Attenuation of Trypanosoma brucei is associated with reduced immunosuppression and concomitant production of Th2 lymphokines

Journal of Infectious Diseases

Volumn 181, Issue 3, 2000, Pages 1110-1120

  Namangala, Boniface ^a   De Baetselier, Patrick ^a   Brijs, Lea ^a   Stijlemans, Benoît ^a   Noël, Wim ^a   Pays, Etienne ^b   Carrington, Mark ^c   Beschin, Alain ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b FREE UNIVERSITY OF BRUSSELS   (Belgium)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONCANAVALIN A; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 4; PHOSPHOLIPASE C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; CYTOKINE PRODUCTION; FEMALE; HOST RESISTANCE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; PROTOZOAL INFECTION; TRYPANOSOMA BRUCEI;

ANIMALS; ANTIBODIES, PROTOZOAN; CYTOKINES; FEMALE; IMMUNE TOLERANCE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, SCID; PARASITEMIA; PHOSPHOLIPASE C; TH2 CELLS; TRYPANOSOMIASIS, AFRICAN;

EID: 0034037627     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/315322     Document Type: Article

References (54)

1. 1. Cross GAM. Cellular and genetic aspects on antigenic variation in trypanosomes. Annu Rev Immunol 1990;8:83-110.
2. 2. Pays E, Vanhamme L, Berberof M. Genetic control for expression of surface antigens in African trypanosomes. Annu Rev Microbiol 1994;48:25-52.
3. 3. Borrowy NK, Sternberg JM, Schreiber D, Nonnengaesser C, Overath P. Suppressive macrophages occuring in murine T. brucei infection inhibit T-cell responses in vivo and in vitro. Parasite Immunol 1990;12:233-46.
4. 4. Kierzenbaum F, Muthukkumar S, Beltz LA, Sztein MB. Suppression by Trypanosoma brucei rhodesiense of the capacities of human T lymphocytes to express interleukin-2 receptors and proliferate after mitogenic stimulation. Infect Immun 1991;59:3518-22.
5. 5. Schleifer KW, Mansfield JM. Suppressor macrophages in African trypanosomiasis inhibit T cell proliferative responses by nitric oxide and prostaglandins. J Immunol 1993;151:5492-503.
6. 6. Sileghem M, Darji A, Hamers R, Van De Winkel M, De Baetselier P. Dual role of macrophages in the suppression of interleukin 2 production and interleukin 2 receptor expression in trypanosome-infected mice. Eur J Immunol 1989;19:829-35.
7. 7. Sileghem M, Darji A, Remels L, Hamers R, De Baetselier P. Different mechanisms account for the suppression of interleukin 2 production and the suppression of interleukin 2 receptor expression in Trypanosoma brucei-infected mice. Eur J Immunol 1989;19:119-24.
8. 8. Darji A, Sileghem M, Heremans H, Brys L, De Baetselier P. Inhibition of T-cell responsiveness during experimental infections with Trypanosoma brucei: active involvement of endogenous gamma interferon. Infect Immun 1993;61:3098-102.
9. 9. Beschin A, Brys L, Magez S, Radwanska M, De Baetselier P. Trypanosoma brucei infection elicits nitric oxide-dependent and nitric oxide-independent suppressive mechanisms. J Leukoc Biol 1998;63:429-39.
10. 10. Mabbott NA, Sutherland IA, Sternberg JM. Suppressor macrophages in Trypanosoma brucei infection: nitric oxide is related to both suppressive activity and life span in vivo. Parasite Immunol 1995;17:143-50.
11. 11. Mabbott NA, Coulson PS, Smythies LE, Wilson RA, Sternberg JM. 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: 476-80.
12. 12. Darji A, Beschin A, Sileghem M, Heremans H, Brys L, De Baetselier P. In vitro simulation of immunosuppression caused by Trypanosoma brucei: active involvement of gamma interferon and tumor necrosis factor in the pathway of suppression. Infect Immun 1996;64:1937-43.
