How the African trypanosomes evade host immune killing

Parasite Immunology

Volumn 33, Issue 8, 2011, Pages 430-437

  Namangala, B ^a  

^a UNIVERSITY OF ZAMBIA   (Zambia)

Author keywords

African trypanosomes; Antigenic variation; Immunomodulation

Indexed keywords

AFRICAN TRYPANOSOME; AFRICAN TRYPANOSOMIASIS; ANTIGEN PRESENTING CELL; COMPLEMENT ACTIVATION; DISEASE COURSE; HOST PARASITE INTERACTION; HUMAN; IMMUNE EVASION; IMMUNE SYSTEM; IMMUNITY; IMMUNOMODULATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PARASITE IMMUNITY; PARASITE SURVIVAL; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TRYPANOSOMA;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENIC VARIATION; B-LYMPHOCYTES; COMPLEMENT ACTIVATION; CYTOKINES; HOST-PARASITE INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MICE; PRIMATES; T-LYMPHOCYTES; TRYPANOSOMA; TRYPANOSOMIASIS, AFRICAN;

PROTOZOA;

EID: 79960395606     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2011.01280.x     Document Type: Review

References (95)

1. Borst P & Rudenko G. Antigenic variation in African trypanosomes. Science 1994; 264: 1872-1873.
2. Cross GAM. Cellular and genetic aspects of antigenic variation in trypanosomes. Annu Rev Immunol 1990; 8: 83-110.
3. Pays E. The variant surface glycoprotein as a tool for adaptation in African trypanosomes. Microbes Infect 2006; 8: 930-937.
4. Borst P. Antigenic variation and allelic exclusion. Cell 2002; 109: 5-8.
5. Van-der-Ploeg LH, Gottesdiener K & Lee MG. Antigenic variation in African trypanosomes. Trends Genet 1992; 8: 452-457.
6. Vickerman K. Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull 1985; 41: 105-114.
7. Vickerman K, Tetley L, Hendry KAK, et al. Biology of African trypanosomes in the tsetse fly. Biol Cell 1988; 64: 109-119.
8. Barry JD & Emergy DL. Parasite development and host responses during the establishment of Trypanosoma brucei infection transmitted by tsetse fly. Parasitology 1984; 88: 67-84.
9. Turner CMR, Aslam N & Dye C. Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology 1995; 111: 289-300.
10. Maxie MG & Losos GJ. Release of Trypanosoma congolense from the microcirculation of cattle by Berenil. Vet Parasitol 1977; 3: 277-281.
11. Banks KL. Binding of Trypanosoma congolense to the wall of small blood vessels. J Protozool 1978; 25: 241-245.
12. Banks KL. Injury induced by Trypanosoma congolense adhesion to cell membranes. J Parasitol 1980; 66: 34-37.
13. Cross GA, Wirtz LE & Navarro M. Regulation of VSG expression site transcription and switching in Trypanosoma brucei. Mol Biochem Parasitol 1998; 91: 77-91.
14. Borst P. Molecular genetics of antigenic variation. Immunol Today 1991; 12: A29-A33.
15. Morrison LJ, Marcello L & McCulloch R. Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complex. Cell Microbiol 2009; 11: 1724-1734.
16. Namangala B, De Baetselier P, Brys L, et al. Attenuation of Trypanosoma brucei is associated with reduced immunosuppression and concomitant production of Th2 lymphokines. J Infect Dis 2000; 181: 1110-1120.
17. Namangala B, Sugimoto C & Inoue N. Effects of exogenous transforming factor β on Trypanosoma congolense infection in mice. Infect Immun 2007; 75: 1878-1885.
18. + T cell-Depletion on Acute Lethal Infection of Mice with Trypanosoma congolense. J Vet Med 2008; 70: 751-759.
19. Stijlemans B, Guilliams M, Raes G, et al. African trypanosomosis: from immune escape and immunopathology to immune intervention. Vet Parasitol 2007; 148: 3-13.
20. Magez S, Schwegmann A, Atkinson R, et al. The role of B-cells and IgM antibodies in parasitemia and VSG switching in Trypanosoma brucei-infected mice. PLoS Pathog 2008; 4: e1000122.
21. + T cells mediate early mortality in highly susceptible mice. J Immunol 2006; 176: 1724-1732.
22. Mansfield JM & Paulnock DM. Regulation of innate and acquired immunity in African trypanosomiasis. Parasite Immunol 2005; 27: 361-371.
23. Barry JD & McCulloch R. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv Parasitol 2001; 49: 1-70.
24. Hudson KM, Byner C, Freeman J, et al. Immunodepression, high IgM levels and evasion of the immune response in murine trypanosomiasis. Nature 1976; 264: 256-258.
