Immune evasion strategies of trypanosomes: A review

Journal of Parasitology

Volumn 98, Issue 2, 2012, Pages 284-292

  Oladiran, Ayoola ^a   Belosevic, Miodrag ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1Q; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MESSENGER RNA;

BIOCHEMICAL COMPOSITION; DOMESTIC SPECIES; ECTOTHERMY; ENDOTHERMY; FUNCTIONAL MORPHOLOGY; HOST-PARASITE INTERACTION; IMMUNE SYSTEM; LITERATURE REVIEW; PARASITE; PARASITIC DISEASE; PROTOZOAN; PUBLIC HEALTH; TAXONOMY; WILD POPULATION;

B LYMPHOCYTE; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMORAL IMMUNITY; IMMUNE EVASION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PHAGOCYTOSIS; PROTOZOAL GENETICS; PROTOZOON; REVIEW; T LYMPHOCYTE; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CARASSII; TRYPANOSOMA CRUZI;

ANIMALS; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNE EVASION; INVERTEBRATES; LIFE CYCLE STAGES; MAMMALS; TRYPANOSOMA; TRYPANOSOMIASIS; VERTEBRATES;

ANIMALIA; HEXAPODA; HIRUDINIDA; PROTOZOA; VERTEBRATA;

EID: 84860273023     PISSN: 00223395     EISSN: 19372345     Source Type: Journal    
DOI: 10.1645/GE-2925.1     Document Type: Review

References (95)

1. ABRAHAMSOHN, I. A., AND R. L. COFFMAN. 1996. Trypanosoma cruzi: IL- 10, TNF, IFN-gamma, and IL-12 regulate innate and acquired immunity to infection. Experimental Parasitology 84: 231-244.
2. AGÜ ERO, F., V. CAMPO, L. CREMONA, A. JÄ GER, J. M. DI NOIA, P. OVERATH, D. O. SÁ NCHEZ, AND A. C. FRASCH. 2002. Gene discovery in the freshwater fish parasite Trypanosoma carassii: Identification of transialidase-like and mucin-like genes. Infection and Immunity 70: 7140-7144. (Pubitemid 35387952)
3. AGUILAR, L., G. RAMÍREZ, C. VALCK, M. C. MOLINA, A. ROJAS, W. SCHWAEBLE, V. FERREIRA, AND A. FERREIRA. 2005. F(ab9)2 antibody fragments against Trypanosoma cruzi calreticulin inhibit its interaction with the first component of human complement. Biological Research 38: 187-195. (Pubitemid 41535619)
4. BAKHIET, M., T. OLSSON, C. EDLUND, B. HOJEBERG, K. HOLMBERG, J. LORENTZEN, AND K. KRISTENSSON. 1993. Trypanosoma brucei brucei derived factors that triggers CD8+ lymphocytes to interferon gamma secretion: Purification, characterization and protective effects in vivo by treatment with monoclonal antibodies against the factor. Scandinavian Journal of Immunology 37: 165-178. (Pubitemid 23063659)
5. BARAL, T. N., P. DE BAESTSELIER, F. BROMBACHER, AND S. MAGEZ. 2007. Control of Trypanosoma evansi infection is IgM mediated and does not require a Type 1 inflammatory response. Journal of Infectious Diseases 195: 1513-1520. (Pubitemid 46717470)
6. BARRETT, M. P., R. J. BURCHMORE, A. STICH, J. O. LAZZARI, A. C. FRASCH, J. J. CAZZULO, AND S. KRISHNA. 2003. The trypanosomiases. Lancet 362: 1469-1480. (Pubitemid 37352887)
7. BARRY, J. D., L. MARCELLO, L. J. MORRISON, A. F. READ, K. LYTHGOE, N. JONES, M. CARRINGTON, G. BLANDIN, U. BOHME, E. CALER, ET AL. 2005. What the genome sequence is revealing about trypanosome antigenic variation. Biochemical Society Transactions 33: 986-989. (Pubitemid 41659096)
8. BERRIMAN, M., E. GHEDIN, C. HERTZ-FOWLER, G. BLANDIN, H. RENAULD, D. C. BARTHOLOMEU, N. J. LENNARD, E. CALER, N. E. HAMLIN, B. HAAS, ET AL. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309: 416-422. (Pubitemid 40994676)
9. BIENEK, D. R., D. A. PLOUFFE, G. F. WIEGERTJES, AND M. BELOSEVIC. 2002. Immunization of goldfish with excretory/secretory molecules of Trypanosoma danilewskyi confers protection against infection. Developmental and Comparative Immunology 26: 649-657. (Pubitemid 34628861)
10. BORST, P. 2002. Antigenic variation and allelic exclusion. Cell 109: 5-8. (Pubitemid 34327511)
11. BRITTINGHAM, A., C. J. MORRISON, W. R. MCMASTER, B. S. MCGWIRE, K. P. CHANG, AND D. M. MOSSER. 1995. Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance tocomplement-mediated lysis. Journal of Immunology 155: 3102-3111.
