Current status of vaccination against African trypanosomiasis

Parasitology

Volumn 137, Issue 14, 2010, Pages 2017-2027

  Magez, Stefan ^a,b   Caljon, Guy ^a,b,c   Tran, Thao ^a,b   Stijlemans, Benoît ^a,b   Radwanska, Magdalena ^d  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^d European Cooperation for Science and Technology   (Belgium)

Author keywords

B cells; Trypanosomiasis; vaccination

Indexed keywords

ADENOVIRUS VECTOR; DIMINAZENE ACETURATE; DIPHTHERIA PERTUSSIS TETANUS VACCINE; MICROTUBULE ASSOCIATED PROTEIN; VARIANT SURFACE GLYCOPROTEIN;

AFRICAN TRYPANOSOMIASIS; ANTIBODY TITER; ANTIGENIC VARIATION; ARTICLE; B LYMPHOCYTE; CLINICAL TRIAL; DISEASE TRANSMISSION; HUMAN; IMMUNE DEFICIENCY; IMMUNOMODULATION; INFECTION PREVENTION; MEDICAL RESEARCH; NONHUMAN; PRIORITY JOURNAL; TRYPANOSOMIASIS; VACCINATION;

ANTIGENIC VARIATION; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNOLOGIC MEMORY; PROTOZOAN VACCINES; TRYPANOSOMA; TRYPANOSOMIASIS, AFRICAN; VARIANT SURFACE GLYCOPROTEINS, TRYPANOSOMA;

EID: 78650309503     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182010000223     Document Type: Article

References (97)

1. Askonas, B. A., Corsini, A. C., Clayton, C. E. and Ogilvie, B. M. (1979). Functional depletion of T- and B-memory cells and other lymphoid cell subpopulations-during trypanosomiasis. Immunology 36, 313-321.
2. Authié, E., Boulange, A., Muteti, D., Lalmanach, G., Gauthier, F. and Musoke, A. J. (2001). Immunisation of cattle with cysteine proteinases of Trypanosoma congolense: targetting the disease rather than the parasite. International Journal for Parasitology 31, 1429-1433.
3. Authié, E., Duvallet, G., Robertson, C. and Williams, D. J. (1993). Antibody responses to a 33 kDa cysteine protease of Trypanosoma congolense: relationship to 'trypanotolerance' in cattle. Parasite Immunology 15, 465-474.
4. Authié, E., Muteti, D. K., Mbawa, Z. R., Lonsdale-Eccles, J. D., Webster, P. and Wells, C. W. (1992). Identification of a 33-kilodalton immunodominant antigen of Trypanosoma congolense as a cysteine protease. Molecular and Biochemical Parasitology 56, 103-116.
5. Balaban, N., Waithaka, H. K., Njogu, A. R. and Goldman, R. (1995). Intracellular antigens (microtubule-associated protein copurified with glycosomal enzymes) - possible vaccines against trypanosomiasis. Journal of Infectious Diseases 172, 845-850.
6. Barry, J. D., Graham, S. V., Fotheringham, M., Graham, V. S., Kobryn, K. and Wymer, B. (1998). VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Molecular and Biochemical Parasitology 91, 93-105.
7. Barry, J. D., Hajduk, S. L., Vickerman, K. and LeRay, D. (1979). Detection of multiple variable antigen types in metacyclic populations of Trypanosoma brucei. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 205-208.
8. Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B., Böhme, U., Hannick, L., Aslett, M. A., Shallom, J., Marcello, L., Hou, L., Wickstead, B., Alsmark, U. C., Arrowsmith, C., Atkin, R. J., Barron, A. J., Bringaud, F., Brooks, K., Carrington, M., Cherevach, I., Chillingworth, T. J., Churcher, C., Clark, L. N., Corton, C. H., Cronin, A., Davies, R. M., Doggett, J., Djikeng, A., Feldblyum, T., Field, M. C., Fraser, A., Goodhead, I., Hance, Z., Harper, D., Harris, B. R., Hauser, H., Hostetler, J., Ivens, A., Jagels, K., Johnson, D., Johnson, J., Jones, K., Kerhornou, A. X., Koo, H., Larke, N., Landfear, S., Larkin, C., Leech, V., Line, A., Lord, A., Macleod, A., Mooney, P. J., Moule, S., Martin, D. M., Morgan, G. W., Mungall, K., Norbertczak, H., Ormond, D., Pai, G., Peacock, C. S., Peterson, J., Quail, M. A., Rabbinowitsch, E., Rajandream, M. A., Reitter, C., Salzberg, S. L., Sanders, M., Schobel, S., Sharp, S., Simmonds, M., Simpson, A. J., Tallon, L., Turner, C. M., Tait, A., Tivey, A. R., Van Aken, S., Walker, D., Wanless, D., Wang, S., White, B., White, O., Whitehead, S., Woodward, J., Wortman, J., Adams, M. D., Embley, T. M., Gull, K., Ullu, E., Barry, J. D., Fairlamb, A. H., Opperdoes, F., Barrell, B. G., Donelson, J. E., Hall, N., Fraser, C. M., Melville, S. E. and El-Sayed, N. M. (2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416-422.
9. Boutlis, C. S., Gowda, D. C., Naik, R. S., Maguire, G. P., Mgone, C. S., Bockarie, M. J., Lagog, M., Ibam, E., Lorry, K. and Anstey, N. M. (2002). Antibodies to Plasmodium falciparum glycosylphosphatidylinositols: inverse association with tolerance of parasitemia in Papua New Guinean children and adults. Infection and Immunity 70, 5052-5057.
10. Caljon, G., Van Den Abbeele, J., Sternberg, J. M., Coosemans, M., De Baetselier, P. and Magez, S. (2006a). Tsetse fly saliva biases the immune response to Th2 and induces anti-vector antibodies that are a useful tool for exposure assessment. International Journal for Parasitology 36, 1025-1035.
11. Caljon, G., Van Den Abbeele, J., Stijlemans, B., Coosemans, M., De Baetselier, P. and Magez, S. (2006b). Tsetse fly saliva accelerates the onset of Trypanosoma brucei infection in a mouse model associated with a reduced host inflammatory response. Infection and Immunity 74, 6324-6330.
12. Clayton, C. E., Ogilvie, B. M. and Askonas, B. A. (1979). Trypanosoma brucei infection in nude mice: B lymphocyte function is suppressed in the absence of T lymphocytes. Parasite Immunology 1, 39-48.
13. Cornelissen, A. W., Bakkeren, G. A., Barry, J. D., Michels, P. A. and Borst, P. (1985). Characteristics of trypanosome variant antigen genes active in the tsetse fly. Nucleic Acids Research 13, 4661-4676.
14. Crowe, J. S., Barry, J. D., Luckins, A. G., Ross, C. A. and Vickerman, K. (1983). All metacyclic variable antigen types of Trypanosoma congolense identified using monoclonal antibodies. Nature 306, 389-391.
15. Crowe, J. S., Lamont, A. G., Barry, J. D. and Vickerman, K. (1984). Cytotoxicity of monoclonal antibodies to Trypanosoma brucei. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 508-513.
16. de la Fuente, J., Rodr?́guez, M., Redondo, M., Montero, C., Garc?́a-Garc?́a, J. C., Méndez, L., Serrano, E., Valdés, M., Enriquez, A., Canales, M., Ramos, E., Boué, O., Machado, H., Lleonart, R., de Armas, C. A., Rey, S., Rodr?́guez, J. L., Artiles, M. and Garc?́a, L. (1998). Field studies and cost-effectiveness analysis of vaccination with Gavac against the cattle tick Boophilus microplus. Vaccine 16, 366-373.
17. Engstler, M., Pfohl, T., Herminghaus, S., Boshart, M., Wiegertjes, G., Heddergott, N. and Overath, P. (2007). Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131, 505-515.
18. Esser, K. M., Schoenbechler, M. J. and Gingrich, J. B. (1982). Trypanosoma rhodesiense blood forms express all antigen specificities relevant to protection against metacyclic (insect form) challenge. Journal of Immunology 129, 1715-1718.
