111 85.4
T. simiae 90 85 94.4
Total 315 282 91.6
The number of flies detected by both T. congolense
and Nannomonas specific MoAbs used in the assays.
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In the case of the detection of T. congolense, two different
MoAbs (one Nannomonas and one T. congolense specific) were used.
Confirmed T. congolense infections were those that were detected by both the
Nannomonas and the T. congolense specific MoAbs. As shown in Table 29,
111 out of 130 T. congolense infected flies were detected by both the
Nannomonas MoAb and the T. congolense specific MoAbs, giving a sensitivity
of 85.4%. However, as shown in Table 30, more of the known T. congolense
infections were detected by the Nannomonas MoAb (117) compared to those
detected by the T. congolense specific MoAb (111). Thus, 6 out of 130
known T. congolense infected flies were detected by the Nannomonas but not
the T. congolense specific MoAb. Also, as shown in Table 30, one out of the
111 T. congolense infections detected by the T. congolense specific MoAb,
was not detected by the Nannomonas specific MoAb.
Investigations into the sensitivity of the modified dot-ELISA in
terms of the number of trypanosomes required in test samples before they
could be detected positive, revealed that, as low as 5x10s trypanosomes/ml or
1.5xl03 trypanosomes/dot could be detected in gut samples.
6.4.9 Cross-reactivity in the modified dot-ELISA
Some results did raise questions about cross-reactivity. Figure
45 illustrates one such case. The three MoAbs, TC6/25 (Nannomonas
specific), TC6 (T. congolense specific) and KT39a (T. brucei specific) used in
this experiment were shown to react specifically with the control trypanosome
dots.
As shown on the strip tested with the Nannomonas specific
antibody (TC6/25), four of the five infected flies were clearly positive,
suggesting that those flies were infected with T. congolense or T. simiae.
Three of these four flies (IF2, IF3 and IF4) were negative on the strips tested
with the T. congolense specific MoAb (TC6) as well as the T. brucei specific
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Table 30
Detection of T. congolense in the midguts of experimentally infected Glossina
by a modified dot-ELISA
Number of flies positive when tested using: Percentage of flies
detected as
T. congolense T. simiae
Trypanosome
species
Number of
infected flies
Nannomonas species-
specific MoAbs
T. congolense
specific MoAbs
T. congolense 130 117 111 85.4 4.6**
One of the flies was detected by the T. congolense, but not the Nannomonas specific MoAb.
T. congolense infections that could be mistakenly attributed to T. simiae.
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2 4 7
Figure 45
Detection of T. simiae CP813 in the midguts of experimentally infected G.
morsitans centralis using a modified dot-ELISA. Each of the NC
membrane strips was "dotted" with midgut samples from five T. simiae
infected flies (IF1 to IF5) and five uninfected control flies (UF1 to UF5),
as well as cultured control trypanosomes consisting of lxlO5 parasites per
dot of T. congolense K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T.
simiae KETRI 2431 (TS). The MoAbs used were: Nannomonas subgenus-
specific (TC6/25); T. congolense specific (TC6); and T. brucei species-
specific (KT39a). Strip 'C ' was processed through the modified dot-ELISA
as a conjugate control.
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Figure 45
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248
MoAb (KT39a), when compared with the control strip C, indicating by
exclusion that those flies were infected with T. simiae. However, the sample
from one fly IF5, appeared to be positive when tested with TC6 as well as
KT39a, thus suggesting cross-reactivity. The results also showed that the
sample from fly IF5 gave a reaction when tested on the conjugate control strip
C which was not incubated with any specific MoAb, suggesting that the
reactions seen on the sample dots from IF5 were non-specific. Further
analysis of the results revealed that, whilst the intensity of the reactions on the
sample dots from IF5 were uniform on the conjugate control, and T.
congolense and T. brucei incubated strips, it was far more intense on the strip
tested with the Nannomonas subgenus-specific MoAb. This indicated that
despite a general background given by that sample, the Nannomonas subgenus-
specific MoAb was the only one that reacted with it.
6.4.10 Stability of dotted samples
Sample "dotted" NC membrane strips were stored under
desiccated conditions at room temperature (19-26°C). Some of the strips were
retrieved and tested for antigen potency at various time intervals with selected
trypanosome species-specific MoAbs (KT39a, TC6, KN4 and TC6/25), in the
modified dot-ELISA. No significant loss in assay reactivity was observed in
up to 90 days of storage for any of the tested MoAbs. However, after 7 days
of storage, the frequency of occurrence, as well as the intensity of the non
specific ring reaction increased on strips tested with the T. brucei specific
MoAb (KT39a).
6.4.11 Detection of T. brucei in the salivary glands of experimentally
infected tsetse flies
Attempts to use the dot-ELISA developed and standardized for
the differentiation of in vitro derived trypanosomes, in detecting T. brucei in
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2 4 9
the salivary glands of infected tsetse flies were not successful. None of the
four T. brucei specific MoAbs (KT39a, TR7, KT43/33 and KT43/27) was able
to detect T. brucei (IL375) in microscopically confirmed G. m. centralis
infected salivary glands, even though each of the MoAbs reacted specifically
with T. brucei control parasite dots. The most likely causes of this failure to
detect T. brucei in infected salivary glands, were thought to be: (1)
interference due to factors such as enzymes, and (2) inability of the sample
buffers (PBS and PSG) to release infecting trypanosomes from the salivary
glands and promote their binding onto NC membrane in a way that they can be
detected.
Addition of protease inhibitors (Leupeptin and E-64) to PBS,
PSG or plain distiled water, did not solve the problem. Further
experimentation revealed that 5mM Na2EDTA was a suitable sample buffer for
the assay. Figure 46 shows the results of one experiment in which using 5mM
Na2EDTA as sample buffer, the dot-ELISA was used to detect T. brucei in the
salivary glands of infected tsetse flies. The two T. brucei specific MoAbs
(KT39a and KT43/33) reacted specifically with the T. brucei control parasite
dots, and the conjugate control strip C showed no background. The T. brucei
specific MoAb (KT39a) which was selected for diagnosing T. brucei in
infected tsetse gut was able to detect 3 of the 5 infected salivary glands. In
comparison, KT43/33 clearly detected all the five T. brucei infected salivary
glands. As shown in Figure 46, the reactivity of KT39a on the control T.
brucei parasite dot was always far stronger than that of KT43/33. The
superior ability of KT43/33 to detect T. brucei salivary gland infections was
confirmed in all other experiments.
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2 50
Figure 46
Detection of T. brucei IL375 in the salivary glands of experimentally
infected G. morsitans centralis using dot-ELISA. Each of the NC
membrane strips was "dotted" with salivary gland samples from five
infected flies (IF1 to IF5) and five uninfected control flies (UF1 to
UF5). A control sector at the lower section of each strip was applied
with lxlO5 trypanosomes per dot of in vitro propagated T. congolense
K/83/IL/97/2 (TCK), T. brucei IL2616 (TB) and T. simiae KETRI2431
(TS). The MoAbs used were: KT43/33 and KT39a, both T. brucei
species-specific. Strip 'C ' was processed as a conjugate control.