25. Rurangirwa FR, Tabel H, Losos GJ, et al. Suppression of antibody response to Leptospira biflexa and Brucella abortus and recovery from immunosuppression after Berenil treatment. Infect Immun 1979; 26: 822-826.
26. Askonas BA. Macrophages as mediators of immunosuppression in murine African trypanosomiasis. Curr Top Microbiol Immunol 1985; 117: 119-127.
27. Goodwin IG, Green DG, Guy MW, et al. Immunosuppression during trypanosomiasis. Br J Exp Pathol 1970; 53: 40-43.
28. Sharpe RT, Langley AM, Mowat GN, et al. Immunosuppression in bovine trypanosomiasis: response of cattle infected with Trypanosoma congolense to foot-and-mouth disease vaccination and subsequent live virus challenge. Res Vet Sci 1982; 32: 289-293.
29. Yamamoto K, Onodera M, Kato K, et al. Involvement of suppressor cells induced with membrane fractions of trypanosomes in immunosuppression on trypanosomiasis. Parasite Immunol 1985; 7: 95-106.
30. Gomez-Rodriquez J, Stijlemans B, De Muylder G, et al. Identification of a parasitic modulatory protein triggering the development of suppressive M1 macrophages during African trypanosomiasis. J Infect Dis 2009; 200: 1849-1860.
31. Jayawardena AN, Waksman BH & Eardley DD. Activation of distinct helper and suppressor T cells in experimental trypanosomiasis. J Immunol 1978; 121: 622-628.
32. Namangala B, De Baetselier P, Noël W, et al. Alternative versus classical macrophage activation during experimental African trypanosomosis. J Leukoc Biol 2001; 69: 387-396.
33. De Baetselier P, Namangala B, Noël W, et al. Alternative versus classical macrophage activation during experimental African trypanosomosis: a review. Int J Parasitol 2001; 31: 574-586.
34. Noel W, Hassanzadeh G, Raes G, et al. Infection stage-dependent modulation of macrophage activation in Trypanosoma congolense-resistant and -susceptible mice. Infect Immun 2002; 70: 6180-6187.
35. Stijlemans B, Vankrunkelsven A, Brys L, et al. Scrutinizing the mechanisms underlying the induction of anemia of inflammation through GPI-mediated modulation of macrophage activation in a model of African trypanosomiasis. Microbes Infect 2010; 12: 389-399.
36. Kodelja V, Müller C, Politz O, et al. Alternative macrophage activation-associated CC-chemokine-1, a novel structural homologue of macrophage inflammatory protein-α with a Th2-associated expression pattern. J Immunol 1998; 160: 1411-1418.
37. Munder M, Eichmann K, Morán JM, et al. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J Immunol 1999; 163: 3771-3777.
38. Xong HV, Vanhamme L, Chamekh M, et al. A VSG expression site-associated gene confers resistance to human serum in Trypanosoma rhodesiense. Cell 1998; 95: 839-846.
39. Vanhollebeke B, Truc P, Poelvoorde P, et al. Human Trypanosoma evansi infection linked to a lack of apolipoprotein L-1. N Engl J Med 2006; 355: 2752-2756.
40. Vanhamme L, Paturiaux-Hanocq F, Poelvoorde P, et al. Apolipoprotein L-1 is the trypanosome lytic factor of human serum. Nature 2003; 422: 83-87.
41. Vanhollebeke B & Pays E. The function of apolipoproteins L. Cell Mol Life Sci 2006; 63: 1937-1944.
42. Vanhollebeke B & Pays E. The trypanolytic factor of human serum: many ways to enter the parasite, a single way to kill. Mol Microbiol 2010; 76: 806-814.
43. Wheeler RJ. The trypanolytic factor-mechanism, impacts and applications. Trends Parasitol 2010; 26: 457-464.
44. Vanhollebeke B, De Muylder G, Nielsen MJ, et al. A haptoglobin-hemoglobin receptor conveys innate immunity to Trypanosoma brucei in humans. Science 2008; 320: 677-681.
45. Molina-Portela MP, Samanovic M & Raper J. Distinct roles of apolipoprotein components within the trypanosome lytic factor complex revealed in a novel transgenic mouse model. J Exp Med 2008; 205: 1721-1728.
46. de Greef C & Hamers R. The serum resistance-associated (SRA) gene of Trypanosoma brucei rhodesiense encodes a variant surface glycoprotein-like protein. Mol Biochem Parasitol 1994; 68: 277-284.
47. Radwanska M, Chamekh M, Van Hamme L, et al. The serum resistance-associated gene as a diagnostic tool for the detection of Trypanosoma brucei rhodesiense. Am J Trop Med Hyg 2002; 67: 684-690.