12. BUDZKO, D. B., M. C. PIZZIMENTI, AND F. KIERSZENBAUM. 1975. Effects of complement depletion in experimental Chagas disease: Immune lysis of virulent blood forms of Trypanosoma cruzi. Infection and Immunity 11: 86-91.
13. BUSCAGLIA, C. A., V. A. CAMPO, A. C. FRASCH, AND J. M. DI NOIA. 2006. Trypanosoma cruzi surface mucins: Host-dependent coat diversity. Nature Reviews Microbiology 4: 229-236.
14. CARDILLO, F., J. C. VOLTARELLI, S. G. REED, AND J. S. SILVA. 1996. Regulation of Trypanosoma cruzi infection in mice by gamma interferon and interleukin 10: Role of NK cells. Infection and Immunity 64: 128-134. (Pubitemid 26009351)
15. CONNELL, N. D., E. MEDINA-ACOSTA, W. R. MCMASTER, B. R. BLOOM, AND D. G. RUSSELL. 1993. Effective immunization against cutaneous leishmaniasis with recombinant bacille Calmette-Guerin expressing the Leishmania surface proteinase gp63. Proceedings of the National Academy of Sciences USA 90: 11473-11437.
16. DAMIAN, R. T. 1997. Parasite immune evasion and exploitation: Reflections and projections. Parasitology 115: 169-175.
17. DARJI, A., A. BESCHIN, M. SILEGHEM, H. HEREMANS, L. BRYS, AND P. DE BAETSELIER. 1996. In vitro simulation of immunosuppression caused by Trypanosome brucei: Active involvement of gamma interferon and tumor necrosis factor in the pathway of suppression. Infection and Immunity 64: 1937-1943 (Pubitemid 26165649)
18. M. SILEGHEM, H. HEREMANS, L. BRYS, AND P. DE BAETSELIER. 1993. Inhibition of T-cell responsiveness during experimental infections with Trypanosoma brucei: Active involvement of endogenous gamma interferon. Infection and Immunity 61: 3098-3102. (Pubitemid 23182317)
19. DE GREEF, C., H. IMBRECHTS, G. MATTHYSSENS, N. VAN MEIRVENNE, AND R. HAMERS. 1989. A gene expressed only in serum-resistant variants of Trypanosoma brucei rhodesiense. Molecular and Biochemical Parasitology 36: 169-176. (Pubitemid 19212840)
20. DEVINE, D. V., R. J. FALK, AND A. E. BALBER. 1986. Restriction of the alternative pathway of human complement by intact Trypanosoma brucei subsp. gambiense. Infection and Immunity 52: 223-229. (Pubitemid 16137705)
21. DI NOIA, J. M., G. D. POLLEVICK, M. T. XAVIER, J. O. PREVIATO, L. MENDOCA-PREVIATO, D. O. SANCHEZ, AND A. C. FRASCH. 1996. High diversity in mucin genes and mucin molecules in Trypanosoma cruzi. Journal of Biological Chemistry 271: 32078-32083. (Pubitemid 26422237)
22. DONELSON, J. E., K. L. HILL, AND N. M. A. EL-SAYED. 1998. Multiple mechanisms of immune evasion by African trypanosomes. Molecular and Biochemical Parasitology 91: 51-56.