13. 13. Magez S, Radwanska M, Beschin A, Sekikawa K, De Baetselier P. Tumor necrosis factor alpha is a key mediator in the regulation of experimental Trypanosoma brucei infections. Infect Immun 1999;67:3128-32.
14. 14. Levine RF, Mansfield JM. Genetics of resistance to the African trypanosomes, III: variant specific antibody responses of H-2 compatible resistant and susceptible mice. J Immunol 1984;133:1564-9.
15. 15. Ogunremi O, Tabel H. Genetics of resistance to Trypanosoma congolense in inbred mice: efficiency of apparent clearance of parasites correlates with long-term survival. J Parasitol 1995;81:876-81.
16. 16. Taylor KA. Immune responses of cattle to African trypanosomes: protective or pathogenic? Int J Parasitol 1998;28:219-40.
17. 17. Taylor KA, Lutje V, Kennedy D, et al. Trypanosoma congolense: B-lymphocyte responses differ between trypanotolerant and trypanosusceptible cattle. Exp Parasitol 1996;83:106-16.
18. 18. Authie E, Duvallet G, Robertson C, Williams DJL. Antibody response to a 33 kDa cysteine protease of Trypanosoma congolense: relationship to "trypanotolerance" in cattle. Parasite Immunol 1993;15:465-74.
19. 19. Authie E, Muteti DK, Williams DJL. Antibody response to invariant antigens of Trypanosoma congolense in cattle of differing susceptibility to trypanosomiasis. Parasite Immunol 1993;15:101-11.
20. 20. De Gee ALW, Levine RR, Mansfield JM. Genetics of resistance to the African trypanosomes. VI. Heredity of resistance and variable surface glycoprotein-specific immune responses. J Immunol 1988;140:283-8.
21. 21. Whitelaw DD, Mac Askill JA, Holmes PH, Jennings FW, Urquhart GM. Immune mechanisms in C57B1 mice genetically resistant to Trypanosoma congolense infection. I. Effects of immune modulation. Parasite Immunol 1983;5:85-94.
22. 22. Mansfield JM. Immunology of African trypanosomes. In: Weiler DJ, ed. Modern parasite biology. New York: J. Freeman, 1990:222-46.
23. 23. 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.
24. 24. Uzonna JE, Kaushik RS, Gordon JR, Tabel H. Experimental murine Trypanosoma congolense infections. I. Administration of anti-IFN-γ antibodies alters trypanosome-susceptible mice to a resistant-like phenotype. J Immunol 1998;161:5507-15.
25. 25. Uzonna JE, Kaushik RS, Gordon JR, Tabel H. 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 Immunol 1998;20:293-302.
26. 26. Uzonna JE, Kaushik RS, Gordon JR, Tabel H. Cytokines and antibody responses during Trypanosoma congolense infections in two inbred mouse strains that differ in resistance. Parasite Immunol 1999;21:57-71.
27. 27. Kaushik RS, Uzonna JE, Radzioch D, Gordon JR, Tabel H. Innate resistance to experimental Trypanosoma congolense infection: differences in IL-10 synthesis by macrophage cell lines from resistant and susceptible inbred mice. Parasite Immunol 1999;21:119-31.
28. 28. Hertz CJ, Filutowicz H, Mansfield JM. Resistance to the African trypanosomes is IFN-γ-dependent. J Immunol 1998;161:6775-83.
29. 29. Hertz CJ, Mansfield JM. IFN-γ-dependent nitric oxide production is not linked to resistance in experimental African trypanosomiasis. Cell Immunol 1999;192:24-32.
30. 30. Webb H, Carnall N, Vanhamme L, et al. The GPI-phospholipase C of Trypanosoma brucei in nonessential but influences parasitemia in mice. J Cell Biol 1997;139:103-14.
31. 31. Magez S, Stijlemans B, Radwanska M, Pays E, Ferguson MAJ, De Baetselier P. The glysosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. J Immunol 1998;160:1949-56.
32. 32. Turner CMR, Aslam N, Dye C. Replication, differentiation, growth and the virulence of Trypanosoma brucei infections. Parasitology 1995;111: 289-300.
