Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-25T10:10:01.943Z Has data issue: false hasContentIssue false

Polyclonal activation of B lymphocytes during experimental infection with Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

L. M. Lopes
Affiliation:
Department of Biochemistry and Immunology, Instituto de Ciências Biolódgicas, Universidade Federal de Minas Gerais, 31270 Belo Horizonte, MG, Brasil
M. A. C. Pereira
Affiliation:
Department of Biochemistry and Immunology, Instituto de Ciências Biolódgicas, Universidade Federal de Minas Gerais, 31270 Belo Horizonte, MG, Brasil
S. E. Gerken
Affiliation:
Department of Biochemistry and Immunology, Instituto de Ciências Biolódgicas, Universidade Federal de Minas Gerais, 31270 Belo Horizonte, MG, Brasil
N. Vaz
Affiliation:
Department of Biochemistry and Immunology, Instituto de Ciências Biolódgicas, Universidade Federal de Minas Gerais, 31270 Belo Horizonte, MG, Brasil

Summary

A significant polyclonal activation of B lymphocytes was observed during experimental infection of C57BL/10J mice with Schistosoma mansoni. The isotypic pattern of this expansion, assessed by the Protein-A plaque-forming cell method, was compared with and found to differ from those occurring after infection by Trypanosoma cruzi or injection of bacterial LPS. In the infection of S. mansoni an early expansion of most immunoglobulin isotypes occurs together with a late, sustained expansion of IgG1-secreting cells. High levels of polyclonal B cell activation were observed after adoptive transfer of spleen cells from infected mice to isogenic recipients pre-treated with hydroxyurea.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, J., Coutinho, A., Lernhardt, W. & Melchers, F. (1977). Clonal growth and maturation to immunoglobulin secretion in vitro of every growth-inducible B-lymphocyte. Cell 10, 2731.CrossRefGoogle Scholar
Bernabe, R. R., Tuneskog, M., Forni, L., Martinez, C-A., Holmberg, D., Ivars, F. & Coutinho, A. (1981). The protein A plaque assay for the detection of immunoglobulin-secreting cells. In Immunological Methods, vol. 3, pp. 187198. New York: Academic Press.Google Scholar
Biozzi, G., Mouton, D., Sant'anna, O. A., Passos, H. C., Gennari, M., Reis, M. H., Ferreira, V. C. A., Heuman, A. M., Bouthillier, Y., Ibanez, O. M., Stiffel, C. & Siqueira, M. (1979). Genetics of immunoresponsiveness to natural antigens in the mouse. Current Topics in Microbiology and Immunology 85, 3198.Google ScholarPubMed
Björklund, M. & Couthino, A. (1983). Isotype commitment in the in vivo immune responses. II Polyclonal PFC responses to LPS in the spleen and bone marrow. European Journal of Immunology 13, 4450.Google Scholar
Björklund, M., Forni, L. & Coutinho, A. (1987). T cell-dependent modulation of the polyclonal B-lymphocyte responses in normal spleen cell cultures stimulated by lipopolysaccharide. Annales d'Immunologie 138C, 181–99.Google Scholar
Bout, D., Rousseau, R., Carlier, Y. & Capron, A. (1980). Kinetics of classes and subclasses of total immunoglobulins and specific antibodies to Schistosoma mansoni during murine infection. Parasitology 80, 247–56.Google Scholar
Buus, S., Sette, A. & Grey, H. (1987). The interaction between protein-derived immunogenic peptides and Ia. Immunological Reviews 98, 115–41.CrossRefGoogle ScholarPubMed
Colley, D. G. (1981). Immune responses and immunoregulation in experimental and clinical schistosomiasis. In Diseases, vol. 1, (ed. Mansfield, J. M.) pp. 252. New York: Marcel Dekker.Google Scholar
Coutinho, A., Forni, L., Holmberg, D., Ivars, F. & Vaz, N. (1984). From an antigen-centred clonal perspective of immune responses to an organism-centred network perspective of autonomous activity in a self-determined immune system. Immunological Reviews 79, 151–68.Google Scholar
Coutinho, A. & Möller, G. (1974). Immune activation of B cells: evidence for one non-specific triggering signal not delivered by Ig receptors. Scandinavian Journal of Immunology 3, 133–9.CrossRefGoogle Scholar
Crandall, C. A. & Crandall, R. B. (1971). Ascaris suum: Immunoglobulin response in mice. Experimental Parasitology 30, 426–37.Google Scholar