23. DRENNAN, M. B., B. STIJLEMANS, V. ABBEELE, V. J. QUESNIAUX, M. BARKHUIZEN, F. BROMBACHER, P. DE BAESTSELIER, B. RYFFEL, AND S. MAGEZ. 2005. The induction of a type 1 immune response following Trypanosoma brucei infection is MyD88 dependent. Journal of Immunology 175: 2501-2509. (Pubitemid 41113861)
24. DULEU, , S., P. VINCENDEAU, P. COURTOIS, S. SEMBALLA, I. LAGROYE, S. DAULOUEDE, J. L. BOUCHER, K. T. WILSON, B. VEYRET, AND A. P. GOBERT. 2004. Mouse strain susceptibility to trypanosome infection: An arginase-dependent effect. Journal of Immunology 172: 6298-6303. (Pubitemid 38621237)
25. EL-SAYED, N. M., AND J. E. DONELSON. 1997. African trypanosomes have differentially expressed genes encoding homologues of the Leishmania GP63 surface protease. Journal of Biological Chemistry 272: 26742-26748. (Pubitemid 27458902)
26. ENGSTLER, M., T. PFOHL, S. HERMINGHAUS, M. BOSHART, G. WIEGERTJES, N. HEDDERGOTT, AND P. OVERATH. 2007. Hydrodynamic flowmediated protein sorting on the cell surface of trypanosomes. Cell 131: 505-515. (Pubitemid 350007695)
27. FARGEAS, C., C. Y. WU, T. NAKAJIMA, D. COX, T. NUTMAN, AND G. DELESPESSE. 1992. Differential effect of transforming growth factor beta on the synthesis of Th1- and Th2-like lymphokines by human lymphocytes. European Journal of Immunology 22: 2173-2176.
28. FERREIRA, V., C. VALCK, G. SANCHEZ, A. GINGRAS, S. TZIMA, M. C. MOLINA, R. SIM, W. SCHWAEBLE, AND A. FERREIRA. 2004. The classical activation pathway of the human complement system is specifically inhibited by calreticulin from Trypanosoma cruzi. Journal of Immunology 172: 3042-3050. (Pubitemid 38263693)
29. GROSSKINSKY, C. M., AND B. A. ASKONAS. 1981. Macrophages as primary target cells and mediators of immune dysfunction in African trypanosomiasis. Infection and Immunity 33: 149-155. (Pubitemid 11066038)
30. GUIRNALDA, P., N. B. MURPHY, D. NOLAN, AND S. J. BLACK. 2007. Anti- Trypanosoma brucei activity in Cape buffalo serum during the cryptic phase of parasitemia is mediated by antibodies. International Journal for Parasitology 37: 1391-1399. (Pubitemid 47285111)
31. HAMADIEN, M., N. LYCKE, AND M. BAKHIET. 1999. Induction of the trypanosome lymphocyte-triggering factor (TLTF) and neutralizing antibodies to the TLTF in experimental African trypanosomiasis. Immunology 96: 606-611. (Pubitemid 29179800)
32. KATZENBACK, B. A., D. A. PLOUFFE, G. HADDAD, AND M. BELOSEVIC. 2008. Administration of recombinant parasite b-tubulin to goldfish (Carassius auratus L) confers partial protection against challenge with Trypanosoma danilewskyi Laveran and Mesnil, 1904. Veterinary Parasitology 151: 36-45.