19. Gull, K. (2003). Host-parasite interactions and trypanosome morphogenesis: a flagellar pocketful of goodies. Current Opinions in Microbiology 6, 365-370.
20. Haddow, J. D., Haines, L. R., Gooding, R. H., Olafson, R. W. and Pearson, T. W. (2005). Identification of midgut proteins that are differentially expressed in trypanosome-susceptible and normal tsetse flies (Glossina morsitans morsitans). Insect Biochemistry and Molecular Biology 35, 425-433.
21. Hemphill, A., Lawson, D. and Seebeck, T. (1991). The cytoskeletal architecture of Trypanosoma brucei. Journal of Parasitology 77, 603-612.
22. Holland, W. G., Do, T. T., Huong, N. T., Dung, N. T., Thanh, N. G., Vercruysse, J. and Goddeeris, B. M. (2003). The effect of Trypanosoma evansi infection on pig performance and vaccination against classical swine fever. Veterinary Parasitology 111, 115-123.
23. Honigberg, B. M., Hampton, R. W. and Cunningham, I. (1991). Effect of polyclonal anti-procyclic antibodies on development of Trypanosoma brucei brucei in tsetse flies. Parasitology Research 77, 39-43.
24. Jackson, D. G., Windle, H. J. and Voorheis, H. P. (1993). The identification, purification, and characterization of two invariant surface glycoproteins located beneath the surface coat barrier of bloodstream forms of Trypanosoma brucei. Journal of Biological Chemistry 268, 8085-8095.
25. Kamanga-Sollo, E. I., Musoke, A. J., Nantulya, V. M., Rurangirwa, F. R. and Masake, R. A. (1991). Differences between N'Dama and Boran cattle in the ability of their peripheral blood leucocytes to bind antibody-coated trypanosomes. Acta Tropica 49, 109-117.
26. Kamhawi, S., Belkaid, Y., Modi, G., Rowton, E. and Sacks, D. (2000). Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290, 1351-1354.
27. Kennedy, P. (2009). Cytokines in central nervous system trypanosomiasis: cause, effect or both? Trends in Parasitology 103, 213-214.
28. Kinyua, J. K., Nguu, E. K., Mulaa, F. and Ndung'u, J. M. (2005). Immunization of rabbits with Glossina pallidipes tsetse fly midgut proteins: effects on the fly and trypanosome transmission. Vaccine 23, 3824-3828.
29. Kohl, L. and Gull, K. (1998). Molecular architecture of the trypanosome cytoskeleton. Molecular and Biochemical Parasitology 93, 1-9.
30. Lalmanach, G., Boulangé, A., Serveau, C., Lecaille, F., Scharfstein, J., Gauthier, F. and Authié, E. (2002). Congopain from Trypanosoma congolense: drug target and vaccine candidate. Biological Chemistry 383, 739-749.
31. Le Ray, D., Barry, J. D. and Vickerman, K. (1978). Antigenic heterogeneity of metacyclic forms of Trypanosoma brucei. Nature 273, 300-302.
32. Li, S. Q., Fung, M. C., Reid, S. A., Inoue, N. and Lun, Z. R. (2007). Immunization with recombinant beta-tubulin from Trypanosoma evansi induced protection against T. evansi, T. equiperdum and T. b. brucei infection in mice. Parasite Immunology 29, 191-199.
33. Li, S. Q., Yang, W. B., Ma, L. J., Xi, S. M., Chen, Q. L., Song, X. W., Kang, J. and Yang, L. Z. (2009). Immunization with recombinant actin from Trypanosoma evansi induces protective immunity against T. evansi, T. equiperdum and T. b. brucei infection. Parasitology Research 104, 429-435.
34. Lubega, G. W., Byarugaba, D. K. and Prichard, R. K. (2002a). Immunization with a tubulin-rich preparation from Trypanosoma brucei confers broad protection against African trypanosomosis. Experimental Parasitology 102, 9-22.
35. Lubega, G. W., Ochola, D. O. and Prichard, R. K. (2002b). Trypanosoma brucei: anti-tubulin antibodies specifically inhibit trypanosome growth in culture. Experimental Parasitology 102, 134-142.
