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In vivo regulation of S. japonica granuloma formation by an IL-2 antagonist

Published online by Cambridge University Press:  06 April 2009

T. F. Kresina
Affiliation:
Department of Medicine, Program of Geographic Medicine, Miriam Hospital and Brown University International Health Institute, Providence, Rhode Island 02906, USA

Summary

The present study shows an in vivo role for interleukin-2 in the formation of hepatic granulomatous inflammation in murine Schistosoma japonicum infection. Mice which had been administered an inhibitor to interleukin-2 function during acute infection were noted to have reduced cell-mediated immune responses to ConA and S. japonicum soluble egg antigen (SEA). Lymphoid tissue from these treated mice also have reduced numbers of cells which could be activated by ConA to produce interleukin-2 mRNA as shown by in situ hybridization studies. Mice with less activated lymphocytes had, on the average, a 70% reduction in the granulomatous inflammation surrounding eggs deposited in hepatic tissues of acutely infected mice. The data demonstrate that IL-2 is a key factor in the generation of granulomatous inflammation in S. japonicum infection and suggest that a potential anti-pathology vaccine could be generated based on limiting the presence of IL-2 generated during acute infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

REFERENCES

Abe, T. & Colley, D. G. (1984). Modulation of Schistosoma mansoni egg-induced granuloma formation III. Evidence for an anti-idiotypic I-J positive, I-J restricted soluble T suppressor factor. Journal of Immunology 132, 2084–9.CrossRefGoogle ScholarPubMed
Boros, D. L. & Warren, K. S. (1970). Delayed hyper-sensitivity type granuloma formation and dermal reactions induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. Journal of Experimental Medicine 132, 488507.CrossRefGoogle Scholar
Boros, D. & Ragheb, S. (1989). Phenotypic and functional characterization of granuloma T cells for S. mansoni infected mice. Journal of Immunology 142, 3239–46.Google Scholar
Cheever, A. W., Byron, J. E. & Von Lichtenberg, F. (1985). Immunopathology of Schistosoma japonicum infection in athymic mice. Parasite Immunology 7, 387–98.CrossRefGoogle ScholarPubMed
Cheever, A. W., Deb, S. & Duvall, R. H. (1989). Granuloma formation in Schistosoma japonicum-infected nude mice: the effects of recognition with L3T4+ on Lyt2+ splenic cells. American Journal of Tropical Medicine and Hygiene 40, 6671.CrossRefGoogle Scholar
Chensue, S. W., Boros, D. L. & David, C. S. (1983). Regulation of granulomatous inflammation in murine schistosomiasis II. T-suppressor cell-derived I-C subregion-encoded soluble suppressor factor mediates regulation of lymphokine production. Journal of Experimental Medicine 57, 219–26.CrossRefGoogle Scholar
Coffman, R. L., Seymour, B. W. P., Hudak, S., Jackson, J. & Rennick, D. (1989). Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science 245, 308–10.CrossRefGoogle ScholarPubMed
El Meneza, S., Olds, G. R., Kresina, T. F. & Mahmoud, A. A. F. (1989). Dynamics of hepatic connective tissue matrix constituents during murine S. mansoni infection. Hepatology 9, 50–6.CrossRefGoogle Scholar
Fernandez-BOTRAN, R., Sanders, V. M., Mosmann, T. R., Uhr, J. W. & Vitetta, E. S. (1988). Lymphokine-mediated regulation of the proliferative responses of clones Th1 and Th2 cells. Journal of Experimental Medicine 168, 543–58.CrossRefGoogle Scholar
Garb, K. S., Stavitsky, A. B. & Mahmoud, A. A. F. (1981). Dynamics of antigen and mitogen induced responses in murine schistosomiasis japonica: in vitro comparison between hepatic granulomas and splenic cells. Journal of Immunology 128, 1391–3.Google Scholar
Kasaian, M. T. & Biron, C. A. (1989). The activation of IL-2 transcription in L3T4 and Ly 2+ Lymphocytes during virus infection in vivo. Journal of Immunology 142, 1287–93.CrossRefGoogle ScholarPubMed
Kresina, T. F. (1988 a). Antigen-specific down regulation of murine collagen induced arthritis: T suppressor cell circuits in arthritis immunotherapy. International Review of Immunology 4, 91106.CrossRefGoogle ScholarPubMed
Kresina, T. F. (1988 b). Down regulation of collagen-induced arthritis by a suppressor inducer T cell hybridoma. Experimental Cell Biology 56, 86102.Google Scholar
Kresina, T. F. (1990). A contra-IL-2 cytokine derived from mice suppressed for collagen induced arthritis. Cellular Immunology 125, 171–82.CrossRefGoogle ScholarPubMed