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Figure
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2 5 1
6.4.12 Specificity and sensitivity of the dot-ELISA used in detecting T.
brucei in experimentally infected tsetse salivary glands
During the development and standardization of the assay,
sample dots made from some uninfected salivary glands reacted positively in
the dot-ELISA. Whenever they occurred, such false positive reactions were
found on all dots made from the same sample, irrespective of whether they
were incubated with specific MoAb or not. The presence of such reactions on
strips tested as conjugate control (without reaction with specific MoAb),
indicated that the reactions were indeed not specific (background).
Investigations into the cause of this background revealed that it was due to
contamination of salivary gland samples with pigments originating from the
gut, through spillage of gut contents during dissection. Following this finding,
dissection of the salivary glands were always completed before dissection of
the gut in the same fly. As a result, none of 70 uninfected salivary glands
tested using the standardized dot-ELISA were positive. Of 70 T. brucei
infected salivary glands that were tested, 63 reacted positively (Table 31),
giving a sensitivity of 90%.
6.4.13 Detection of T. coneolense and T. vivax in the proboscides of
experimentally infected tsetse flies
Several methods of tsetse proboscide sample preparations were
tested using dot-ELISA. The most simplified method investigated was the
excision of the proboscis about a third way from the tip using a pair of scissors
and subsequent dotting of fluid expelled by squeezing the thorax of the fly.
Samples obtained from T. congolense or T. vivax infected tsetse proboscides
using this method were, however, not successfully diagnosed using the dot-
ELISA. In an attempt to reveal very weak, inconspicuous reactions that may
be present, the biotin/streptavidin reaction amplification steps were
incorporated into the dot-ELISA procedure. Nevertheless, none of the
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252
Table 31
Detection of trypanosomes in the salivary glands of experimentally
infected Glossina by dot-ELISA
Trypanosome Number of Number of flies % positive
species infected flies positive by test (sensitivity)
T. brucei 70 63 90
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253
microscopically confirmed T. congolense or T. vivax infected tsetse
proboscides tested, using the method, was positive. Another procedure
involving the suspension of dissected tsetse mouthparts in distiled water which
was expected to lyse infecting trypanosomes and release their constituent
antigens, was tried. However, this method of tsetse proboscide sample
preparation also failed to give positive results using known infected
mouthparts.
In order to ensure the release of trypanosomes from infected
proboscides, tsetse mouthparts were dissected in distiled water, PBS, PSG or
5mM Na2EDTA in the wells of multitest immunofluorescence slides, and the
labrum and hypopharynx cut into pieces using a small knife, and the sample
fluids transferred from the wells directly onto NC membrane strips in dots.
This method of sample preparation, permitted the detection of about 20% of T.
congolense infected tsetse proboscides using the biotin/streptavidin amplified
dot-ELISA. The use of distiled water did not give any positive results even
though microscopically confirmed infected proboscides were tested.
Microscopic examination of the sample remnants in multitest slide wells in
which mouthparts were dissected revealed the presence of some trypanosomes,
showing that not all the infecting organisms were transferred onto NC
membrane for testing. Following that finding, further experiments were
conducted using silicon coated multitest slides. The results were, however, not
better than those obtained earlier using the uncoated slides.
In order to maximise the number of trypanosomes transferred
onto NC membrane for testing, each tsetse proboscis including the thecal bulb
was separated from the insects head and tested. In this experiment., all the
infected as well as the uninfected proboscides tested positive, irrespective of
which sample buffer was used (data not shown). The loss of specificity was in
part attributable to higher concentrations of biological debris originating from
the massive thecal bulb. To reduce the amount of biological debris in the test
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25 4
samples without drastically reducing the number of trypanosomes available for
testing, the thecal bulb was cut at a position leaving about a third of it still
attached to the mouthparts, and the two thirds discarded. The mouthparts
together with the third of the thecal bulb were transferred into Eppendorf tubes
and disrupted with the tip of a pipette. The samples were then transferred onto
NC membrane in dots and tested using the amplified dot-ELISA. The results
of this experiment revealed that PBS, PSG or 5mM Na2EDTA could be used
to detect T. congolense (IL1180) infections in the mouthparts of infected G. m.
centralis.
Using this method of sample preparation, T. vivax (IL3096) was
successfully detected in the mouthparts of experimentally infected G. m.
centralis (Figure 47a). Both strips were tested using the T. vivax specific
MoAb KD32. The reactivity of the MoAb with only the T. vivax (TV) control
antigen showed that it reacted specifically in the test. Whilst none of the
uninfected proboscides was positive, the infected fly proboscides were all
positive on each of the two strips.
Figure 47b shows the results obtained for another experiment in
which two T. congolense specific MoAbs (TC6 and TC39) were used to detect
that parasite in tsetse mouthparts. Both MoAbs were shown to react
specifically with the T. congolense control antigen dots (Figure 47b).
Furthermore, each of the MoAbs detected clearly, four out of five infected
proboscides, and none of the uninfected samples.
6.4.14 Specificity and sensitivity of the dot-ELISA used in detecting T.
consolense and T. vivax in experimentally infected tsetse
proboscides
Using the standardized dot-ELISA, a total of 45 and 64
uninfected tsetse proboscides were tested using the T. congolense specific
MoAb (TC6) and the T. vivax specific MoAb (KD32), respectively. None of
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Figure 47a, b
Detection of T. vivax (A) and T. congolense (B) in the mouthparts of
experimentally infected G. morsitans centralis using dot-ELISA. Each
infected or uninfected tsetse mouthpart was processed and placed onto NC
membrane in a single dot for testing. KD32 was a T. vivax specific MoAb,
whilst TC6 and TC39 were both T. congolense specific.
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CM
CO
O
*
Two infected
mouthparts
Two uninfected
mouthparts
TV -
TCK —
TB -
TS -
Figure 47a
CM
CO
Q
*
Five infected
mouthparts
Five uninfected
mouthparts
TCK
TB -
TS -
Figure 47b
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2 5 6
these uninfected proboscides tested positive in the dot-ELISA, giving a
specificity of 100%. The overall sensitivity of the assay was, however, lower
than 50% (Table 32). Thus, of 45 T. congolense infected tsetse proboscides
that were tested, 25 reacted positively, giving a sensitivity of 55.6%, whilst
28(43.8%) of the 64 T. vivax infected proboscides were detected.
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Table 32
Detection of trypanosomes in tbe mouthparts
of experimentally infected Glossina
by dot-ELISA
Trypanosome Number of Number of flies % positive
species infected flies positive by test (sensitivity)
T. congolense 45 25 55.6
T. vivax 64 28 43.8
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The p r im a ry a im of this particular part of the study, as indicated
before, was to apply the dot-ELISA developed and standardized for the
differentiation of in vitro derived insect stage trypanosomes, to the detection of
T. brucei, T. congolense and T. simiae in the gut, T. brucei in salivary glands,
and T. congolense and T. vivax in the proboscides of experimentally infected
tsetse flies.
Unlike trypanosome suspensions from in vitro cultures, which
did not stain NC membrane upon dotting, tsetse gut suspensions were found to
stain the membrane when applied for testing. The staining colours ranged
from red through brown to black, with occasional greenish or colourless
shades, depending on the state of digestion of the blood meal in the fly. These
stains affected the specificity of the dot-ELISA when used for the detection and
differentiation of trypanosome species in infected tsetse guts. Also, false
positive reactions were encountered even in uninfected control sample dots
processed with substrate and chromogen alone, ie., without incubation with
MoAb or anti-MoAb HRPO-conjugate. This observation suggested that there
were peroxidase-like substances in the sample dots. Such substances could
utilise H202 and cause the oxidation of the chromogenic substrate (DAB), and
thereby elicit positive reactions. This indeed appeared to be the case.