36. MacAskill, J. A., Holmes, P. H., Whitelaw, D. D., Jennings,F. W. and Urquhart,G. M. (1983). Immune mechanisms in C57B1 mice genetically resistant to Trypanosoma congolense infection. II. Aspects of the humoral response. Parasite Immunology 5, 577-586.
37. Magez, S., Radwanska, M., Drennan, M., Fick, L., Baral, T. N., Allie, N., Jacobs, M., Nedospasov, S., Brombacher, F., Ryffel, B. and De Baetselier, P. (2007). Tumor necrosis factor (TNF) receptor-1 (TNFp55) signal transduction and macrophage-derived soluble TNF are crucial for nitric oxide-mediated Trypanosoma congolense parasite killing. Journal of Infectious Diseases 196, 954-962.
38. Magez, S., Radwanska, M., Drennan, M., Fick, L., Baral, T. N., Brombacher, F. and De Baetselier, P. (2006). Interferon-gamma and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 Infections. Journal of Infectious Disease 193, 1575-1583.
39. Magez, S., Radwanska, M., Beschin, A., Sekikawa, K. and De Baetselier, P. (1999). Tumor necrosis factor alpha is a key mediator in the regulation of experimental Trypanosoma brucei infections. Infection and Immunity 67, 3128-3132.
40. Magez, S., Stijlemans, B., Baral, T. and De Baetselier, P. (2002). VSG-GPI anchors of African trypanosomes: their role in macrophage activation and induction of infection-associated immunopathology. Microbes and Infection 4, 999-1006.
41. Magez, S., Stijlemans, B., Radwanska, M., Pays, E., Ferguson, M. A. and De Baetselier, P. (1998). The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. Journal of Immunology 160, 1949-1956.
42. Magez, S., Truyens, C., Merimi, M., Radwanska, M., Stijlemans, B., Brouckaert, P., Brombacher, F., Pays, E. and De Baetselier, P. (2004). P75 tumor necrosis factor-receptor shedding occurs as a protective host response during African trypanosomiasis. Journal of Infection Diseases 189, 527-539.
43. Marcello, L. and Barry, J. D. (2007). From silent genes to noisy populations-dialogue between the genotype and phenotypes of antigenic variation. Journal of Eukaryote Microbiology 54, 14-17.
44. Maudlin, I., Turner, M. J., Dukes, P. and Miller, N. (1984). Maintenance of Glossina morsitans morsitans on antiserum to procyclic trypanosomes reduces infection rates with homologous and heterologous Trypanosoma congolense stocks. Acta Tropica 41, 253-257.
45. Mbawa, Z. R., Gumm, I. D., Shaw, E. and Lonsdale-Eccles, J. D. (1992). Characterisation of a cysteine protease from bloodstream forms of Trypanosoma congolense. European Journal of Biochemistry 204, 371-379.
46. McCulloch, R. and Horn, D. (2009). What has DNA sequencing revealed about the VSG expression sites of African trypanosomes? Trends in Parasitology 25, 359-363.
47. Mitchell, L. A. and Pearson, T. W. (1983). Antibody responses induced by immunization of inbred mice susceptible and resistant to African trypanosomes. Infection and Immunity 40, 894-902.
48. Mkunza, F., Olaho, W. M. and Powell, C. N. (1995). Partial protection against natural trypanosomiasis after vaccination with a flagellar pocket antigen from Trypanosoma brucei rhodesiense. Vaccine 13, 151-154.
49. Murray, M., Hirumi, H. and Moloo, S. K. (1985). Suppression of Trypanosoma congolense, T. vivax and T. brucei infection rates in tsetse flies maintained on goats immunized with uncoated forms of trypanosomes grown in vitro. Parasitology 91, 53-66.
50. Murray, P. K., Jennings, F. W., Murray, M. and Urqhart, G. M. (1974a). The nature of immunosuppression in Trypanosoma brucei infections in mice. I. The role of the macrophage. Immunology 27, 815-824.