Crandall, R. B. & Crandall, C. A. (1972). Trichinella spiralis: Immunologic response to infection in mice. Experimental Parasitology 31, 378–98.Google Scholar
Cumano, A., Vieira, P., Colle, J. H., Truffa-Bachi, P. & Freitas, A. (1986). Effects of hydroxyurea in vivo treatment on the antibody response in mice. Annales d'Immunologie 137D, 355–67.Google Scholar
Cunningham, D. S., Kuhn, E. E., Tarleton, R. L. & Dunn, R. S. (1981). Trypanosoma cruzi: effect on B cell responsiveness and responding clones. Experimental Parasitology 51, 257–62.Google Scholar
Curtain, C. G. & Kidson, C. (1964). Malaria antibody content of gamma-2 7S globulin in tropical populations. Nature, London 203, 1366–7.Google Scholar
D'Imperio-Lima, M. R., Joskowicz, M., Coutinho, A., Kipnis, T. & Eisen, H. (1985). Very large and isotypically atypical polyclonal plaque-forming cell responses in mice infected with Trypanosoma cruzi. European Journal of Immunology 15, 201–3.CrossRefGoogle ScholarPubMed
Fisher, E., Camus, D., Santoro, F. & Capron, A. (1981). Schistosoma mansoni auto-antibodies and polyclonal B cell activation in infected mice. Clinical and Experimental Immunology 46, 8994.Google Scholar
Freitas, A. A., Rocha, B. & Coutinho, A. (1986). Lymphocyte population dynamics in the mouse. Immunological Reviews 91, 512.Google Scholar
Gazzinelli, R., Morato, M. F. J., Nunes, R. M. B., Cançado, J. R. & Gazzinelli, G. (1987). Imunoregulação idiotípica em doença de Chagas. Proceedings of II Reunião Anual FESBE, Rio de Janeiro (Abstract in Portuguese), p. 456.Google Scholar
Goldberg, S. S., Cordeiro, M. N., Silva Pereira, A. A. & Mares-Guia, M. L. (1983). Release of lipopolysaccharide (LPS) from cell surface of T. cruzi by EDTA. International Journal for Parasitology 13, 1116.CrossRefGoogle Scholar
Greenwood, B. M. (1974). Possible role of a B cell mitogen in hypergammaglobulinemia in malaria and trypanosomiais. Lancet 1, 435–6.Google Scholar
Greenwood, B. M. & Vick, R. M. (1985). Evidence for malaria mitogen in human malaria. Nature, London 257, 582–5.Google Scholar
Hang, L. M., Boros, D. L. & Warren, K. S. (1974). Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. Journal of Infectious Diseases 130, 515–22.CrossRefGoogle ScholarPubMed
Holmberg, D., Forsgren, S., Ivars, F. & Coutinho, A. (1985). Reactions among IgM antibodies derived from normal neonatal mice. European Journal of Immunology 14, 435–9.Google Scholar
Jarrett, E. (1973). Elevation of total serum IgE in rats following helminth parasite infection. Nature, London 251, 613–14.Google Scholar
Jarrett, E. & Fergusson, A. (1974). Effect of T Cell depletion on the potentiated reagin response. Nature, London 259, 450–4.Google Scholar
Jerne, N. K. (1974). Towards a network theory of the immune system. Annales d'Immunologie 124C, 373–89.Google Scholar
Kearney, J. F. & Lawton, A. R. (1975). B lymphocyte differentiation induced by lipopolysaccharide. I. Generation of cells synthesizing four major immunoglobulin classes. Journal of Immunology 115, 671–6.CrossRefGoogle ScholarPubMed
Kincade, P. W. & Phillips, R. A. (1985). B lymphocyte development. Federation Proceedings 44, 2874–81.Google Scholar
Kohler, H., Urbain, J. & Cazzenave, P.-A. (1984). Idiotypy in Biology and Medicine, London New York: Academic Press.Google Scholar
Lanzavechia, A. (1985). Antigen-specific interaction between T and B cells. Nature, London 314, 537–9.Google Scholar
Levy, M., Vieira, P., Coutinho, A. & Freitas, A. (1987). The májority of ‘natural’ immunoglobulin-secreting cells are short-lived and the progeny of cycling lymphocytes. European Journal of Immunology 17, 849–54.CrossRefGoogle ScholarPubMed
Lewert, R. M. & Mandelowitz, S. (1969). Schistosomiasis: prenatal induction of tolerance to antigens. Nature, London 224, 1029–30.CrossRefGoogle ScholarPubMed
Lima, M. S., Gazzinelli, G., Nascimento, E., Parra, J. C., Montesano, M. A. & Colley, D. G. (1986). Immune responses during human schistosomiasis mansoni. Evidence for anti-idiotypic T lymphocyte responsiveness. Journal of Clinical Investigation 78, 983–8.CrossRefGoogle Scholar
