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T Cell and cytokine basis of host variability in response to intestinal nematode infections

Published online by Cambridge University Press:  06 April 2009

R. K. Grencis
R. K. Grencis
Affiliation:
School of Biological Sciences, Stopford Building, University of Manchester, Oxford Road, Manchester M13 9PT, UK
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Summary

Infection by a variety of species of intestinal nematode infection gives rise to a wide variation in parasite load within a host population. There has been much investigation into the basis of this variation and is thought to involve several factors. Studies of infections of gut dwelling nematodes in laboratory rodents has clearly demonstrated that this variation may be due to the production of cytokines produced as part of the host immune response to infection. More specifically, activation of distinct T helper cell subsets leads to the generation of effective or ineffective responses resulting in clearance of the parasite load or maintenance of chronic infection. The induction of differential responses remains to be determined but is likely to be influenced at a number of levels including involvement of accessory cells and activation of co-stimulatory molecules on antigen presenting cells. Moreover, it appears that these parasites may actively interfere with the host cytokine response to promote their own survival. This review concentrates on recent findings of cytokine mediated control of intestinal nematodes highlighting a central role for the immune system in regulating both acute and chronic infection by these parasites.

Keywords

Cytokinesimmunityimmune evasionintestinal nematodesT helper cells.
Type
Research Article
Information
Parasitology , Volume 112 , Supplement S1: Symposia of the British Society for Parasitology Volume 33:Genetics of host and parasite: implications for immunity, epidemiology and evolution , March 1996 , pp. S31 - S37
Copyright
Copyright © Cambridge University Press 1996