51. Murray, P. K., Jennings, F. W., Murray, M. and Urqhart, G. M. (1974b). The nature of immunosuppression in Trypanosoma brucei infections in mice. II. The role of the T and B lymphocytes. Immunology 27, 825-840.
52. Mwangi, D. M., Munyua, W. K. and Nyaga, P. N. (1990). Immunosuppression in caprine trypanosomiasis: effects of acute Trypanosoma congolense infection on antibody response to anthrax spore vaccine. Tropical Animal Health and Production 22, 95-100.
53. Naessens, J. (2006). Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome? International Journal for Parasitology 36, 521-528.
54. Naik, R. S., Branch, O. H., Woods, A. S., Vijaykumar, M., Perkins, D. J., Nahlen, B. L., Lal, A. A., Cotter, R. J., Costello, C. E., Ockenhouse, C. F., Davidson, E. A. and Gowda, D. C. (2000). Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. Journal of Experimental Medicine 192, 1563-1576.
55. Nantulya, V. M., Doyle, J. J. and Jenni, L. (1980a). Studies on Trypanosoma (nannomonas) congolense III. Antigenic variation in three cyclically transmitted stocks. Parasitology 80, 123-131.
56. Nantulya, V. M., Doyle, J. J. and Jenni, L. (1980b). Studies on Trypanosoma (nannomonas) congolense IV. Experimental immunization of mice against tsetse fly challenge. Parasitology 80, 133-137.
57. Nogge, G. and Giannetti, M. (1979). Midgut absorption of undigested albumin and other proteins by tsetse, Glossina M. morsitans (Diptera: Glossinidae). Journal of Medical Entomology 16, 263.
58. Nogge, G. and Giannetti, M. (1980). Specific antibodies: a potential insecticide. Science 209, 1028-1029.
59. Nolan, D. P., Geuskens, M. and Pays, E. (1999). N-linked glycans containing linear poly-N-acetyllactosamine as sorting signals in endocytosis in Trypanosoma brucei. Current Biology 9, 1169-1172.
60. Nolan, D. P., Jackson, D. G., Windle, H. J., Pays, A., Geuskens, M., Michel, A., Voorheis, H. P. and Pays, E. (1997). Characterization of a novel, stage-specific, invariant surface protein in Trypanosoma brucei containing an internal, serine-rich, repetitive motif. Journal of Biological Chemistry 272, 29212-29221.
61. O'Beirne, C., Lowry, C. M. and Voorheis, H. P. (1998). Both IgM and IgG anti-VSG antibodies initiate a cycle of aggregation-disaggregation of bloodstream forms of Trypanosoma brucei without damage to the parasite. Molecular and Biochemical Parasitology 91, 165-193.
62. O'Gorman, G. M., Park, S. D., Hill, E. W., Meade, K. G., Coussens, P. M., Agaba, M., Naessens, J., Kemp, S. J. and MacHugh, D. E. (2009). Transcriptional profiling of cattle infected with Trypanosoma congolense highlights gene expression signatures underlying trypanotolerance and trypanosusceptibility. BMC Genomics 10, 207.
63. Olenick, J. G., Wolff, R., Nauman, R. K. and McLaughlin, J. (1988). A flagellar pocket membrane fraction from Trypanosoma brucei rhodesiense: immunogold localization and nonvariant immunoprotection. Infection and Immunity 56, 92-98.
64. Outchkourov, N. S., Roeffen, W., Kaan, A., Jansen, J., Luty, A., Schuiffel, D., van Gemert, G. J., van de Vegte-Bolmer, M., Sauerwein, R. W. and Stunnenberg, H. G. (2008). Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proceedings of the National Academy of Sciences, USA 105, 4301-4305.
65. Pan, W., Ogunremi, O., Wei, G., Shi, M. and Tabel, H. (2006). CR3 (CD11b/CD18) is the major macrophage receptor for IgM antibody-mediated phagocytosis of African trypanosomes: diverse effect on subsequent synthesis of tumor necrosis factor alpha and nitric oxide. Microbes and Infection 8, 1209-1218.
