Intradermal infections of mice by low numbers of African trypanosomes are controlled by innate resistance but enhance susceptibility to reinfection

Journal of Infectious Diseases

Volumn 203, Issue 3, 2011, Pages 418-429

  Wei, Guojian ^a   Bull, Harold ^a   Zhou, Xia ^a,b   Tabel, Henry ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b SHIHEZI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ADAPTIVE IMMUNITY; AFRICAN TRYPANOSOMIASIS; ANIMAL EXPERIMENT; ARTICLE; CYTOKINE PRODUCTION; FEMALE; INFECTION SENSITIVITY; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REINFECTION; SPLEEN CELL; TRYPANOSOMA BRUCEI; TRYPANOSOMA CONGOLENSE; WILD TYPE;

ANIMALS; ANTIBODIES, PROTOZOAN; DISEASE SUSCEPTIBILITY; DNA-BINDING PROTEINS; FEMALE; IMMUNITY, INNATE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; TRYPANOSOMIASIS, AFRICAN;

EID: 79751484087     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jiq051     Document Type: Article

References (49)

1. Welburn SC, Coleman PG, Maudlin I, Fevre EM, Odiit M, Eisler MC. Crisis, what crisis? Control of Rhodesian sleeping sickness. Trends Parasitol 2006; 22:123-8. (Pubitemid 43290227)
2. Barrett MP, Burchmore RJ, Stich A, et al. The trypanosomiases. Lancet 2003; 362:1469-80. (Pubitemid 37352887)
3. Mulligan HW, Potts WH. The African trypanosomiases. New York: Wiley-INTERSCIENCES, 1970.
4. Tabel H, Kaushik RS, Uzonna JE. Susceptibility and resistance to Trypanosoma congolense infections. Microbes Infect 2000; 2:1619-29.
5. Barry JD, McCulloch R. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv Parasitol 2001; 49:1-70.
6. Borst P, Rudenko G, Blundell PA, et al. Mechanisms of antigenic variation in African trypanosomes. Behring Inst Mitt 1997; 18:1-15.
7. Cross GA. Cellular and genetic aspects of antigenic variation in trypanosomes. Annu Rev Immunol 1990; 8:83-110. (Pubitemid 20135622)
8. Askonas BA. Macrophages as mediators of immunosuppression in murine African trypanosomiasis. Curr Top Microbiol Immunol 1985; 117:119-27.
9. Hudson KM, Byner C, Freeman J, Terry RJ. Immunodepression, high IgM levels and evasion of the immune response in murine trypanosomiasis. Nature 1976; 264:256-8.
10. Roelants GE, Pinder M. Immunobiology of African trypanosomiasis. Contemp Top Immunobiol 1984; 12:225-74.
11. Sacks DL, Selkirk M, Ogilvie BM, Askonas BA. Intrinsic immunosuppressive activity of different trypanosome strains varies with parasite virulence. Nature 1980; 283:476-8. (Pubitemid 10142616)
12. Uzonna JE, Kaushik RS, Zhang Y, Gordon JR, Tabel H. Experimental murine Trypanosoma congolense infections. II. Role of splenic adherent CD31Thy1.21 TCR-alpha beta- gamma delta- CD418- and CD31Thy1.21 TCR-alpha beta- gamma delta- CD4-8- cells in the production of IL-4, IL-10, and IFN-gamma and in trypanosome-elicited immunosuppression. J Immunol 1998; 161:6189-97. (Pubitemid 28539855)
13. Ferguson MA. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci 1999; 112:2799-809. (Pubitemid 29430025)
14. Gerold P, Striepen B, Reitter B, et al. Glycosyl-phosphatidylinositols of Trypanosoma congolense: two common precursors but a new protein-anchor. J Mol Biol 1996; 261:181-94. (Pubitemid 26275801)
15. Gray AR, Luckins AG. The initial stage of infection with cyclically-transmitted Trypanosoma congolense in rabbits, calves and sheep. J Comp Pathol 1980; 90:499-512. (Pubitemid 11202147)
16. Macaskill JA, Holmes PH, Whitelaw DD, McConnell I, Jennings FW, Urquhart GM. Immunological clearance of 75Se-labelled Trypanosoma brucei in mice. II. Mechanisms in immune animals. Immunology 1980; 40:629-35.
17. Pan W, Ogunremi O, Wei G, Shi M, Tabel H. 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 Infect 2006; 8:1209-18. (Pubitemid 43831686)
18. Shi M, Wei G, Pan W, Tabel H. Trypanosoma congolense infections: antibody-mediated phagocytosis by Kupffer cells. J Leukoc Biol 2004; 76:399-405. (Pubitemid 39006954)
19. Basic biology and anatomy of the tsetse fly. ftp://ftp.fao.org/docrep/ fao/011/i0535e/i0535e01.pdf. Accessed 26 January 2009.
20. Fairbairn H, Burtt E. The infectivity to man of a strain of Trypanosoma rhodesiense transmitted cyclically by Glossina morsitans through sheep and antelope: evidence that man requires a minimum infective dose of metacyclic trypanosomes. Ann Trop Med Parasitol 1946; 40:270-313.
21. Barry JD, Emery DL. Parasite development and host responses during the establishment of Trypanosoma brucei infection transmitted by tsetse fly. Parasitology 1984; 88:67-84. (Pubitemid 14036270)
22. Beschin A, Brys L, Magez S, Radwanska M, De Baetselier P. Trypanosoma brucei infection elicits nitric oxide-dependent and nitric oxidein-dependent suppressive mechanisms. J Leukoc Biol 1998; 63:429-39. (Pubitemid 28163182)