33. KEMP, M., A. S. HEY, J. A. KURTZHALS, C. B. CHRISTENSEN, A. GAAFAR, M. D. MUSTAFA, A. A. KORDOFANI, A. ISMAIL, A. KHARAZMI, AND T. G. THEANDER. 1994. Dichotomy of the human T cell response to Leishmania antigens. I. Th1-like response to Leishmania major promastigote antigens in individuals recovered from cutaneous leishmaniasis. Clinical and Experimental Immunology 96: 410-415. (Pubitemid 24224858)
34. KITANI, H., S. J. BLACK, Y. NAKAMURA, J. NAESSENS, N. B. MURPHY, Y. YOKOMIZO, J. GIBSON, AND F. IRAQI. 2002. Recombinant tumor necrosis factor alpha does not inhibit the growth of African trypanosomes in axenic cultures. Infection and Immunity 70: 2210-2214. (Pubitemid 34242225)
35. KRAUTZ, G. M., J. C. KISSINGER, AND A. U. KRETTLI. 2000. The targets of the lytic antibody response against Trypanosoma cruzi. Parasitology Today 16: 31-34. (Pubitemid 30101614)
36. KULKARNI, M. M., C. L. OLSON, D. M. ENGMAN, AND B. S. MCGWIRE. 2009. Trypanosoma cruzi gp63 proteins undergo stage-specific differential posttranslational modification and are important for host cell infection. Infection and Immunity 77: 2193-2200.
37. KURTZHALS, J. A., A. S. HEY, A. JARDIM, M. KEMP, K. U. SCHAEFER, E. O. ODERA, C. B. CHRISTENSEN, J. I. GITHURE, R. W. OLAFSON, T. G. THEANDER, ET AL. 1994. Dichotomy of the human T cell response to Leishmania antigens. II. Absent or Th2-like response to gp63 and Th1-like response to lipophosphoglycan- associated protein in cells from cured visceral leishmaniasis patients. Clinical and Experimental Immunology 96: 416-421. (Pubitemid 24224859)
38. LACOUNT, D. J., A. E. GRUSZYNSKI, P. M. GRANDGENETT, J. D. BANGS, AND J. E. DONELSON. 2003. Expression and function of the Trypanosoma brucei major surface protease (GP63) genes. Journal of Biological Chemistry 278: 24658-24664. (Pubitemid 37548621)
39. LI, S. Q., M. C. FUNG, S. A. REID, N. INOUE, AND Z. R. LUN. 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. (Pubitemid 46434885)
40. LISCHKE, A., C. KLEIN, Y. D. STIERHOF, M. HEMPEL, A. MEHLERT, I. C. ALMEIDA, M. A. FERGUSON, AND P. OVERATH. 2000. Isolation and characterization of glycosylphosphatidylinositol-anchored, mucinlike surface glycoproteins from bloodstream forms of the freshwater- fish parasite Trypanosoma carassii. Biochemistry Journal 345: 693-700. (Pubitemid 30099101)
41. LIU, X., AND K. P. CHANG. 1992. Extrachromosomal genetic complementation of surface metalloproteinase (gp63)-deficient Leishmania increases their binding to macrophages. Proceedings of the National Academy of Sciences USA 89: 4991-4995.
42. LOPEZ, N. C., G. RAMIREZ, M. RODRIGUEZ, G. RIBEIRO, J. ORELLANA, I. MALDONADO, A. ALBINI, D. ANACONA, D. LEMUS, L. AQUILAR, ET AL. 2010. Antiangiogenic and antitumor effects of Trypanosoma cruzi calreticulin. PLoS Neglected Tropical Disease 4: e730.