66. Pinder, M., Libeau, G., Hirsch, W., Tamboura, I., Hauck-Bauer, R. and Roelants, G. E. (1984). Anti-trypanosome specific immune responses in bovids of differing susceptibility to African trypanosomiasis. Immunology 51, 247-258.
67. Radwanska, M., Guirnalda, P.,DeTrez, C., Ryffel, B., Black, S. and Magez, S. (2008). Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathogens 4, e1000078.
68. Radwanska, M., Magez, S., Dumont, N., Pays, A., Nolan, D. and Pays, E. (2000a). Antibodies raised against the flagellar pocket fraction of Trypanosoma brucei preferentially recognize HSP60 in cDNA expression library. Parasite Immunology 22, 639-650.
69. Radwanska, M., Magez, S., Michel, A., Stijlemans, B., Geuskens, M. and Pays, E. (2000b). Comparative analysis of antibody responses against HSP60, invariant surface glycoprotein 70, and variant surface glycoprotein reveals a complex antigen-specific pattern of immunoglobulin isotype switching during infection by Trypanosoma brucei. Infection and Immunity 68, 848-860.
70. Rasooly, R. and Balaban, N. (2004). Trypanosome microtubule-associated protein p15 as a vaccine for the prevention of African sleeping sickness. Vaccine 22, 1007-1015.
71. Robinson, D. R. and Gull, K. (1991). Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle. Nature 352, 731-733.
72. Roditi, I. and Lehane, M. J. (2008). Interactions between trypanosomes and tsetse flies. Current Opinions in Microbiology 11, 345-351.
73. Rurangirwa, F. R., Musoke, A. J., Nantulya, V. M. and Tabel, H. (1983). Immune depression in bovine trypanosomiasis: effects of acute and chronic Trypanosoma congolense and chronic Trypanosoma vivax infections on antibody response to Brucella abortus vaccine. Parasite Immunology 5, 267-276.
74. Saraiva, E. M., de Figueiredo Barbosa, A., Santos, F. N., Borja-Cabrera, G. P., Nico, D., Souza, L. O., de Oliveira Mendes-Aguiar, C., de Souza, E. P., Fampa, P., Parra, L. E., Menz, I., Dias, J. G. Jr., de Oliveira, S. M. and Palatnik-de-Sousa, C. B. (2006). The FML-vaccine (Leishmune) against canine visceral leishmaniasis: a transmission blocking vaccine. Vaccine 24, 2423-2431.
75. Schofield, D. L., Hewitt, M. C., Evans, K., Siomos, M. A. and Seeberger, P. H. (2002). Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418, 785-789.
76. Sharpe, R. T., Langley, A. M., Mowat, G. N., MacAskill, J. A. and Holmes, P. H. (1982). Immunosuppression in bovine trypanosomiasis: response of cattle infected with Trypanosoma congolense to foot-and-mouth disease vaccination and subsequent live virus challenge. Research in Veterinary Science 32, 289-293.
77. Shi, M., Wei, G., Pan, W. and Tabel, H. (2005). Impaired Kupffer cells in highly susceptible mice infected with Trypanosoma congolense. Infection and Immunity 73, 8393-8396.
78. Sileghem, M., Flynn, J. N., Logan-Henhrey, L. and Ellis, J. (1994). Tumour necrosis factor production by monocytes from cattle infected with Trypanosoma (Duttonella) vivax and Trypanosoma (Nannomonas) congolense: possible association with severity of anaemia associated with the disease. Parasite Immunology 16, 51-54.
79. Steverding, D., Stierhof, Y. D., Chaudhri, M., Ligtenberg, M., Schell, D., Beck-Sickinger, A. G. and Overath, P. (1994). ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. European Journal of Cell Biology 64, 78-87. (Pubitemid 24205986)
80. Stijlemans, B., Baral, T. N., Guilliams, M., Brys, L., Korf, J., Drennan, M., Van Den Abbeele, J., De Baetselier, P. and Magez, S. (2007). A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis- associated immunopathology. Journal of Immunology 179, 4003-4014.