48. Oli MW, Cotlin LF, Shiflett AM & Hajduk SL. Serum resistance-associated protein blocks lysosomal targeting of trypanosome lytic factor in Trypanosoma brucei. Eukaryot Cell 2006; 5: 132-157.
49. Lugli EB, Pouliot M, Portela Mdel P, et al. Characterization of primate trypanosome trypanolytic factors. Mol Biochem Parasitol 2004; 138: 9-20.
50. Poelvoorde P, Vanhamme L, Van Den Abbeele J, et al. Distribution of apolipoprotein L-1 and trypanosome lytic activity among primate sera. Mol Biochem Parasitol 2004; 134: 155-157.
51. Thomson R, Molina-Portela P, Mott H, et al. Hydrodynamic gene delivery of baboon trypanosome lytic factor eliminates both animal- and human-infective African trypanosomes. PNAS 2009; 106: 19509-19514.
52. Freedman BI, Kopp JB, Langefeld CD, et al. The apoliprotein L1 (APOL1) gene and nodiabetic nephropathy in African Americans. J Am Soc Nephrol 2010; 21: 1422-1426.
53. Genovese G, Friedman DJ, Ross MD, et al. Association of trypanolytic APOL1 variants with kidney disease in African-Americans. Science 2010; 329: 841-845.
54. Ngaira JM, Nantulya VM, Musoke AJ, et al. Phagocytosis of antibody-sensitized Trypanosoma brucei in vitro by bovine peripheral blood monocytes. Immunology 1983; 49: 393-400.
55. Stevens DR & Moulton JE. Ultrastructural and immunological aspects of the phagocytosis of Trypanosoma brucei by mouse peritoneal macrophages. Infect Immun 1978; 19: 972-982.
56. Takayanagi T, Kawaguchi H, Yabu Y, et al. Contribution of the complement system to antibody-mediated binding of Trypanosoma gambiense to macrophages. J Parasitol 1987; 73: 333-341.
57. Greenwood BM, Whittle HC & Molyneux DM. Immunosuppression in Gambian trypanosomiasis. Trans R Soc Trop Med Hyg 1973; 67: 846-850.
58. Russo DC, Williams DJ & Grab DJ. Mechanisms for the elimination of potentially lytic complement-fixing variable surface glycoprotein antibody-complexes in Trypanosoma brucei. Parasitol Res 1994; 80: 487-492.
59. Pan W, Ogunremi O, Wei G, et al. 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 and nitric oxide. Microbes Infect 2006; 8: 1209-1218.
60. Ferrante A & Allison AC. Alternative pathway activation of complement by African trypanosomes lacking a glycoprotein coat. Parasite Immunol 1983; 5: 491-498.
61. Devine DV, Falk RJ & Balber AE. Restriction of the alternative pathway of human complement by intact Trypanosoma brucei subsp. gambiense. Infect Immun 1986; 52: 223-229.
62. Nieslen K. Immunology and pathogenesis of trypanosomiais. In Tizard I (ed.): Complement in Trypanosomiais. Boca Raton, FL, CRC Press, 1985: 133-144.
63. Musoke AJ & Barbet AF. Activation of complement by variant-specific surface antigen of Trypanosoma brucei. Nature 1977; 270: 438-440.
64. Sheppard J, Nielsen K, Tizard I, et al. Direct activation of complement by trypanosomes. J Parasitol 1978; 64: 544-546.
65. Pierre P & Mellman I. Exploring the mechanisms of antigen processing by cell fractionation. Curr Opin Immunol 1998; 10: 145-153.
66. Namangala B, Brys L, Magez S, et al. Trypanosoma brucei brucei infection impairs MHC Class II antigen presentation capacity of macrophages. Parasite Immunol 2000; 22: 361-370.
67. Dagenais TR, Freeman BE, Demick KP, et al. Processing and presentation of variant surface glycoprotein molecules to T cells in African trypanosomiasis. J Immunol 2009; 183: 3344-3355.
68. Shi MQ, Wei GJ & Tabel H. Trypanosoma congolense infections: MHC class II-restricted immune responses mediate either protection or disease, depending on IL-10 function. Parasite Immunol 2007; 29: 107-111.
69. Bagasra O, Schell RF & Le Frock JL. Evidence for depletion of Ia+ macrophages and associated immunosuppression in African trypanosomiasis. Infect Immun 1981; 32: 188-193.
70. Paulnock DM, Smith C & Mansfield JM. Antigen Presenting Cell Function in African Trypanosomiasis. New York: Alan R Liss, Inc, 1989: 135-144.
71. Schleifer KW, Filutowicz H, Schopf LR & Mansfield JM. Characterization of T helper cell responses to the trypanosome variant surface glycoprotein. J Immunol 1993; 150: 2910-2919.
72. Dagenais TT, Demick KP, Bangs JD, et al. T cell response to the trypanosome variant surface glycoprotein are not limited to hypervariable subregions. Infect Immun 2009; 77: 141-151.