According to Bursell (1970), haematin is split off from
haemoglobin in the gut of tsetse during the early stages of digestion, but it is
not absorbed from the gut. It means therefore that haematin is likely to be
present in much of the digestive residue found in the tsetse gut sections that
were dissected out and processed for testing. Moreover, Saunders and co
workers (1964) reported that some haem-proteins could utilize either oxygen or
hydrogen peroxide (H20 2) as a substrate and carry out oxidation,
hydroxylation or oxygenation. Williams (1974) called these haem-proteins,
6.5 Discussion
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peroxidases, in accordance with earlier practice, but also indicated that they
could as well be oxidases or oxygenases. Thus, the high background activity
encountered with the dot-ELISA, was attributable to: (1) staining of NC
membrane by pigmented gut samples, and (2) false reactivity resulting from
oxidation of DAB by haem.
It was reasoned, therefore, that one method of eliminating the
non-specific reactions was to change the enzyme/substrate system to one that
did not require the addition of free H20 2 to the solution. To achieve this, the
HRPO enzyme was substituted for glucose oxidase, which made it possible to
use a substrate solution in which H2O2 was substituted for glucose. This
change of enzyme, however, did not substantially reduce the non-specific
staining. Moreover, the use of glucose oxidase-conjugated antibodies,
introduced an additional problem of higher "assay background" which made it
more difficult to detect weak positive reactions. A similar contribution to high
assay background has been reported for alkaline phosphotase-conjugated
antibodies (Pappas, 1988b). Consequently, the use of glucose oxidase-
conjugated antibodies in the dot-ELISA was abandoned.
Another possibility was to degrade the haem-proteins in the test
samples through a chemical process, such as oxidation, prior to analysis of the
samples with the dot-ELISA. The most suitable of the oxidizing agents tried
was H20 2.
H20 2 is a strong oxidising agent. Earlier research by Lemberg
(cited by Jackson, 1974) had shown that the first step in haemoglobin
catabolism is an oxidative degradation of the molecule, which leads to
separation of the haem from globin and the loss of iron. Treatment of
haematin with excess H20 2 might lead to a similar degradation of the haem-
protein, with accompanying loss of colour. This discovery that H20 2 could be
used to decolorize pigmented samples obtained from the guts of laboratory
reared tsetse flies, without affecting the integrity of trypanosome species-
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260
specific diagnostic antigens, suggests that: (1) the modified dot-ELISA that
utilized this innovation, may do even better when it came to detecting and
differentiating between trypanosome species in naturally infected Glossina;
since such flies are known to digest their blood meals faster (Langley, 1967b)
and will, therefore, present less staining problems; (2) H2O2 destaining may be
potentially useful in the development of colorimetric assays for the detection of
parasites in pigmented samples.
Tellez-Giron, Ramos, Dufour, Alvarez and Montante (1987)
reported the occurrence of a non-specific ring-pattem reaction in a dot-ELISA
that they used for detecting Cysticercus cellulosae antigens in cerebrospinal
fluid. There was, however, no explanation offered for the occurrence of the
so-called "ring phenomenon". In this study, a similar non-specific "ring-
pattem" reaction occurred on some sample dots, despite the use of H2O2 .
These ring reactions did not occur on samples tested as conjugate controls, thus
showing that specific MoAb played a role in their occurrence. Of the four T,
brucei specific MoAbs tested with the dot-ELISA, only one (KT39a) induced
the ring reactions, although not all samples tested with that particular MoAb
showed the phenomenon. Despite the need to elucidate the mechanisms
responsible for the ring formation, it has been shown in this work that the
presence of the rings did not hamper interpretation of the results of the
modified dot-ELISA.
The inability to enhance the reactivity of the T. congolense
specific MoAbs by lysing the infecting organisms in suspension, was
attributable to two causes. Firstly, it is known that some detergents such as
NP-40 could remove protein from NC membranes (Lin and Kasamatsu, 1983),
suggesting that their presence in the sample suspensions could reduce the
binding efficiency of the antigens. Secondly, lysing the trypanosomes,
together with the mass of biological debris present in the gut suspensions,
could enormously increase the competition for binding between released
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trypanosome antigens and other substances. The method of applying T.
congolense infected gut suspensions onto NC membrane before lysing the
parasites in the bound sample, circumvented the above listed problems and led
to successful identification of these infections with the modified dot-ELISA.
The success of this procedure could be explained by the earlier finding that the
T. congolense specific MoAbs detected antigens that were not exposed on the
surface of intact trypanosomes (Chapter 4).
Parasite detection and identification methods intended for field
use need to be simple, in addition to being specific and sensitive. Methods
that reduce time spent on sample preparation are, therefore, desirable. In this
study, tsetse gut samples collected by simply cutting away the distal end of the
insect's abdomen and squeezing out its contents for testing in the dot-ELISA,
gave results that were comparable, in terms of detection and identification of
parasites, to those following the more time consuming methods of tsetse
midgut dissection. The suitability of this simplified method of tsetse gut tissue
extraction for the dot-ELISA, was indicated by the finding that none of the
trypanosome species-specific MoAbs cross-reacted with T. grayi, which is
known to reside mainly in the hindgut of tsetse flies infected with the species
(Hoare, 1972).
The tsetse gut sample preparation methods, employed in this
dot-ELISA, afford the opportunity of analysing multiple dots of the same
sample, using different species and/or subgenus-specific MoAbs. This has
made it possible, for instance, to use T, congolense specific MoAbs and
Nannomonas subgenus-specific MoAbs to specifically detect T. congolense
infections in tsetse gut, or detect T. simiae infections in this organ in the same
fly, by exclusion of T. congolense. Also, with the present dot-ELISA, it
should be possible to tell whether a tsetse fly was infected with T. grayi in the
gut, by excluding the presence of T. congolense, T. simiae, and T. brucei.
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Theoretically, it would be expected that all T. congolense
infections should be detected by T. congolense specific MoAbs and by the
Nannomonas subgenus-specific MoAbs. However, it was shown in this study
that T. congolense infections could be detected by Nannomonas specific
MoAbs without being detected by T. congolense specific MoAbs. It is,
however, important to note that the frequency of occurrence of this discordant
reaction was low (<5%) as only 6 out of 117 T. congolense infected flies
were detected by the Nannomonas but not by the T. congolense specific
MoAb. This inability of the T. congolense specific MoAb to detect all the T.
congolense tsetse gut infections revealed by the Nannomonas MoAb, could be
attributed to differences in sensitivity between the two groups of MoAbs.
Another observation made in this study was that one T.
congolense tsetse gut infection out of 110 (<1%) was detected by the T.
congolense specific MoAbs without being detected by Nannomonas specific
MoAbs in the same experiment. Two possible explanations could be offered
for this unusual reactivity: Firstly the occurrence of 1 out of 110 is statistically
insignificant and could be simply due to variations in test conditions, such as
the amount of residual Triton X-114 or H2O2 that remained on a test strip
following washings. Secondly, it might be the result of the destruction of the
Nannomonas subgenus-specific antigen by factors such as enzymes in tsetse gut
which nevertheless did not affect the T. congolense species-specific antigen.
