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. 1991 Oct;74(2):310–316.

The role of the macrophage in induction of immunosuppression in Trypanosoma congolense-infected cattle.

J N Flynn 1, M Sileghem 1
PMCID: PMC1384610  PMID: 1748479

Abstract

Impairment of T-cell function in Boran (Bos indicus) cattle during primary infection with Trypanosoma congolense ILNat 3.1 was found to occur in peripheral blood, spleen and, in particular, the lymph nodes. Lymph node cells from infected cattle failed to proliferate in response to mitogenic stimulus and suppressed proliferation of both normal peripheral blood mononuclear cells and lymph node cells in co-culture assays. The addition of indomethacin, to inhibit prostaglandin synthesis, had no effect on the ability of lymph node cells from infected cattle to suppress the proliferative response of responder cells from uninfected cattle. The supplementation of the culture media with catalase, which degrades hydrogen peroxide, either alone or in combination with indomethacin, also did not result in restoration of proliferation. This suggested the presence of suppressor cells in lymph nodes of infected cattle which exert their effects via a prostaglandin-independent mechanism. By depleting lymph node cells from infected cattle of the monocyte-macrophage population using a cell sorter it was possible to abrogate the previously observed immunosuppression, thus indicating a key role for these macrophages in the induction of trypanosome-associated immunosuppression.