33. 33. Carrington M, Carnall N, Crow MS, et al. The properties and function of the glycosylphosphatidylinositol-phospholipase C in Trypanosoma brucei. Mol Biochem Parasitol 1998;91:153-64.
34. 34. Taylor K, 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: 4115-22.
35. 35. Flynn JN, Sileghem M. The role of macrophage in induction of immunosuppression in Trypanosoma congolense-infected cattle. Immunology 1991;74:310-6.
36. 36. Sileghem M, Flynn JN. Suppression of interleukin-2 secretion and interleukin-2 receptor expression during tsetse-transmitted trypanosomiasis in cattle. Eur J Immunol 1992;22:767-73.
37. 37. Al-Ramadi BK, Chen YW, Meissler JJJ, Eisenstein TK. Immunosuppression induced by attenuated Salmonella: reversal by IL-4. J Immunol 1991;147: 1954-61.
38. 38. Al-Ramadi BK, Meissler JJJ, Huang D, Eisenstein TK. Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur J Immunol 1992;22:2249-54.
39. 39. Ding L, Linsley PS, Huang L, Germain RN, Shevach EM. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol 1993;151:1224-34.
40. 40. Fiorentino DF, Zlotnik A, Vicira P, et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 1991;146: 3444-51.
41. 41. Howard M, O'Garra A. Biological properties of interleukin 10. Immunol Today 1992;13:198-200.
42. 42. Goerdt S, Orfanos CE. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 1999;10:137-42.
43. 43. Schleifer KW, Filutowicz H, Schopf LR, Mansfield JM. Characterization of T helper cell responses to the trypanosome variant surface glycoprotein. J Immun 1993;150:2910-9.
44. 44. Schopf LR, Filutowicz H, Bi XJ, Mansfield JM. Interleukin-4-dependent immunoglobulin G1 isotype switch in the presence of a polarized antigen-specific Th1-cell response to trypanosome variant surface glycoprotein. Infect Immun 1998;66:451-61.
45. 45. Taylor-Robinson AW. Regulation of immunity to malaria: valuable lessons learned form murine models. Parasitol Today 1995,11:334-42.
46. 46. Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-γ. Annu Rev Immunol 1997;15:749-95.
47. 47. Finkelman FD, Holmes J, Katona IM, et al. Lymphokine control of in vivo immunoglobulin isotype selection. Annu Rev Immunol 1990;8:303-33.
48. 48. Mertens B, Taylor K, Muriuki C, Rocchi M. Cytokine mRNA profiles in trypanotolerant and trypanosusceptible cattle infected with the protozoan parasite Trypanosoma congolense: protective role for interleukin-4? J Interferon Cytokine Res 1999;19:59-65.
49. 49. Taylor K, Mertens B, Lutje V, Saya R. Trypanosoma congolense infection of trypanotolerant N'Dama (Bos taurus) cattle is associated with decreased secretion of nitric oxide by interferon-γ-activated monocytes and increased transcription of interleukin-10. Parasite Immunol 1998;20:421-9.
50. 50. Williams DJL, Taylor K, Newson J, Gichuki B, Naessens J. The role of anti-variable surface glycoprotein antibody responses in bovine trypanotolerance. Parasite Immunol 1996;18:209-18.
51. 51. Mensa-Wilmot K, Garg N, McGwire BS, et al. Roles of free GPIs in amastigotes of Leishmania. Mol Biochem Parasitol 1999;99:103-16.
52. 52. Carnall N, Webb H, Carrington M. Mutagenesis study of the glycosylphosphatidylinositol phospholipase C of VSG. Mol Biochem Parasitol 1997; 90:423-32.
53. 53. Mensa-Wilmot K, Hereld D, Englund PT. Glycosylphosphatidylinositol-specific phospholipase C of Trypanosoma brucei: expression in Escherichia coli. Mol Biochem Parasitol 1992;56:311-22.
54. 54. Rolin S, Hanocq-Quertier J, Paturiaux-Hanocq F, et al. Simultaneous but independent activation of adenylate cyclase and glycophosphatidylinositol-phospholipase C under stress conditions in Trypanosoma brucei. J Biol Chem 1996;271:10844-52.