The likelihood of the second possibility was supported by earlier findings, that
the T. congolense specific antigenic epitope(s) were of protein nature, whilst
the Nannomonas specific antigenic epitope(s) were of carbohydrate nature
(Chapter 4).
The opportunity to test each tsetse gut sample at least 15 times
using the dot-ELISA, made the technique even more suitable for the purpose
of detecting and differentiating between trypanosome species in infected tsetse
gut. This is because, five main species of trypanosomes (T. brucei, T.
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263
congolense, T. simiae, T. suis and T. grayi) are known to infect the gut of the
Glossina species. This ability to replicate tsetse gut originated test samples,
therefore, offered two additional advantages. The first was the possibility of
detecting mixed infections in tsetse by employing the different trypanosome
species and subgenus-specific MoAbs. The second advantage was the
opportunity to utilize undigested tsetse blood meal in unused gut samples, in
the identification of tsetse host, using methods such as described with the
micro-plate ELISA developed by Rurangirwa, Minja, Musoke, Nantulya,
Grootenhuis and Moloo (1986).
In this study, a total of 315 tsetse flies experimentally infected
with T. brucei, T. congolense or T simiae in the guts, were tested using the
modified dot-ELISA. The sensitivity of the assays was high, as 90.5% of the
tsetse infected with T brucei, 85.4% of those infected with T. congolense and
94.4% of those infected with T. simiae were correctly identified. This gave an
overall sensitivity of 91.6% for detecting and differentiating between
trypanosome species in the guts of experimentally infected tsetse flies. The
specificity of these assays was greater than 99.9%.
Decreased reactivity of the T. congolense specific antigen was
recorded when culture-derived vector stage trypanosomes were applied and
stored on NC membrane at room temperature (17-26°C) for more than 60 days
(Chapter 5). However, no significant loss in reactivity was observed in up to
90 days of storing trypanosome infected tsetse gut samples under similar
conditions. This stability of the antigens, introduces a degree of flexibility in
this test, since the collected samples need not be analysed at once.
The T. brucei specific MoAb (KT39a) which was used for
detecting this parasite in infected tsetse gut, was not used for the detection of
the parasite in the salivary glands of the vector. This was because, another T.
brucei specific MoAb (KT43/33) performed better and was, therefore,
selected. This difference in the performance of the two MoAbs was explained
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as follows. It was found in Chapter 4 of this thesis that, KT39a bound to an
antigenic epitope which was only partially sensitive to proteinase-K and which
was located on a 90 kDa antigen peptide. On the other hand, KT43/33 bound
to an antigenic epitope which was completely susceptible to proteinase-K and
which was located on an antigen which localized in a series of peptide bands
ranging between 21 and 47 kDa. These findings suggested that the T. brucei
species-specific antigens detected by the two MoAbs (KT39a and KT43/33),
were indeed different. It is, therefore, possible that the T. brucei specific
antigens detected by the two MoAbs are expressed in different quantities in the
different life cycle stages of the parasite. If this were the case, then the
antigen detected by KT39a was better expressed in the procyclic stages of the
parasites which predominate in the vector's midgut, whilst the antigen detected
by KT43/33 was better expressed in the epimastigote and metacyclic stages in
the vector's salivary glands. Another possible cause of the differences in the
performance of the two MoAbs, was differential susceptibility of the specific
antigens to degradative enzymes that may be present in the tsetse salivary
glands.
As shown in the case of the identification of trypanosomes in the
guts of infected tsetse flies, the sensitivity of the dot-ELISA for the detection
of T. brucei in infected salivary glands was high (90%). The specificity of the
assay was greater than 99.9%. Furthermore, the opportunity to test each pair
of tsetse salivary glands at least three times, indicated that if the need arose,
and MoAbs were made against T. suis which can also infect the vector's
salivary glands, then this parasite could also be tested for alongside T. brucei
in the dot-ELISA.
It has also been shown in this work that both T. congolense and
T. vivax could be detected in the proboscides of infected tsetse flies.
However, the sensitivity of the dot-ELISA in detecting these two trypanosome
species in the target organ was low (55.6% for T. congolense and 43.8% for
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2 6 5
T. vivax). This low detection rate of trypanosomes in the proboscis of
Glossina, might be related to three factors: (1) the relative numbers of T.
congolense or T. vivax parasites present in the proboscis at a certain point in
their life cycles in the vector; (2) difficulties in releasing trypanosomes from
the proboscis as a result of anatomical peculiarities of that organ, and (3)
differences in sensitivity of the trypanosome species-specific MoAbs employed
in the study. The inability to test each tsetse proboscis more than once, is
clearly a drawback. One way to circumvent this limitation is to randomly
place suspected tsetse proboscides into two groups, and to test one group with
T. vivax specific MoAb and the other with T. congolense specific MoAb.
From this study, it could be concluded that the dot-ELISA is
potentially a practical method for the diagnosis of trypanosome infections in
tsetse flies. However, in order to determine the full potential of this
technique, there was the need to investigate its applicability in the field. This
was done, and the results obtained were recorded in the next chapter.
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CHAPTER 7
266
FIELD EVALUATION OF A DOT-ELISA DEVELOPED FOR THE
DETECTION AND DIFFERENTIATION OF TRYPANOSOME
SPECIES IN INFECTED TSETSE FLIES (GLOSSINA SPP.)
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A rapid, visually read, dot-ELISA developed for the detection and
differentiation of trypanosome species in tsetse flies (Glossina spp.), was field
tested alongside the standard fly dissection method on a ranch in south eastern
Kenya.
Of a total of 104 G. pallidipes dissected, two were found to be
infected with trypanosomes in their midguts. By the dissection method the
infecting trypanosome species could not be identified, as both flies were free
from salivary gland infections. However, using the dot-ELISA, the two flies
were shown to be infected with T. congolense in their midguts. The midguts
of an additional 6(5.8%) of the 104 G. pallidipes tested positive for T.
congolense in the dot-ELISA, even though no trypanosomes were seen on
dissection. The infection rate for this fly species as determined using the dot-
ELISA, therefore, was 7.7% for T. congolense in midgut infections compared
to 1.9% identified by fly dissection. The salivary glands and mouthparts of
the 6 additional tsetse flies identified by dot-ELISA, were all negative as
determined by the two techniques.
None of 390 G. longipennis flies dissected and examined for
trypanosomes in the midgut, salivary glands and mouthparts was shown, by
this method, to be infected. Using the dot-ELISA, however, 17(4.4%) of the
flies tested positive for T. congolense in the midguts, whilst the salivary glands
and mouthparts of the same flies were negative.
Thus, the dot-ELISA appears to be more sensitive than the fly
dissection method under field conditions. Moreover, the dot-ELISA was
performed in the field without electricity. It was simple to perform, and was
not affected by high ambient temperatures (22-32°C), or by contamination of
reactants with dust.