73. Sileghem M, Flynn JN, Logan-Henfrey L, et al. Tumor 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 Immunol 1994; 16: 51-54.
74. Radwanska M, Guirnalda P, De Trez C, et al. Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog 2008; 4: e1000078.
75. Flynn JN & Sileghem M. The role of the macrophage in induction of immunosuppression in Trypanosoma congolense-infected cattle. Immunology 1991; 74: 310-316.
76. De Baetselier P. T-cell subsets and cytokine interplay in infectious disease. In Mustafa AS, Al-Attiyah RJ, Nath I & Chugh TD (eds): Mechanisms Underlying Trypanosome-induced T-cell Immunosuppression. Basle, S. Karger, 1996: 124-139.
77. Beschin A, Brys L, Magez S, et al. Trypanosoma brucei infection elicits nitric oxide-dependent and nitric oxide-independent suppressive mechanisms. J Leukoc Biol 1998; 63: 429-439.
78. Mabbott NA, Coulson PS, Smythies LE, et al. African trypanosome infections in mice that lack the interferon-γ receptor gene: nitric oxide-dependent and independent suppression of T cell proliferative responses and the development of anaemia. Immunology 1998; 94: 476-480.
79. Sternberg JM. Immunobiology of African trypanosomiasis. Chem Immunol 1998; 70: 186-199.
80. Taylor KA. Immune responses of cattle to African trypanosomes: protective or pathogenic? Int J Parasitol 1998; 28: 219-240.
81. Uzonna JE, Kaushik RS, Gordon JR, et al. Experimental murine Trypanosoma congolense infections. I. Administration of anti-IFN-γ antibodies alters trypanosome-susceptible mice to a resistant-like phenotype. J Immunol 1998; 161: 5507-5515.
82. Taylor KA, Lutje V & Mertens B. Nitric oxide synthesis is depressed in Bos indicus cattle infected with Trypanosoma congolense and Trypanosoma vivax and does not mediate T cell suppression. Infect Immun 1996; 64: 4115-4122.
83. Namangala B, De Baetselier P & Beschin A. Both Type-I and Type-II responses contribute to murine trypanotolerance. J Vet Med 2009; 71: 313-318.
84. Namangala B, De Baetselier P & Beschin A. Quantitative differences in immune responses in mouse strains that differ in their susceptibility to Trypanosoma brucei brucei infection. J Vet Med 2009; 71: 951-956.
85. Drennan MB, Stijlemans B, Van Den Abbeele J, et al. The induction of a type 1 immune response following a Trypanosoma brucei infection is MyD88-dependent. J Immunol 2005; 175: 2501-2509.
86. Magez S, Radwanska M, Drennan M, et al. Interferon-gamma and nitric oxide in collaboration with antibodies are key protective host immune factors during trypanosome Tc13 infections. J Infect Dis 2006; 193: 1575-1583.
87. Stijlemans B, Baral TN, Guilliams M, et al. A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis-associated immunopathology. J Immunol 2007; 179: 4003-4014.
88. Guilliams M, Oldenhove G, Noel W, et al. African trypanosomiasis: naturally occurring regulatory T cells favour trypanotolerance by limiting pathology associated with sustained type I inflammation. J Immunol 2007; 179: 2748-2757.
89. Magez S, Radwanska M, Drennan M, et al. Tumor necrosis factor (TNF) receptor-1 (TNFp55) signal transduction and macrophage-derived soluble TNF are crucial for nitric oxide-mediated Trypanosoma congolense parasite killing. J Infect Dis 2007; 196: 954-962.
90. Hertz CJ, Filutowicz H & Mansfield JM. Resistance to African tyrpanosomes is IFN-γ dependent. J Immunol 1998; 161: 6775-6783.
91. Wei G & Tabel H. Regulatory T cells prevent control of experimental African trypanosomiasis. J Immunol 2008; 180: 2514-2521.
92. Buza J, Sileghem M, Gwakisa P & Naessens J. CD5+ B lymphocytes are the main source of antibodies reactive with non-parasite antigens in Trypanosoma congolense-infected cattle. Immunology 1997; 92: 226-233.
93. Williams DJL, Taylor KA, Newson J, et al. The role of anti-variable surface glycoprotein antibody responses in bovine trypanotolerance. Parasite Immunol 1996; 18: 209-218.
94. Buza J & Naessens J. Trypanosome non-specific IgM antibodies detected in serum of Trypanosoma congolense-infected cattle is polyreactive. Vet Immunol Immunopathol 1999; 69: 1-9.
95. Sacks DL & Askonas BA. Trypanosome-induced suppression of anti-parasite responses during experimental African trypanosomiasis. Eur J Immunol 1980; 10: 971-974.