Lammie, P. J., Phillips, S. M., Linette, G. P., Michael, A. I. & Bentley, A. G. (1986). In vitro granuloma formation using defined antigenic nidi. Annals of the New York Academy of Science 465, 340–6.CrossRefGoogle ScholarPubMed
Lawrence, J. B. & Singer, R. H. (1985). Quantitative analysis of in situ hybridization methods for the detection of actin gene expression. Nucleic Acids Research 13: 1777–82.CrossRefGoogle ScholarPubMed
Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951). Protein measurement with the folin phenol agent. Journal of Biological Chemistry 193, 154–65.CrossRefGoogle Scholar
Mathew, R. C. & Boros, D. L. (1986). Anti-L3T4 antibody treatment suppresses hepatic granuloma formation and abrogates antigen induced interleukin-2 production in Schistosoma mansoni infection. Infection and Immunity 54, 820–6.CrossRefGoogle ScholarPubMed
Mosmann, T. R., Cherwinski, H., Bond, M. W., Gredlin, M. A. & Coffman, R. L. (1986). Two types of murine helper T cell clone 1 definition according to profiles of lymphokine activities and secreted protein. Journal of Immunology 136, 2348–57.CrossRefGoogle Scholar
Olds, G. E., El Meneza, S., Mahmoud, A. A. F. & Kresina, T. F. (1989). Differential immunoregulation of granulomatous inflammation, portal hypertension and hepatic fibrosis in murine Schistosomiasis mansoni. Journal of Immunology 142, 3605–11.CrossRefGoogle ScholarPubMed
Olds, G. R., Finegan, C. & Kresina, T. F. (1986). Glycosaminoglycan analysis in murine Schistosoma japonicum infection. Gastroenterology 91, 1335–42.CrossRefGoogle ScholarPubMed
Olds, G. R., Griffin, A. & Kresina, T. F. (1985). Dynamics of collagen accumulation and polymorphism in murine Schistosoma japonicum. Gastroenterology 89, 617–24.CrossRefGoogle ScholarPubMed
Olds, G. R. & Kresina, T. F. (1985). Network interactions in Schistosoma japonicum infection. Journal of Clinical Investigation 76, 2338–47.CrossRefGoogle ScholarPubMed
Olds, G. R., Olveda, R. R., Travy, J. W. & Mahmoud, A. A. F. (1982). Adoptive transfer of modulation of granuloma formation and hepatosplenic disease in murine schistosomiasis japonica by serum from chronically infected mice. Journal of Immunology 128, 1391–83.CrossRefGoogle Scholar
Olds, G. R. & Stavitsky, A. B. (1986). Mechanics of in vivo modulation of granulomatous inflammation in murine schistosomiasis japonicum. Infection and Immunity 52, 513–18.CrossRefGoogle Scholar
Perrin, P. J. & Phillips, S. M. (1988). The molecular basis of granuloma formation in schistosomiasis I. A T cell derived suppressor effector factor. Journal of Immunology 141, 1714–19.CrossRefGoogle Scholar
Phillips, S. M. & Lammie, P. J. (1986). Immunopathology of granuloma formation and fibrosis in schistosomiasis. Parasitology Today 2, 296300.CrossRefGoogle ScholarPubMed
Secor, E. W., Stewart, S. J. & Colley, D. G. (1990). Eosinophils and immune mechanisms VI. The synergistic combination of granulocyte macrophage colony stimulating factor and IL-5 accounts for eosinophil stimulation proto activity in Schistosoma mansoni-infected mice. Journal of Immunology 144, 1484–9.CrossRefGoogle Scholar
Sher, A., Coffman, R. L., Hieny, S., Scott, P. & Cheever, A. W. (1990). Interleukin 5 is required for the blood and tissue eosinophilia but not granuloma formation induced by infection with Schistosoma mansoni. Proceedings of the National Academy of Sciences, USA 87, 61–5.CrossRefGoogle Scholar
Spannaus-MARTIN, D. J., Holmdahl, R. & Kresina, T. F. (1990). Immunotherapy of collagen induced arthritis by a T cell anti-proliferative molecule. American Journal of Pathology 137, 331–40.Google Scholar
Stavitsky, A. B. (1987). Immune regulation in schistosomiasis japonica. Immunology Today 8, 228–33.CrossRefGoogle ScholarPubMed
Stavitsky, A. B. & Harold, W. W. (1988). Deficiency of interleukin-2 activity upon addition of soluble egg antigen to cultures of spleen cells from mice infected with Schistosoma japonicum. Infection and Immunity 56, 1778–84.CrossRefGoogle ScholarPubMed
Stavitsky, A. B. & Harold, W. W. (1989). Deficiency of interleukin-2 production upon addition of soluble egg antigen to cultures of isolated hepatic granulomas as hepatic granuloma cells from mice infected with Schistosoma japonicum. Infection and Immunity 57, 2339–44.CrossRefGoogle ScholarPubMed
Stavitsky, A. B., Olds, G. R. & Peterson, K. B. (1985). Regulation of egg antigen-induced in vitro proliferation response by splenic suppressor T cells in murine Schistosoma japonicum infection. Infection and Immunity 49, 635–40.CrossRefGoogle ScholarPubMed
Warren, K. S. (1982). The secret of the immunopathogenesis of schistosomiasis: in vivo models. Immunology Review 61, 189213.CrossRefGoogle ScholarPubMed