7.1 Summary
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The tsetse dissection method, first introduced by Lloyd and
Johnson (1924), is the method used in routine epidemiological surveys to
determine trypanosome infection rates in Glossina. This is still the case even
though a recombinant DNA technique was introduced by Kukla and colleagues
(1987), for the diagnosis of trypanosome infections in the tsetse fly. The
reason for this is partly because, the present DNA probes cannot recognise all
the intra-species variants of targeted trypanosome species. Secondly, the DNA
technique is not simple enough to be performed in most laboratories.
In the studies recorded in this Chapter, the dot-ELISA developed
for differentiating between in vitro propagated trypanosome species (Chapter
5), and which was successfully modified for detecting and differentiating
between infecting trypanosome species in the mouthparts, salivary glands or
midguts of experimentally-infected Glossina species (Chapter 6), was
evaluated in the field for the diagnosis of natural trypanosome infections in the
vector.
It is shown here, that the dot-ELISA developed hereto, is capable
of detecting and identifying infecting trypanosome species in naturally infected
tsetse flies when the assay was performed under field conditions.
7.2 Introduction
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269
7.3.1 The dot-ELISA kit
7.3.1.1 Nitrocellulose CNC) membrane template
Lines were drawn on NC membrane sheets to form a grid
consisting of square and rectangular shaped areas as shown in Figure 48. The
columns representing the outlines of demarcated strips were numbered, and in
vitro propagated procyclic T. congolense (TCK), T. brucei (TB) and T. simiae
(TS), and epimastigotes of T. vivax (TV) were applied, lxlO5
trypanosomes/dot onto each of the demarcated NC membrane strips as shown
in Figure 48, to provide the controls. The NC membrane sheets were sealed
in polythene bags and transported to the field for use.
7.3.1.2 Materials
7.3 Materials and methods
1. Two Bio-Rad slot incubation trays
2. One 500ml plastic measuring cylinder
3. Two 500ml plastic beakers
4. One rubber pipette aid
5. 10ml plastic pipettes
6. 0.5 to 10/d adjustable pipette and pipette tips
7. 1.5ml Eppendorf tubes
8. Multitest IF A slides.
7.3.1.3 Chemicals, reagents and buffers
Chemicals, reagents and buffers, enough for screening at
least 1,000 tsetse flies, were transported to the field. These
were:
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Figure 48
A nitrocellulose membrane grid showing demarcated spaces for sample
application,
TCK = lxlO5 trypanosomes/dot of T. congolense Kilifi type culture
procyclics.
TB = lxlO5 trypanosomes/dot of T. b. brucei culture procyclics.
TS = lxlO5 trypanosomes/dot of T. simiae culture procyclics.
TV = lxlO5 trypanosomes/dot of T. vivax culture epimastigotes.
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Figure
48
< CO 03 O
Tv
* * I *
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1. 5Qmg weights of 3-3'diaminobenzidine (DAB) in 1.5ml
Eppendorf tubes, each enough for assaying samples from
100 tsetse flies
2. 5g weights of skimmed milk in sealed polythene bags, each
enough for assaying samples from 50 tsetse flies
3. 1ml of concentrated hydrochloric acid
4. 50ml of 30% hydrogen peroxide (H20 2)
5. Aliquots of trypanosome species or subgenus-specific
MoAbs and goat anti-mouse horseradish peroxidase
(HRPO)-conjugated antibodies kept on ice in thermos
flasks.
6. 100ml of phosphate buffered saline, pH 7.4
7. 100 ml 5mM Na2EDTA buffer
8. 1.5 litres of xlO concentrated Tris buffered saline, pH 8.
9. 2ml of Triton X-114
10. 10 litres of deionised water
11. 200ml of Phosphate/Na2EDTA buffer
7.3.2 The dissecting kit
7.3.2.1 Equipment
1. Dissection microscope
2. Compound microscope
7.3.2.2 Other materials
1. Microscope slides and cover slips
2. Kit of dissecting instruments
3. Phosphate buffered saline, pH 7.4, listed under 7.3.1.3
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272
7.3.3 Study area and trapping of tsetse flies
7.3.3.1 Study area
Field evaluation of the dot-ELISA was conducted at the Galana
Ranch which covers an area of approximately 6000 km2 in the coastal
hinterland of Kenya. The mean altitude is 270 m, with an average annual
rainfall of 550 mm (Wilson, Gatuta, Njogu, Mgutu and Alushula, 1986). The
vegetation consists of riverine thickets along the Galana river, and thick coastal
bush in the east which gives way to grasslands and scattered thickets in the
west. Four species of tsetse have been identified on this ranch, inhabiting
different ecological zones that make up to 35% of the area of the Ranch. The
tsetse species were: Glossina longipennis in the drier savannah areas, away
from the river; G. austeni, restricted to the river-bed; G. brevipalpis, in
forested areas in the east; and G. pallidipes in thickets along the river and in
the east.
7.3.3.2 Trapping of wild tsetse flies
Male and female G. longipennis and G. pallidipes flies were
trapped from their natural habitats using the F4 and biconical traps,
respectively. The F4 traps (Figure 49) were set up in the late afternoon at
about 4.00 pm in the grassland areas infested by G. longipennis and emptied
the following day at about 9 am. Biconical traps (Figure 50) were also set up
around 4.00 pm, in the G. pallidipes infested areas, in the east of the Ranch,
and emptied the following day at about 4.00 pm.
7.3.4 Experimental design
Tsetse flies were killed by anaesthesia using chloroform, and sorted
into groups according to species. The flies were also separated into tenerals
and non-tenerals. The teneral flies were discarded.
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Figure 49. F4 trap used for catching G. longipennis in the savannah areas at
the Galana Ranch.
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Figure 50. Biconical trap used for catching G. pallidipes in the thickets in the
west of the Galana Ranch.
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As shown in Figure 51 for G. pallidipes, each species of tsetse was
first separated on the basis of sex. The flies in either sex (male and female)
were subsequently sorted randomly, each into two groups; M l and M2 for the
males and; FI and F2 for the females (Figure 51). The males in group M l
were then added to the females in group FI to form batch 1 tsetse flies whose
mouthparts were dissected and examined microscopically, and tested with a T.
vivax specific MoAb (KD32/48.17) using the dot-ELISA described in Chapter
6. The mouthparts of the second batch of flies consisting of flies from M2 and
F2, were also dissected, but tested with a T. congolense specific MoAb
(TC6/42.6.3) in the dot-ELISA.
The midgut and salivary glands of all the flies were also dissected
and examined microscopically for trypanosomes and also tested using the dot-
ELISA as described in Chapter 6.
7.3.5 Dot-ELISA procedure
Tsetse proboscide, midgut and salivary gland samples were
prepared and applied onto the NC membrane template (Figure 48) following
the procedure described in Chapter 6, and the NC membrane cut out into
strips. The dot-ELISA procedures were also as previously described (Chapter
6, section 6.3.7) except that the shaking of the slot incubation trays was
accomplished manually.
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Figure 51
Sorting G pallidipes into two batches, for testing for infecting trypanosomes in
the mouthparts. Flies in 'Batch 1' were tested with a T. congolense specific
MoAb, whereas flies in 'Batch 2' were tested with a T. vivax specific MoAb.