23. Magez S, Radwanska M, Drennan M, et al. Interferon-gamma and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 infections. J Infect Dis 2006; 193:1575-83. (Pubitemid 43841392)
24. Mansfield JM, Paulnock DM. Regulation of innate and acquired immunity in African trypanosomiasis. Parasite Immunol 2005; 27:361-71. (Pubitemid 41413484)
25. Dagenais TR, Freeman BE, Demick KP, Paulnock DM, Mansfield JM. Processing and presentation of variant surface glycoprotein molecules to T cells in African trypanosomiasis. J Immunol 2009; 183:3344-55.
26. Tabel H. Activation of the alternative pathway of bovine complement by Trypanosoma congolense. Parasite Immunol 1982; 4:329-35. (Pubitemid 13255992)
27. Otesile EB, Tabel H. Enhanced resistance of highly susceptible Balb/c mice to infection with Trypanosoma congolense after infection and cure. J Parasitol 1987; 73:947-53. (Pubitemid 18022488)
28. Lanham SM, Godfrey DG. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol 1970; 28:521-34.
29. Shi M, Pan W, Tabel H. Experimental African trypanosomiasis: IFN-gamma mediates early mortality. Eur J Immunol 2003; 33:108-18. (Pubitemid 36163325)
30. Wei G, Tabel H. Regulatory T cells prevent control of experimental African trypanosomiasis. J Immunol 2008; 180:2514-21.
31. Campbell GH, Esser KM, Weinbaum FI. Trypanosoma rhodesiense infection in B-cell-deficient mice. Infect Immun 1977; 18:434-8. (Pubitemid 8232220)
32. Kaushik RS, Uzonna JE, Gordon JR, Tabel H. Innate resistance to Trypanosoma congolense infections: differential production of nitric oxide by macrophages from susceptible BALB/c and resistant C57Bl/6 mice. Exp Parasitol 1999; 92:131-43. (Pubitemid 29370071)
33. Vincendeau P, Daulouede S, Veyret B, Darde ML, Bouteille B, Lemesre JL. Nitric oxide-mediated cytostatic activity on Trypanosoma brucei gambiense and Trypanosoma brucei brucei. Exp Parasitol 1992; 75:353-60.
34. MacMicking J, Xie QW, Nathan C. Nitric oxide and macrophage function. Annu Rev Immunol 1997; 15:323-50. (Pubitemid 27169284)
35. Marcoux V, Wei G, Tabel H, Bull HJ. Characterization of major surface protease homologues of Trypanosoma congolense. J Biomed Biotechnol 2010; 2010:418157.
36. Tabel H, Wei G, Shi M. T cells and immunopathogenesis of experimental African trypanosomiasis. Immunol Rev 2008; 225:128-39.
37. Stevenson HL, Jordan JM, Peerwani Z, Wang HQ, Walker DH, Ismail N. An intradermal environment promotes a protective type-1 response against lethal systemic monocytotropic ehrlichial infection. Infect Immun 2006; 74:4856-64. (Pubitemid 44157273)
38. Fynan EF, Webster RG, Fuller DH, Haynes JR, Santoro JC, Robinson HL. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc Natl Acad Sci U S A 1993; 90:11478-82. (Pubitemid 24008662)
39. Devine DV, Falk RJ, Balber AE. Restriction of the alternative pathway of human complement by intact Trypanosoma brucei subsp. gambiense. Infect Immun 1986; 52:223-9. (Pubitemid 16137705)
40. Diffley P, Honigberg BM. Immunologic analysis of host plasma proteins on bloodstream forms of African pathogenic trypanosomes. II. Identification and quantitation of surface-bound albumin, nonspecific IgG, and complement on Trypanosoma congolense. J Parasitol 1978; 64:674-81. (Pubitemid 9039086)
41. Macadam RF, Herbert WJ. Fine structural demonstration of cytoplasmic protrusions (filopodia) in trypanosomes. Exp Parasitol 1970; 27:1-8.
42. Wright KA, Lumsden WH, Hales H. The formation of filopodium-like processes by Trypanosoma (Trypanozoon) brucei. J Cell Sci 1970; 6:285-97.
43. Frevert U, Reinwald E. Trypanosoma congolense bloodstream forms evade complement lysis in vitro by shedding of immune complexes. Eur J Cell Biol 1990; 52:264-9. (Pubitemid 20281562)
44. Shakibaei M, Frevert U. Cell surface interactions between Trypanosoma congolense and macrophages during phagocytosis in vitro. J Protozool 1992; 39:224-35.
45. Guilbride DL, Gawlinski P, Guilbride PD. Why functional pre-erythrocytic and bloodstage malaria vaccines fail: a meta-analysis of fully protective immunizations and novel immunological model. PLoS One 2010; 5:e10685.
46. World Health Organization. Rabies. http://www.who.int/immunization/ topics/rabies/en/index.html. Accessed 6 August 2010.
47. Brun R, Blum J, Chappuis F, Burri C. Human African trypanosomiasis. Lancet 2009; 375:148-59.
48. Gray AR. Immunological research and the problem of immunization against African trypanosomiasis. Trans R Soc Trop Med Hyg 1976; 70:119-21.
49. Stuart K, Brun R, Croft S, et al. Kinetoplastids: related protozoan pathogens, different diseases. J Clin Invest 2008; 118:1301-10. (Pubitemid 351500422)