43. LUBEGA, G. W., D. K. BYARUGABA, AND R. K. PRICHARD. 2002. Immunization with a tubulin-rich preparation from Trypanosoma brucei confers broad protection against African trypanosomiasis. Experimental Parasitology 102: 9-22. (Pubitemid 36279579)
44. LUCAS, R., S. MAGEZ, R. DE LEYS, L. FRANSEN, J. P. SCHEERLINCK, M. RAMPELBERG, E. SABLON, AND P. DE BAESTSELIER. 1994. Mapping the lectin-like activity of tumor necrosis factor. Science 263: 814-817. (Pubitemid 24093210)
45. MA, L., K. CHEN, Q.MENG, Q. LIU, P. TANG, S. HU, AND J. YU. 2011. An evolutionary analysis of trypanosomatid Gp63 proteases. Parasitology Research. 109: 1075-1084.
46. MAGEZ, S., M. RADWANSKA, M. DRENNAN, L. FICK, T. N. BARAL, F. BROMBACHER, AND P. DE BAESTSELIER. 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. (Pubitemid 43841392)
47. MAINA, N., J. M. NGOTHO, T.WERE, J. K. THUITA, D. M. MWANGANGI, J. M. KAGIRA, M.NDUNG'u, AND J. STERNBERG. 2004. Pro-inflammatory cytokine expression in the early phase of Trypanosoma brucei rhodesiense infection in Vervet monkeys (Cercopithecus aethiops). Infection and Immunity 72: 3063-3065. (Pubitemid 38542440)
48. MARCELAIN, K., A. COLOMBO, M. C.MOLINA, L. FERREIRA, M. LORCA, J. C. AGUILLÓ N, AND A. FERREIRA. 2000. Development of an immunoenzymatic assay for the detection of human antibodies against Trypanosoma cruzi calreticulin, an immunodominant antigen. Acta Tropica 75: 291-300. (Pubitemid 30320866)
49. MATTHEWS, K. R., J. R. ELLIS, AND A. PATEROU. 2004. Molecular regulation of the life cycle of African trypanosomes. Trends in Parasitology 20: 40-47. (Pubitemid 38045238)
50. NAMANGALA, B., W. NOEL, P. DE BAETSELIER, L. BRYS, AND A. BESCHIN. 2001. Relative contribution of interferon- c and interleukin-10 to resistance to murine African trypanosomiasis. Journal of Infectious Disease 183: 1794-1800. (Pubitemid 32523243)
51. NARESHA, S., A. SURYAWANSHI, M. AGARWAL, B. P. SINGH, AND P. JOSHI. 2009. Mapping the complement C1q binding site in Haemonchus contortus calreticulin. Molecular and Biochemical Parasitology 166: 42-46.
52. NORRIS, K. A. 1998. Stable transfection of Trypanosoma cruzi epimastigotes with the trypomastigote-specific complement regulatory protein cDNA confers complement resistance. Infection and Immunity 66: 2460-2465 (Pubitemid 28261739)
53. B. BRADT, N. R. COOPER, AND M. SO. 1991. Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the human complement regulatory protein, decayaccelerating factor. Journal of Immunology 147: 2240-2247.
54. J. E. SCHRIMPF AND M. J. SZABO. 1997. Identification of the gene family encoding the 160-kilodalton Trypanosoma cruzi complement regulatory protein. Infection and Immunity 65: 349-357. (Pubitemid 27053194)
55. OLADIRAN, A., D. BEAUPARLANT, AND M. BELOSEVIC. 2011. The expression analysis of inflammatory and antimicrobial genes in the goldfish (Carassius auratus L.) infected with Trypanosoma carassii. Fish and Shellfish Immunology 31: 606-613.
56. AND M. BELOSEVIC. 2009. Trypanosoma carassii hsp70 increases expression of inflammatory cytokines and chemokines in macrophages of the goldfish (Carassius auratus L.). Developmental and Comparative Immunology 33: 1128-1136., AND 2010. Trypanosoma carassii calreticulin binds host complement component C1q and inhibits classical complement pathway-mediated lysis. Developmental and Comparative Immunology 34: 396-405.