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G. pa/I/c/fpes
Males Females
Males(M1) Males(M2) Females(FI) Females(F2)
1 * ' l
! ' s
M1 + F1 = Batch 1 M2 + F2= Batch 2
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7 .4 . 1 Detection of trypanosome infections in tsetse flies using the
dissection method
The mouthparts, salivary glands and midguts of 104 G. pallidipes
(44 males and 60 females), and 390 G. longipennis (154 males and 236
females) were dissected and examined for trypanosomes. Two of the G.
pallidipes flies (1.9%), both of them females, were found to be infected with
trypanosomes in the midguts (Table 33), and no trypanosomes were seen in the
mouthparts or salivary glands of the same flies. Trypanosomes were not
detected in any of the G. longipennis.
7.4.2 Detection of trypanosome species in tsetse flies using the dot-
ELISA
The mouthparts, salivary glands and midguts of all the dissected
tsetse flies were also tested using the dot-ELISA.
Of the 104 G. pallidipes that were tested, 8(7.7%) were positive
for T. congolense in the midgut (Table 33). These included the two flies
which were determined by the dissection method to be infected with
trypanosomes in their midguts. Gut samples from all the 8 flies reacted
positively with the T. congolense specific MoAb as well as with the
Nannomonas subgenus-specific MoAb (Table 34). No T. vivax or T. brucei
antigens were detected in any of the organs that were tested.
Out of the 390 G. longipennis tested using the dot-ELISA,
17(4.3%) were positive for trypanosome infections in the midguts (Table 33).
Nine of those 17 midguts gave positive reactions with T. congolense and the
Nannomonas specific MoAbs (Table 35), whilst the remaining 8 midguts tested
positive with only the T. congolense specific MoAb (Table 35).
74 Results
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Table 33
Detection of trypanosome infections in the midguts of G. pallidipes and
G. longipennis using the dissection and dot-ELISA techniques
Tsetse
species
Number
tested
Dissection
Number (% positive)
Dot-ELISA
Number (% positive)
G. pallidipes 104 2(1.9%)* 8(7.7%)
G. longipennis 390 0 17(4.3%)
Total 494 2(0.4%) 25(5.1%)
Infections detected only in the midgut by the fly dissection method.
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Table 34
Detection and differentiation of trypanosome species
in the midguts of G. pallidipes using the dot-ELISA
Reactivity of tsetse midguts with different
Tsetse flies trypanosome species-specific MoAbs
detected b y --------------------------------------------------------------------------
assay T. congolense T. brucei Nannomonas T. vivax
1 + + -
2 + + -
3* + + -
4 + +
5* + - +
6 + +
7 + +
8 + +
*
Tsetse flies with infected midguts as determined by
the dissection method.
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Table 35
Detection and differentiation of trypanosome species
in the midguts of G. longipennis using the dot-ELISA
Reactivity of tsetse midguts with different
Tsetse flies trypanosome species-specific MoAbs
detected by ------------------------------------------------------------------------
assay T. congolense T. brucei Nannomonas T. vivax
1 + +
2 + - + -
3 + + -
4 + + -
5 + + -
6 + + -
7 + + -
8 + + -
9 + - + -
10 + -
11 + - - -
12 + -
13 + -
14 + -
15 + -
16 + -
17 + -
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7.4.3 Problems encountered, and special observations made during tl
performance of the dot-ELISA under field conditions
In the laboratory, all incubations in the dot-ELISA were made
slot trays under continuous shaking on an electrical powered gentle rocke
Under field conditions, the unavailability of electrical power necessitate
improvisation. Consequently, shaking of the slot trays during the varioi
incubation steps in the first dot-ELISA performed in the field w;
accomplished manually by tilting the trays in a rocking motion continuous]
for 1-2 min, and then allowing the trays to stand for 15 min before repeatiri
the shaking. The reactivity of the specific MoAbs on the control trypanoson:
dots included in the test were, however, weaker than those obtained in tl
laboratory using the electric rocker. In order to eliminate the effect c
interrupted shaking on the reaction intensities, an improvised technique we
tested. The improvisation consisted of suspending the incubation trays on
rope that was tied to the branch of a tree, and swinging to emulate the simp]
pendulum motion (Figure 52). In addition, the trays were rocked manually a
before. This procedure increased the intensity of the reactions in the doi
ELISA.
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Figure 52. Field improvisation of a rocker during incubations.
Note the suspended tray.
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The aim of the studies conducted in this Chapter was to evaluate
the applicability of the dot-ELISA in terms of its ability to detect and identify
trypanosome species involved in natural infections in the vector, when the
assay was performed under field conditions. The field conditions under which
the dot-ELISA was evaluated, constituted a realistic situation likely to be
encountered in other tsetse infested areas.
The NC membrane strips, applied with control trypanosomes, and
the reagents and buffers proved to be stable over the period of one week that
they were used in the field. The presence of strong winds, coupled with the
abundance of sandy dust, brought about contamination of reagent solutions
with dust and plant debris during the performance of the assays. However,
this contamination, together with the high ambient temperatures (22 to 31°C)
prevailing during the assays, did not adversely affect the results. This
indicated that the dot-ELISA was robust as far as conditions such as
temperature and dust were concerned.
In this study, only 2 midgut infections were detected in a total of
494 tsetse flies that were screened using the dissection method, on the Galana
Ranch. However, in an earlier study conducted on the same ranch by Wilson,
Gatula, Njogu, Mgutu and Alushula (1986), T. vivax, T. congolense and T.
brucei infection types were all detected in tsetse flies, using the dissection
method, with T. vivax infections being the most common. The most likely
explanation for these differences in observations made in the present study and
that of Wilson et al, (1986), is that, the tsetse and trypanosomiasis control
programme being implemented on the ranch (Opiyo, Njogu and Omuse, 1990)
may have altered the status of trypanosome infections and transmission.
This field study revealed that the trypanosome infection rate in G.
pallidipes was higher than that in G. longipennis, regardless of the technique
7 .5 Discussion
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used. This finding was in agreement with an earlier report which showed that
G. pallidipes was the major vector of trypanosomiasis on the Galana Ranch
(Opiyo, Dolan, Njogu, Sayer and Mgutu, 1987).
The identity of the trypanosome species involved in the two midgut
infections which were detected in G. pallidipes could not be determined using
the dissection method, since there were no accompanying infections in the
mouthparts or salivary glands of the two flies. Using the dot-ELISA,
however, it was possible to identify T. congolense as the parasite species
involved, since the parasites reacted with both the Nannomonas and the T.
congolense specific MoAbs. Furthermore, it was possible to ascertain the
absence of T. brucei in those infections. Unfortunately, at the time that this
study was conducted, the T. simiae specific MoAb reported in Chapter 4 had
not been derived, and was not, therefore, included in the evaluation.
It was also found that the dot-ELISA detected T. congolense
antigens in the midguts of some parasitologically negative flies. This was a
new observation that could be attributed to three possible causes, namely: (1)
correct identification of infected tsetse by the dot-ELISA as a result of
differences in sensitivity between the two tests, (2) false detection of
uninfected tsetse due to reactivity of MoAbs with circulating T. congolense
antigens present in the blood meal ingested from infected hosts, and (3) false
detection of uninfected tsetse due to reactivity of MoAbs with trypanosome
antigens originating from ingested whole bloodstream form trypanosomes that
were unable to establish an active infection. However, this observation would
appear to indicate that the dot-ELISA had a higher sensitivity compared with
the tsetse dissection method. A statistical comparison of the dissection
technique with the dot-ELISA using Chi-square analysis, indicated that the two
tests were significantly different in their ability to detect trypanosomes in tsetse
midgut, at P< 0.05. This possibility of diagnosing trypanosome infections in
the midguts of tsetse flies, even though no infecting parasites are seen using
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2 8 5
the dissection method, has not been indicated or discounted in the use of the
recombinant DNA technique. This is simply because, in all the studies that the
recombinant DNA technique was tried in the field, only flies shown by the
dissection method to be infected with trypanosomes, were tested.