81. Taylor, K. A. (1998). Immune responses of cattle to African trypanosomes: protective or pathogenic? International Journal for Parasitology 28, 219-240.
82. Taylor, K. A., Lutje, V., Kennedy, D., Authié, E., Boulangé, A., Logan-Henfrey, L., Gichuki, B. and Gettinby, G. (1996). Trypanosoma congolense: B-lymphocyte responses differ between trypanotolerant and trypanosusceptible cattle. Experimental Parasitology 83, 106-116.
83. Tetley, L., Vickerman, K. and Moloo, S. K. (1981). Absence of a surface coat from metacyclic Trypanosoma vivax: possible implications for vaccination against vivax trypanosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 409-414.
84. Thiakaki, M., Rohousova, I., Volfova, V., Volf, P., Chang, K. P. and Soteriadou, K. (2005). Sand fly specificity of saliva-mediated protective immunity in Leishmania amazonensis-BALB/c mouse model. Microbes and Infection 7, 760-766.
85. Tran, T., Büscher, P., Vandenbuscche, G., Wyns, L., Messens, J. and De Greve, H. (2008). Heterologous expression, purification and characterisation of the extracellular domain of trypanosome invariant surface glycoprotein ISG75. Journal of Biotechnology 135, 247-254.
86. Tran, T., Cleas, F., Dujardin, J. C. and Büscher, P. (2006). The invariant surface glycoprotein ISG75 gene family consists of two main groups in the Trypanozoon subgenus. Parasitology 133, 613-621.
87. Urwyler, S., Studer, E., Renggli, C. K. and Roditi, I. (2007). A family of stage-specific alanine-rich proteins on the surface of epimastigote forms of Trypanosoma brucei. Molecular Microbiology 63, 218-228.
88. Van Meirvenne, N., Janssens, P. G. and Magnus, E. (1975a). Antigenic variation in syringe passaged populations of Trypanosoma (Trypanozoon) brucei. 1. Rationalization of the experimental approach. Annales de la Société Belge de Médecine Tropicale 55, 1-23.
89. Van Meirvenne, N., Janssens, P. G., Magnus, E., Lumsden, W. H. and Herbert, W. J. (1975b). Antigenic variation in syringe passaged populations of Trypanosoma (Trypanozoon) brucei. II. Comparative studies on two antigenic-type collections. Annales de la Société Belge de Médecine Tropicale 55, 25-30.
90. Vickerman, K. (1978). Antigenic variation in trypanosomes. Nature 273, 613-617.
91. Whitelaw, D. D., Scott, J. M., Reid, H. W., Holmes, P. H., Jennings, F. W. and Urquhart,G. M. (1979). Immunosuppression in bovine trypanosomiasis: studies with louping-ill vaccine. Research in Veterinary Science 26, 102-107.
92. Willadsen, P., Bird, P., Cobon, G. S. and Hungerford, J. (1995). Commercialisation of a recombinant vaccine against Boophilus microplus. Parasitology 110 (Suppl), S43-S50.
93. Willadsen, P., Riding, G. A., McKenna, R. V., Kemp, D. H., Tellam, R. L., Nielsen, J. N., Lahnstein, J., Cobon, G. S. and Gough, J. M. (1989). Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. Journal of Immunology 143, 1346-1351.
94. Williams, D. J., Taylor, K., Newson, J., Gichuki, B. and Naessens, J. (1996). The role of anti-variable surface glycoprotein antibody responses in bovine trypanotolerance. Parasite Immunology 18, 209-218.
95. Ziegelbauer, K., Multhaup, G. and Overath, P. (1992b). Molecular characterization of two invariant surface glycoproteins specific for the bloodstream stage of Trypanosoma brucei. Journal of Biological Chemistry 267, 10797-10803.
96. Ziegelbauer, K. and Overath, P. (1992a). Identification of invariant surface glycoproteins in the bloodstream stage of Trypanosoma brucei. Journal of Biological Chemistry 267, 10791-10796.
97. Ziegelbauer, K. and Overath, P. (1993). Organization of two invariant surface glycoproteins in the surface coat of Trypanosoma brucei. Infection and Immunity 61, 4540-4545.