57. OLSSON, T., M. BAKHIET, C. EDLUND, B. HOJEBERG, P. H. VAN DER MEIDE, AND K. KRISTENSSON. 1991. Bidirectional activating signals between Trypanosoma brucei and CD8+ T cells: A trypanosome-released factor triggers interferon-gamma production that stimulates parasite growth. European Journal of Immunology 21: 2447-2454.
58. OVERATH, P., J. HAAG, M.G. MAMEZA, AND A. LISCHKE. 1999. Freshwater fish trypanosomes: Definition of two types, host control by antibodies and lack of antigenic variation. Parasitology 119: 591-601.
59. PAN, W., O. OGUNREMI, G. WEI, M. SHI, AND H. TABEL. 2006. CR3 (CD11b/CD18) is a major macrophage receptor for IgM antibodymediated phagocytosis of African trypanosomes: Diverse effect on subsequent synthesis of tumor necrosis factor a and nitric oxide. Microbes and Infection 5: 1209-1218. (Pubitemid 43831686)
60. PLOUFFE, D. A., AND M. BELOSEVIC. 2004. Enzyme treatment of Trypanosoma danilewskyi (Laveran and Mesnil) increases its susceptibility to lysis by the alternative complement pathway of goldfish Carassius auratus (L). Journal of Fish Disease 27: 277-285. (Pubitemid 38641587)
61. QADRI, S. 1962. An experimental study of the life cycle of Trypanosoma danilewskyi in the leech, Hemiclepsis marginata. Journal of Protozoology 9: 254-258.
62. RIBEIRO, C. H., N. C. LOPEZ, G. A. RAMIREZ, C. E. VALCK, M. C.MOLINA, L. AGUILAR, M. RODRIGUEZ, I. MALDONADO, R. MARTINEZ, C. GONZALEZ, ET AL. 2009. Trypanosoma cruzi calreticulin: A possible role in Chagas' disease autoimmunity. Molecular Immunology 46: 1092-1099.
63. RICHARDSON, J. P., R. P. BEECROFT, D. L. TOLSON, M. K. LIU, AND T. W. PEARSON. 1988. Procyclin: An unusual immunodominant glycoprotein surface antigen from the procyclic stage of African trypanosomes. Molecular and Biochemical Parasitology 31: 203-216.
64. ROBERTSON, M. 1912. Transmission of flagellates living in the blood of certain fresh-water fishes. Philosophical Transactions of the Royal Society 202: 29-50.
65. RODITI, I., A. FURGER, S. RUEPP, N. SCHURCH, AND P. BUTIKOFER. 1998. Unravelling the procyclin coat of Trypanosoma brucei. Molecular and Biochemical Parasitology 91: 117-130.
66. RUSZCZYK, A., M. FORLENZA, H. F. SAVELKOUL, AND G. F. WIEGERTJES. 2008. Molecular cloning and functional characterization of a cathepsin L-like proteinase from the fish kinetoplastid parasite Trypanosoma carassii. Fish Shellfish Immunology 24: 205-214.
67. SAMUDIO, M., S. MONTENEGRO-JAMES, M. CABRAL, J. MARTINEZ, A. ROJAS DE ARIAS, AND M. A. JAMES. 1998. Cytokine responses in Trypanosoma cruzi-infected children in Paraguay. American Journal Tropical Medicine 58: 119-121. (Pubitemid 28071420)
68. SCHLEIFER, K. W., AND J. M. MANSFIELD. 1993. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. Journal of Immunology 151: 5492-5503. (Pubitemid 23332359)
69. SEPULVEDA, P., M. HONTEBEYRIE, P. LIEGEARD, A. MASCILLI, AND K. A. NORRIS. 2000. DNA-Based immunization with Trypanosoma cruzi complement regulatory protein elicits complement lytic antibodies and confers protection against Trypanosoma cruzi infection. Infection and Immunity 68: 4986-4991.