It was also interesting to note that gut samples from some of the
parasitologically negative tsetse flies could react with the T. congolense
specific MoAb without reacting with the Nannomonas subgenus-specific MoAb
in the dot-ELISA. Three likely explanations could be offered for this unusual
reactivity. Firstly, it could be due to differences in the levels of biochemical
substances such as enzymes which are able to affect the integrity of the epitope
on the Nannomonas subgenus-specific antigen, without affecting the T.
congolense specific antigen. If this were true, it would mean that the species
of tsetse may be an important factor, since the observation was associated with
G. longipennis, but not G. pallidipes. Secondly, it could be that the G.
longipennis were infected with different T. congolense variants, some of which
may not be expressing the Nannomonas subgenus-specific antigen detected by
the MoAb. This possibility is however unlikely, since the Nannomonas
specific MoAb was able to react with T. congolense organisms isolated from
different geographical areas (Chapter 4). Thirdly, the T. congolense specific
MoAb could be cross-reacting with unidentified antigens present in the tsetse
gut. However, this possibility was also thought to be unlikely, since in
extensive studies with experimental tsetse flies (Chapter 6), no cross-reactivity
was observed.
The results obtained from this limited evaluation of the dot-ELISA
clearly showed that the technique was a practical alternative to the dissection
method which is currently employed in the diagnosis of trypanosome infections
in Glossina species. This is especially so, considering the fact that each of the
MoAbs used had been shown to react with various trypanosome isolates from
different geographical areas. Besides, the materials required can easily be
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transported to field locations, and the assay could be performed without the
need for electricity. The test is rapid, simple to perform, and will be
inexpensive in screening large numbers of tsetse flies at a time. Moreover, it
is specific and detects more trypanosome infections in field caught tsetse flies
in comparison with the dissection method. These are strong indications that
the dot-ELISA could contribute greatly to studies aimed at further elucidating
the role played by the tsetse fly in the epidemiology of the African
trypanosomiases.
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CHAPTER 8
287
GENERAL DISCUSSION
AND CONCLUSIONS
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Since the discovery that tsetse flies were the main vectors of the
African trypanosomiases, attempts have been made to reduce the disease
prevalence by vector control and by the use of trypanocidal drugs. These
methods have, however, been expensive and relatively unsuccessful. As a
result, vast areas of land are still infested with tsetse flies, while areas
previously cleared of the fly are prone to reinfestation (MacLennan, 1981).
This, together with the emergence of drug resistant strains of trypanosomes
(Kupper and Wolters, 1983; Pinder and Authie, 1984), reveals the true extent
of the threat posed by trypanosomiasis.
Estimation of the trypanosomiasis risk or challenge to domestic
animals or humans, requires the determination of several factors, including
tsetse relative density, the proportion of blood meals taken from target hosts,
and trypanosome infection rates in tsetse (Lloyd and Johnson, 1924; Challier
and Laveisiere, 1973). Assessment of these parameters is currently important,
as sites are investigated for trypanosomiasis risk in relation to productivity of
trypanotolerant breeds (Leak et al., 1988).
The diagnosis of trypanosome infections in the tsetse fly, at
present, is by dissection. This method, however, can only be used to identify
the parasites up to the subgeneric level (Hoare, 1972; Stephen, 1986;
McNamara and Snow, 1991). It is, therefore, essential to develop a more
accurate method that is capable of detecting and differentiating between
trypanosome species in infected tsetse flies. In this thesis, the suitability of a
MoAb-based approach was investigated.
Several species of parasitic protozoa (including Plasmodia spp.,
Leishmania spp., T. cruzi and Trypanosoma spp.) possess species and/or
subgenus-specific antigens (Santoro, Cochrane, Nussenzweig, Nardin,
Nussensweig, Gwardz and Ferreira, 1983; Flint, Schechter, Chapman and
Miles, 1984; McMahon-Pratt, Bennet and David, 1982; Parish, Morrison and
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Pearson, 1986; Nantulya et al., 1987). In the case of the Trypanosoma, this
had been shown by the generation of MoAbs that are specific to the T.
congolense species, and the Nannomonas, Trypanozoon and Duttonella
subgenera. However, no MoAbs specific to T. simiae or any of the subspecies
that constitute the Trypanozoon subgenus had been produced. In studies
described in Chapter 4, a MoAb specific to T. simiae (KNS7/14.X) was
produced using spleen cells from a BALB/c mouse that had been immunized
with purified T. simiae antigens obtained using the purification procedure
described by Ijagbone et al., (1989). The production of a T. simiae specific
MoAb has shown for the first time that both trypanosome species within the
Nannomonas subgenus (T. congolense and T. simiae), possess immunogenic
species-specific antigens that could be used to differentiate between them.
The potential usefulness of the trypanosome species-specific
MoAbs as diagnostic reagents was demonstrated through their reactivity with
vector stages of the parasites that had been isolated from different geographical
areas (Chapter 4). In those experiments, it was recorded that the majority of
the MoAbs could also detect the bloodstream forms of the target parasite
species, indicating that some of the MoAbs may also be useful in the diagnosis
of trypanosomiasis in the mammalian host. A similar observation was made
by Nantulya and co-workers (1987) for MoAbs that they produced against
membrane antigens of procyclic trypanosomes, and which were later utilized in
developing diagnostic assays for detecting circulating bloodstream trypanosome
antigens in both infected humans and animals (Nantulya and Lindqvist, 1989;
Nantulya, 1989; Nantulya, Doua and Molisho, 1992).
Since it had previously been established that procyclic tsetse midgut
forms and culture forms of the African trypanosomes express similar antigens
(Richardson et a l , 1986; Pearson, Moloo and Jenni, 1987), efforts were first
initiated to establish a simple, sensitive and specific MoAb-based assay that
could detect and differentiate between culture derived T. brucei, T. congolense
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and T. simiae procyclics, and T. vivax epimastigotes. The NC membrane-
based dot-ELISA was the preferred choice. The reason for this was that, this
technique had been shown to be simple, sensitive, specific and field portable
(Pappas, 1988a). Ensuing experiments led to the development and
standardization of a simple, sensitive and specific NC membrane-based dot-
ELISA (Chapter 5) that utilized trypanosome species-specific MoAbs in the
detection and differentiation of in vitro propagated forms of the
aforementioned trypanosome species. In these experiments, the dot-ELISA
correctly identified the trypanosome species in both single and artificially
mixed trypanosome populations. This finding showed that the trypanosome
species present in artificial cultures could be ascertained using the dot-ELISA.
This was considered important since culture derived trypanosomes were
becoming increasingly utilized in trypanosome research (Ross and Taylor,
1990). Hence, there was the need for simple reliable techniques that could be
used in identification and confirmation of the propagated trypanosome species.