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Selected References

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  1. Akol G. W., Murray M. Early events following challenge of cattle with tsetse infected with Trypanosoma congolense: development of the local skin reaction. Vet Rec. 1982 Mar 27;110(13):295–302. doi: 10.1136/vr.110.13.295. [DOI] [PubMed] [Google Scholar]
  2. Borowy N. K., Sternberg J. M., Schreiber D., Nonnengasser C., Overath P. Suppressive macrophages occurring in murine Trypanosoma brucei infection inhibit T-cell responses in vivo and in vitro. Parasite Immunol. 1990 May;12(3):233–246. doi: 10.1111/j.1365-3024.1990.tb00951.x. [DOI] [PubMed] [Google Scholar]
  3. Cillari E., Liew F. Y., Lelchuk R. Suppression of interleukin-2 production by macrophages in genetically susceptible mice infected with Leishmania major. Infect Immun. 1986 Nov;54(2):386–394. doi: 10.1128/iai.54.2.386-394.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corsini A. C., Clayton C., Askonas B. A., Ogilvie B. M. Suppressor cells and loss of B-cell potential in mice infected with Trypanosoma brucei. Clin Exp Immunol. 1977 Jul;29(1):122–131. [PMC free article] [PubMed] [Google Scholar]
  5. Dwinger R. H., Murray M., Moloo S. K. Potential value of localized skin reactions (chancres) induced by Trypanosoma congolense transmitted by Glossina morsitans centralis for the analysis of metacyclic trypanosome populations. Parasite Immunol. 1987 May;9(3):353–362. doi: 10.1111/j.1365-3024.1987.tb00513.x. [DOI] [PubMed] [Google Scholar]
  6. Eardley D. D., Jayawardena A. N. Suppressor cells in mice infected with Trypanosoma brucei. J Immunol. 1977 Sep;119(3):1029–1033. [PubMed] [Google Scholar]
  7. Ellis J. A., Davis W. C., MacHugh N. D., Emery D. L., Kaushal A., Morrison W. I. Differentiation antigens on bovine mononuclear phagocytes identified by monoclonal antibodies. Vet Immunol Immunopathol. 1988 Oct;19(3-4):325–340. doi: 10.1016/0165-2427(88)90118-3. [DOI] [PubMed] [Google Scholar]
  8. Fumoux F., Queval R., Traore-Leroux T. Stimulation in vitro des lymphocytes périphériques des bovines de l'Ouest africain par les lectines: intérêt dans la trypanosomose. Rev Elev Med Vet Pays Trop. 1984;37(Spec No):236–247. [PubMed] [Google Scholar]
  9. Gasbarre L. C., Hug K., Louis J. Murine T lymphocyte specificity for African trypanosomes. II. Suppression of the T lymphocyte proliferative response to Trypanosoma brucei by systemic trypanosome infection. Clin Exp Immunol. 1981 Jul;45(1):165–172. [PMC free article] [PubMed] [Google Scholar]
  10. Geigy R., Kauffmann M. Sleeping sickness survey in the Serengeti area (Tanzania) 1971. I. Examination of large mammals for trypanosomes. Acta Trop. 1973;30(1):12–23. [PubMed] [Google Scholar]
  11. Greenwood B. M. Possible role of a B-cell mitogen in hypergammaglobulinaemia in malaria and trypanosomiasis. Lancet. 1974 Mar 16;1(7855):435–436. doi: 10.1016/s0140-6736(74)92386-1. [DOI] [PubMed] [Google Scholar]
  12. Jayawardena A. N., Waksman B. H., Eardley D. D. Activation of distinct helper and suppressor T cells in experimental trypanosomiasis. J Immunol. 1978 Aug;121(2):622–628. [PubMed] [Google Scholar]
  13. Kemp S. J., Spooner R. L., Teale A. J. A comparative study of major histocompatibility complex antigens in east African and European cattle breeds. Anim Genet. 1988;19(1):17–29. doi: 10.1111/j.1365-2052.1988.tb00784.x. [DOI] [PubMed] [Google Scholar]
  14. Masake R. A., Pearson T. W., Wells P., Roelants G. E. The in vitro response to mitogens of leucocytes from cattle infected with Trypanosoma congolense. Clin Exp Immunol. 1981 Mar;43(3):583–589. [PMC free article] [PubMed] [Google Scholar]
  15. Metzger Z., Hoffeld J. T., Oppenheim J. J. Macrophage-mediated suppression. I. Evidence for participation of both hdyrogen peroxide and prostaglandins in suppression of murine lymphocyte proliferation. J Immunol. 1980 Feb;124(2):983–988. [PubMed] [Google Scholar]
  16. Musoke A. J., Nantulya V. M., Barbet A. F., Kironde F., McGuire T. C. Bovine immune response to African ;trypanosomes: specific antibodies to variable surface glycoproteins of Trypanosoma brucei. Parasite Immunol. 1981 Summer;3(2):97–106. doi: 10.1111/j.1365-3024.1981.tb00388.x. [DOI] [PubMed] [Google Scholar]
  17. Nantulya V. M., Musoke A. J., Rurangirwa F. R., Barbet A. F., Ngaira J. M., Katende J. M. Immune depression in African trypanosomiasis: the role of antigenic competition. Clin Exp Immunol. 1982 Feb;47(2):234–242. [PMC free article] [PubMed] [Google Scholar]
  18. Nantulya V. M., Musoke A. J., Rurangirwa F. R., Moloo S. K. Resistance of cattle to tsetse-transmitted challenge with Trypanosoma brucei or Trypanosoma congolense after spontaneous recovery from syringe-passaged infections. Infect Immun. 1984 Feb;43(2):735–738. doi: 10.1128/iai.43.2.735-738.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pearson T. W., Roelants G. E., Lundin L. B., Mayor-Withey K. S. Immune depression in trypanosome-infected mice. I. Depressed T lymphocyte responses. Eur J Immunol. 1978 Oct;8(10):723–727. doi: 10.1002/eji.1830081010. [DOI] [PubMed] [Google Scholar]
  20. Pearson T. W., Roelants G. E., Pinder M., Lundin L. B., Mayor-Withey K. S. Immune depression in trypanosome-infected mice. III. suppressor cells. Eur J Immunol. 1979 Mar;9(3):200–204. doi: 10.1002/eji.1830090306. [DOI] [PubMed] [Google Scholar]
  21. Roelants G. E., Pearson T. W., Morrison W. I., Mayor-Withey K. S., Lundin L. B. Immune depression in trypanosome-infected mice. IV. Kinetics of suppression and alleviation by the trypanocidal drug Berenil. Clin Exp Immunol. 1979 Sep;37(3):457–469. [PMC free article] [PubMed] [Google Scholar]
  22. Rurangirwa F. R., Tabel H., Losos G. J., Tizard I. R. Suppression of antibody response to Leptospira biflexa and Brucella abortus and recovery from immunosuppression after Berenil treatment. Infect Immun. 1979 Dec;26(3):822–826. doi: 10.1128/iai.26.3.822-826.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rurangirwa F. R., Tabel H., Losos G., Masiga W. N., Mwambu P. Immunosuppressive effect of Trypanosoma congolense and Trypanosoma vivax on the secondary immune response of cattle to Mycoplasma mycoides subsp mycoides. Res Vet Sci. 1978 Nov;25(3):395–397. [PubMed] [Google Scholar]
  24. 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 May;19(5):829–835. doi: 10.1002/eji.1830190508. [DOI] [PubMed] [Google Scholar]
  25. 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 Jan;19(1):119–124. doi: 10.1002/eji.1830190119. [DOI] [PubMed] [Google Scholar]
  26. Sollod A. E., Frank G. H. Bovine trypanosomiasis: effect on the immune response of the infected host. Am J Vet Res. 1979 May;40(5):658–664. [PubMed] [Google Scholar]
  27. Tarleton R. L. Trypanosoma cruzi-induced suppression of IL-2 production. II. Evidence for a role for suppressor cells. J Immunol. 1988 Apr 15;140(8):2769–2773. [PubMed] [Google Scholar]
  28. Wellhausen S. R., Mansfield J. M. Lymphocyte function in experimental African trypanosomiasis. II. Splenic suppressor cell activity. J Immunol. 1979 Mar;122(3):818–824. [PubMed] [Google Scholar]

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