70. SHARAFELDIN, A., M. HAMADIEN, A. DIAB, H.-L. LI, F.-D. SHI, AND M. BAKHIET. 1999. Cytokine profiles in the central nervous system and the spleen during the early course of experimental African trypanosomiasis. Scandinavian Journal of Immunology 50: 256-261. (Pubitemid 29399898)
71. SHI, M., G. WEI, W. PAN, AND H. TABEL. 2004. Trypanosoma congolense infections: Antibody-mediated phagocytosis by Kupffer cells. Journal of Leukocyte Biology 76: 399-405. (Pubitemid 39006954)
72. SILEGHEM, M., A. DARJI, R. HAMERS, M. VAN DE WINKEL, AND P. DE BAETSELIER. 1989. Dual role of macrophages in the suppression of interleukin 2 production and interleukin 2 receptor expression in trypanosome-infected mice. European Journal of Immunology 19: 829-835. (Pubitemid 19165441)
73. SILVA, J. S., P. J. MORRISSEY, K. H. GRABSTEIN, K. M. MOLLER, D. ANDERSON, AND S. G. REED. 1992. Interleukin 10 and interferon-c regulation of experimental Trypanosoma cruzi infection. Journal of Experimental Medicine 175: 169-174
74. G. N. R. VESPA, M. A. G. CARDOSO, J. C. S. ALIBERTI, AND F. Q. CUNHA. 1995. Tumor necrosis factor alpha mediates resistance to Trypanosoma cruzi infection in mice by inducing nitric oxide production in infected gamma interferon-activated macrophages. Infection and Immunity 63: 4862-4867.
75. SMITH, A. B., AND S. L. HAJDUK. 1995. Identification of haptoglobin as a natural inhibitor of trypanocidal activity in human serum. Proceedings of the National Academy of Sciences USA 92: 10262-10266.
76. STIJLEMANS, B., M. GUILLIAMS, G. RAES, A. BESCHIN, S. MAGEZ, AND P. DE BAESTSELIER. 2007. African trypanosomosis: From immune escape and immunopathology to immune intervention. Veterinary Parasitology 148: 3-13. (Pubitemid 47016765)
77. STUART, K., R. BRUN, S. CROFT, A. FAIRLAMB, R. E. GURTLER, J. MCkERROW, S. REED, AND R. TARLETON. 2008. Kinetoplastids: Related protozoan pathogens, different diseases. Journal of Clinical Investigation 118: 1301-1310. (Pubitemid 351500422)
78. TACHADO, D. S., AND L. SCHOFIELD. 1994. Glycosylphosphatidylinositol toxin of Trypanosoma brucei regulates IL-1a and TNF a expression in macrophages by protein tryrosine kinase mediated signal transduction. Biochemical and Biophysical Research Communication 205: 984-991.
79. TAKAHASHI, Y., H. MIYAMOTO, T. FUKUMA, T. NISHIYAMA, T. ARAKI, AND S. SHINKA. 1987. In vivo interaction between Trypanosoma gambiense and leucocytes in mice. Zentralblat Bakteriologie Mikrobiologie Hygiene A 264: 399-406.