The finding also indicated that the assay might be suitable for detecting and
differentiating between trypanosome species in infected tsetse flies.
Genotypic diversity had been recorded among members of the
Nannomonas subgenus, especially the T. congolense species (Majiwa, Masake,
Nantulya, Hamers and Matthyssens, 1985; Majiwa, Hamers, van Meirvenne
and Matthyssens, 1986). As a result of this diversity, efforts aimed at
producing a DNA probe that could hybridize to all the intra-species variants of
T. congolense, have been unsuccessful.
As reported in Chapter 4, the T. congolense specific and
Nannomonas subgenus-specific MoAbs reacted with all the T. congolense
isolates including the Savannah, Kilifi and riverine-forest types that were
tested. This result showed that despite the reported genotypic differences,
these T congolense genotypes were closely related antigenically, thus
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suggesting that the MoAb approach to diagnosis of trypanosome infections in
Glossina may have an advantage over the recombinant DNA technique.
The gut of an infected tsetse fly contains trypanosomes as well as
digestive residue originating from ingested blood meal. The digestive residue
is normally pigmented, mostly by haematin which is split off the haemoglobin
molecule early in the digestion of tsetse blood meal, but which is not absorbed
(Bursell, 1970). Efforts to test tsetse gut samples for the presence of infecting
trypanosomes using the NC membrane-based dot-ELISA (Chapter 5)
encountered non-specific background. This background was attributable to
two likely causes (Chapter 6); namely, (1) staining of NC membrane by
pigmented gut samples, and (2) false reactivity resulting from the oxidation of
the chromogenic substrate (DAB) by haem. The non-specific stains were
removed using hydrogen peroxide (H2O2 ) as a destaining agent in a modified
dot-ELISA, without any significant effect on the integrity of the trypanosome
species-specific diagnostic antigens (Chapter 6). This ability of H20 2 to
decolorize NC membrane applied pigmented gut samples was attributed to its
(H20 2's) oxidative degradation of haem (Jackson, 1974), and of haematin
(Chapter 6). It should be of interest to further investigate the ability of H20 2
to decolorize NC membrane applied infected gut samples as well as faecal
material obtained from other haematophagous arthropod vectors, such as the
Triatomine bugs that transmit T. cruzi. This could lead to further development
of this H20 2 innovation and allow maximum utilization of colorimetric assays,
which are generally simple and can be read visually (without the aid of
sophisticated equipment).
The modified dot-ELISA was shown to be capable of identifying T.
brucei, T. congolense and T. simiae organisms in the guts of experimentally
infected tsetse flies. The assay had an overall sensitivity greater than 90
percent and a specificity greater than 99.9 percent. This successful detection
of trypanosome species in the guts of laboratory-colonized tsetse flies,
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suggested that the modified dot-ELISA would be even more readily applied in
the detection of trypanosome species in wild tsetse flies which are known to
digest their blood meals faster (Langley, 1967a).
Two main trypanosome species (T. brucei and T. suis) are known to
infect the salivary glands of the Glossina species (Hoare, 1972; Mulligan,
1970). In this study, a T. brucei species-specific MoAb was employed in the
dot-ELISA for the identification of T. brucei in experimentally infected tsetse
salivary glands (Chapter 6). However, the assay could not detect the parasites
in the target organ when PBS or PSG were used as sample buffer, even though
these buffers were the preferred choice for the preparation of tsetse gut
samples for testing with the dot-ELISA (Chapter 6). This observation was
explained as below: Tsetse saliva is known to contain several enzymes and
inhibitors including an antithrombin (Parker and Mant, 1979) and fibrinolytic
proteases (Endege et al., 1989). These enzymes and inhibitors were believed
to affect trypanosome antigens in salivary glands during sample preparation,
leading to interference with the dot-ELISA. Investigations conducted into the
use of alternative sample buffers showed that 5mM Na2EDTA was suitable for
treating tsetse salivary glands prior to testing with the dot-ELISA (Chapter 6).
The successful use of Na2EDTA for this purpose, was explained as follows.
Na2EDTA is an enzyme inhibitor. Its use in the sample buffer may, therefore,
have been necessary to inactivate salivary gland enzymes that affected the T.
brucei diagnostic antigen or interfered with the reaction between specific
MoAb and the target antigens.
Trypanosoma suis had been found on only three separate occasions
since its discovery (Stephen, 1986). As a result, suitable antigens of this
parasite could not be obtained for immunization and production of specific
MoAbs to this species. However, the opportunity to replicate test samples
from tsetse salivary glands for testing with the dot-ELISA, showed that should
the need arise and specific MoAbs made against T. suis, this parasite could
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also be tested alongside T. brucei using the dot-ELISA. The sensitivity of the
dot-ELISA in detecting T. brucei parasites in the salivary glands of tsetse was
high (90%), and the specificity was greater that 99.9%, with no cross
reactivity recorded.
The overall sensitivity of the dot-ELISA in detecting trypanosomes in
the mouthparts of experimentally infected Glossina was low, less than 50%
(Chapter 6). This low detection rate was believed to be due to the relatively
low number of trypanosomes present in infected proboscides as well as to
difficulties in releasing trypanosomes from the proboscis as a result of
anatomical peculiarities of this organ. The specificity of the assay was,
however, high (greater than 99.9%).
Natural trypanosome infection rates in Glossina determined by
dissection are usually low, less than 10% as reported by Jordan (1974).
Evaluation of the dot-ELISA in the field, revealed similarly low trypanosome
infection rates (Chapter 7). In this field study, two tsetse flies that were
identified by dissection as infected with trypanosomes in the midguts, were
also positive by the dot-ELISA (Chapter 7). Using the dissection technique,
such infections were attributable to immature T. brucei or T. congolense or T.
simiae (Lloyd and Johnson, 1924). However, using the dot-ELISA, it was
possible to tell that those two flies were infected with T. congolense (Chapter
The sensitivity of the dissection method had been shown to be below
100% by many investigators. For example, Ward and Bell (1971) performed
experiments with the animal sub-inoculation method of revealing mature
trypanosome infections in the vector, and reported that feeding T brucei
infected tsetse flies individually on mice gave transmission rates that were
about five times higher than those revealed by salivary gland dissections.
Also, Moloo and Kutuza, (1974), used the animal sub-inoculation method to
incriminate G swynnertoni as the vector of sleeping sickness in an area in
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Tanzania, where attempts to find the vector of the disease using the dissection
method had failed. In a field evaluation (Chapter 7), the dot-ELISA detected
T congolense antigens in the guts of tsetse flies that had been assumed to be
uninfected as determined using the dissection technique. This high detection
rate by the dot-ELISA, could be attributed to superior sensitivity of the
technique as compared with the dissection method, thus suggesting that the
dot-ELISA could be a better choice for revealing the true extent of the vectoral
capacity of the Glossina species.
In conclusion, this study provides useful information on the suitability
of MoAbs as diagnostic reagents for detecting and differentiating between the
vector stages of the African trypanosomes. It also provides evidence that a
MoAb-based dot-ELISA could be employed as a practical alternative to the
dissection technique which is currently used for diagnosis of trypanosome
infections in Glossina species.
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2 95
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