Martinez, C.-A. & Coutinho, A. (1982). Immunoglobulin C-gene expression. III. Possible induction of specific genetic events in activated B lymphocytes by the polyclonal stimuli driving clonal expansion. European Journal of Immunology 12, 502–6.CrossRefGoogle Scholar
Martinez, C.-A., Bernabe, R. R., Pereira, P., Cazenave, P.-A. & Coutinho, A. (1985). Establishment of idiotypic helper T cell repertoires early in life. Nature, London 317, 721–4.Google Scholar
Martinez, C.-A., Coutinho, A. & Augustin, A. A. (1980). Immunoglobulin C-gene expression. I. The commitment to IgG subclass of secretory cells is determined by the quality of the nonspecific stimuli. European Journal of Immunology 10, 698702.CrossRefGoogle Scholar
Martinez, C.-A., Pereira, P., Bernabe, R., Bandeira, A., Larsson, E.-L., Cazenave, P.-A. & Coutinho, A. (1984). Internal complementarities in the immune system. Regulation of the expression of T-cell idiotypes. Proceedings of the National Academy of Sciences, USA 81, 4520–3.Google Scholar
Melchers, F. & Anderson, J. (1986). Factors controlling the B cell cycle. Annual Review of Immunology 41, 1317.Google Scholar
Möller, G. (1972). Immunocyte triggering. Cellular Immunology 1, 573–82.Google Scholar
Montesano, A., Lima, M. S., Correa-Oliveira, R., Gazzinelli, G. & Colley, D. G. (1989). Idiotypic differences in clinical forms of schistosomiasis (in the Press).Google Scholar
Olds, G. R. & Kresina, T. F. (1985). Network interactions in Schistosoma japonicum infection. Identification and characterization of a serologically distinct immunoregulatory auto-anti-idiotypic-antibody population. Journal of Clinical Investigation 76, 2338–47.Google Scholar
Ortiz-Ortiz, L, Parks, D. E., Rodrigues, M. & Weigle, W. O. (1980). Polyclonal B lymphocyte activation during Trypanosoma cruzi infection. Journal of Immunology 124, 121–6.CrossRefGoogle ScholarPubMed
Oyeyinka, G. O. (1986). Malaria mitogens or super antigens? Nature, London 319, 543–4.CrossRefGoogle ScholarPubMed
Pereira, P., Larsson, E.-L., Forni, L., Bandeira, A. & Coutinho, A. (1985). Natural effector T lymphocytes in normal mice. Proceedings of the National Academy of Sciences, USA 82, 7691–5.Google Scholar
Phillips, S. M., Fox, E. G., Fathelbar, N. G. & Walker, D. (1986). Epitopic and paratopically directed anti-idiotypic factors in the regulation of resistance to murine schistosomiasis mansoni. Journal of Immunology 137, 2339–47.Google Scholar
Powell, M. R. & Colley, D. G. (1985). Demonstration of splenic auto-anti-idiotypic plaque-forming cells in mice infected with Schistosoma mansoni. Journal of Immunology 134, 4140–5.Google Scholar
Rios, M. J. C., Pereira, M. A. C., Lopes, L. M., Faria, A. M. C., Gontijo, C. M., Castanheira, E. B. & Vaz, N. M. (1988). Tolerance induction and immunological priming initiated by mucosal contacts with protein antigens in inbred strains of mice. Brazilian Journal of Medical and Biological Research 21, 825–36.Google Scholar
Rosemberg, Y. I. (1978). Autoimmune and polyclonal B cell responses during murine malaria. Nature, London 274, 170–2.Google Scholar
Sher, A., McIntyre, S. & Von Lichtenberg, F. (1977). Schistosoma mansoni: kinetics and class specificity of hypergammaglobulinemia induced during murine infection. Experimental Parasitology 41, 415–22.Google Scholar
Tite, J. P., Kaye, J., Saizama, K. N., Ming, J., Katz, M. E., Smith, L. & Janeway, C. A. (1986). Direct interactions between B and T lymphocytes bearing complementary receptors. Journal of Experimental Medicine 163, 189202.Google Scholar
Tonggawa, S. (1985). The molecules of the immune system. Scientific American 253, 104–13.Google Scholar
Vakil, M., Sauter, H., Paige, C. & Kearney, J. F. (1986). In vivo suppression of perinatal multispecific B cells results in a distortion of the adult repertoire. European Journal of Immunology 16, 1159–66.CrossRefGoogle Scholar
Vaz, N. M. (1988). Towards cognitive immunology: G.O.D. is infinite. In Immunosemiotics: Semiotics of Intercellular Communication in the Immune System (ed. Sercarz, E., Mitchison, A., Celada, F. & Tada, T.) pp. 193198. Berlin: Springer Verlag.Google Scholar
Vaz, N. M. & Faria, A. M. C. (1988). Imunologia: aspectos cognitivos. Ciência e Cultura 401, 981–6.Google Scholar