80. TAYLOR, J. E., AND G. RUDENKO. 2006. Switching trypanosome coats: What's in the wardrobe? Trends in Genetics 22: 614-620. (Pubitemid 44740112)
81. TEMPLETON, T. J., L. M. IYER, V. ANANTHARAMAN, S. ENOMOTO, J. E. ABRAHANTE, G. M. SUBRAMANIAN, S.L.HOFFMAN, M. S. ABRAHAMSEN, AND L. ARAVIND. 2004. Comparative analysis of Apicomplexa and genomic diversity in eukaryotes. Genome Research 14: 1686-1695. (Pubitemid 39276425)
82. TURNER, C. M., AND J. D. BARRY. 1989. High frequency of antigenic variation in Trypanosoma brucei rhodesiense infections. Parasitology 99: 67-75. (Pubitemid 19219510)
83. UZONNA, J. E., R. S. KAUSHIK, J. R. GORDON, AND H. TABEL. 1998a. Immunoregulation in experimental murine Trypanosoma congolense infection: Anti-IL-10 antibodies reverse trypanosome-mediated suppression of lymphocyte proliferation in vitro and moderately prolong the lifespan of genetically susceptible BALB/c mice. Parasite Immunology 20: 293-302 (Pubitemid 28270942)
84. AND 1998b. Experimental murine Trypanosoma congolense infections. 1. Administration of anti-IFNgamma antibodies alters trypanosome-susceptible mice to a resistantlike phenotype. Journal of Immunology 161: 5507-5515.
85. Y. ZHANG, J. R. GORDON, AND H. TABEL. 1998. Experimental murine Trypanosoma congolense infections. II. Role of splenic adherent CD3+Thy1.2+ TCR-alpha beta- gamma delta- CD4+82 and CD3+Thy1.2+ TCR-alpha beta- gamma delta- CD4282 cells in the production of IL-4, IL-10, and IFN-gamma and in trypanosome-elicited immunosuppression. Journal of Immunology 161: 6189-6197. (Pubitemid 28539855)
86. VAIDYA, T., M. BAKHIET, K. L. HILL, T. OLSSON, K. KRISTENSSON, AND J. E. DONELSON. 1997. The gene for T lymphocyte triggering factor from African trypanosomes. Journal of Experimental Medicine 186: 433-438. (Pubitemid 27332901)
87. VALCK, C., G. RAMIREZ, N. LOPEZ, C. H. RIBEIRO, I. MALDONADO, G. SANCHEZ, V. P. FERREIRA, W. SCHWAEBLE, AND A. FERREIRA. 2010. Molecular mechanisms involved in the inactivation of the first component of human complement by Trypanosoma cruzi calreticulin. Molecular Immunology 47: 1516-1521.
88. VINCENDEAU, P., AND B. BOUTEILLE. 2006. Immunology and immunopathology of African trypanosomiasis. Annals of Brazillian Academy of Science 78: 645-665. (Pubitemid 44905149)
89. WEBB, H., N. CARNALL, L. VANHAMME, S. ROLIN, J. VAN DEN ABBEELE, S. WELBURN, E. PAYS, AND M. CARRINGTON. 1997. The GPI-phospholipase C of Trypanosoma brucei is nonessential but influences parasitemia in mice. Journal of Cell Biology 139: 103-114. (Pubitemid 27444084)
90. WOO, P. T. K. 1981. Acquired immunity against Trypanosoma danilewskyi in goldfish, Carassius auratus. Parasitology 83: 343-346.
91. WORLD HEALTH ORGANIZATION (WHO). 1998. Control and surveillance of African trypanosomiasis. Report of a WHO Expert Committee. WHO Technical Report Series No. 881, Geneva, Switzerland, 113 p.
92. -2001. African trypanosomiasis (sleeping sickness). Report of the scientific working group meeting on African trypanosomiasis. World Health Organization, Geneva, Switzerland, 169 p.
93. -2002. Control of Chagas' disease, WHO Technical Report Series No. 905. World Health Organization, Geneva, Switzerland, 109 p.
94. XONG, H., L. VANHAMME, M. CHAMEKH, C. E. CHIMFWEMBE, J. VAN DEN ABBEELE, A. PAYS, N. VAN MEIRVENNE, R. HAMERS, P. DE BAETSELLER, AND E. PAYS. 1998. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 95: 839-846. (Pubitemid 29014463)
95. ZHANG, L., AND R. L. TARLETON. 1996. Characterization of cytokine production in murine T. cruzi infection by in situ immunochemistry: Lack of association between susceptibility and T helper type 2 cytokine production. European Journal of Immunology 26: 102-109.