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References

Alcami, A. & Smith, G. L. (1995). Cytokine receptors encoded by poxvirus: a lesson in cytokine biology. Immunology Today 16, 474–8.CrossRefGoogle ScholarPubMed
Bancroft, A. J., Else, K. J. & Grencis, R. K. (1994). Low level infection of Trichuris muris significantly affects the polarisation of the CD4 response. European Journal of Immunology 24, 3113–18.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Wakelin, D. (1978). The Survival of Trichuris muris in wild mouse populations of its natural host. Parasitology 67, 157–64.CrossRefGoogle Scholar
Bellaby, T., Robinson, K. J. & Wakelin, D. (1996). Induction of differential T helper responses in mice infected with the parasitic nematode Trichuris muris. Infection and Immunity. In Press.CrossRefGoogle ScholarPubMed
Borish, L., Mascali, J. J., Klinnert, M., Leppert, M. & Rosenwasser, L. j. (1994). SSC polymorphisms in interleukin genes. Human Molecular Genetics 3, 1710.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. (1995). Epidemiology and transmission of intestinal helminths. In Enteric Infection 2. Intestinal Helminths (ed. Farthing, M. J. C., Keusch, G. T. & Wakelin, D.), pp. 5–24. London: Chapman & Hall.Google Scholar
Bundy, D. A. P., Thompson, D. E., Golden, M. H. N., Cooper, E. S., Anderson, R. M. & Harland, P. S. E. (1985). Population distribution of Trichuris trichiura in a community of Jamaican children. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 232–7.CrossRefGoogle Scholar
Croll, N. A., Anderson, R. M., Gyorkos, T. W. & Ghadirian, E. (1982). The population biology and control of Ascaris lumbricoides in a rural community in Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 187–97.CrossRefGoogle Scholar
Doherty, P. C., Allan, W., Eichelberger, M. & Carding, s. R. (1992). Roles of αβ and γδT cell subsets in viral immunity. Annual Review of Immunology 10, 123–51.CrossRefGoogle Scholar
Else, K. J., Entwistle, G. M. & Grencis, R. K. (1993). Correlations between worm burden and markers of Thl and Th2 cell subset induction in an inbred strain of mouse infected with Trichuris muris. Parasite Immunology 10, 595–600.CrossRefGoogle Scholar
Else, K. J.Finkelman, F. D., Maliszewski, C. R. & Grencis, R. K. (1994). Cytokine mediated regulation of chronic intestinal helminth infection. Journal of Experimental Medicine 179, 347–51.CrossRefGoogle ScholarPubMed
Else, K. j. & Grencis, R. K. (1991). Cellular immune responses to the nematode parasite Trichuris muris. I. Differential cytokine production during acute or chronic infection. Immunology 72, 508–13.Google ScholarPubMed
Else, K. J., Hültner, L. & Grencis, R. K. (1992). Cellular immune responses to the murine nematode parasite Trichuris muris. II. Differential induction of Th cell subsets in resistant versus susceptible mice. Immunology 75, 232–7.Google Scholar
Else, K. j. & Wakelin, D. (1988). The effects of H-2 and non-H-2 genes on the expulsion of the nematode Trichuris muris from inbred and congenic strains of mouse. Parasitology, 96, 543–50CrossRefGoogle Scholar
Else, K. J., Wakelin, D. & Roach, T. I. A. (1989). Host predisposition to trichuriasis: the mouse– T. muris model. Parasitology 98, 275–82.CrossRefGoogle ScholarPubMed
Else, K. J., Wakelin, D., Wassom, D.L. & Hauda, K. M. (1990). The influence of genes mapping within the major histocompatibility complex on resistance to Trichuris muris infections in mice. Parasitology 96, 543–8.CrossRefGoogle Scholar
Ferrick, D. A., Schrenzel, M. D., Mulvania, T., Hsieh, B., Ferlin, w. G. & Lepper, H. (1995). Differential production of interferon y and interleukin4 in response to Thl and Th2 stimulating pathogens by γδ T cells in vivo. Nature. 373, 255–7.CrossRefGoogle Scholar
Finkelman, F. D., Holmes, J., Katona, I. M., Urban, J. F. Jr., Beckman, L. S., Park, K. A., Schooley, R. L., Coffman, R. L., Mosmann, T. R. & Paul, W. E. (1990). Lymphokine control of in vivo immunoglobulin isotype selection. Annual Review of Immunology 8, 303–34.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Madden, K. B., Cheever, A. W., Katona, I. M., Morris, S. C., Gately, M. K., Hubbard, B. R., Cause, W. C. & Urban, J. F. Jr. (1994). Effects of IL-12 on immune responses and host protection in mice infected with intestinal nematode parasites. Journal of Experimental Medicine 179, 1563–8.CrossRefGoogle ScholarPubMed
Fitch, F. W., Mcklsic, D. W., Lancki, D. W. & Gajewski, T. F. (1993). Differential regulation of murine T lymphocyte subsets. Annual Review of Immunology 11, 29–48.CrossRefGoogle ScholarPubMed
Gajewski, T. F., Pinnas, M., Wong, T. & Fitch, F. W. (1991). Murine Th1 and Th2 clones proliferate optimally in response to distinct antigen presenting cell populations. Journal of Immunology 146, 1750–8.CrossRefGoogle ScholarPubMed
Grencis, R. K., Hültner, L. & Else, K. J. (1991). Host protective immunity to Trichinella spiralis in mice: activation of Th cell subsets and lymphokine secretion in mice expressing different response phenotypes. Immunology 74, 329–32.Google ScholarPubMed
Grencis, R. K., Reidlinger, J. & Wakelin, D. (1985). L3T4 positive lymphoblasts are responsible for transfer of immunity to Trichinella spiralis in mice. Immunology 56, 213–18.Google ScholarPubMed
Haas, W., Pereira, P. & Tonegawa, S. (1993). Gamma/delta cells. Annual Review of Immunology 11, 637–86.CrossRefGoogle ScholarPubMed
Haswell-Elkins, M. R., Elkins, D. B., Manjula, K., Michael, E. & Anderson, R. M. (1987). The distribution and abundance of Enterobius vermicularis in a South Indian fishing community. Parasitology 95, 339–52.CrossRefGoogle Scholar
Katona, I. M., Urban, J. F. Jr. & Finkelman, F. D. (1988). The role of L3T4+ and Ly2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. Journal of Immunology 140, 3206–11.CrossRefGoogle Scholar
Koyama, K., Tamanchi, H. & Ito, Y. (1995). The role of CD4+ and CD8+ T cells in protective immunity to the murine parasite Trichuris muris. Parasite Immunology 17, 161–5.CrossRefGoogle Scholar
Kuchroo, V. K., Prabhu, Das M., Brown, J. A., Ranger, A. M., Zamvil, S. S., Sobel, R. A., Weiner, H. L., Nabavi, N. & Glimcher, L. H. (1995). B7–1 and B7–2 costimulatory molecules activate differentially the Thl/Th2 developmental pathways: application to autoimmune disease therapy. Cell 80, 707–18.CrossRefGoogle Scholar
Lee, T. D. G. & Wakelin, D. (1982). The use of host strain variation to assess the significance of mucosal mast cells in the spontaneous cure response of mice to the nematode Trichuris muris. International Archives of Allergy and Applied Immunology 67, 302–7.CrossRefGoogle Scholar
Linsley, P. S. & Ledbetter, J. A. (1993). The role of CD28 receptor during T cell response to antigen. Annual Review of Immunology 11, 191–212.CrossRefGoogle Scholar
Lu, P., Di Hou, X., Chen, S. J., Moorman, M., Morris, S. C., Finkelman, F. D., Linsley, P., Urban, J. F. & Cause, w. c. (1994). CTLA-4 ligands are required to induce an in vivo interleukin 4 response to a gastrointestinal nematode parasite. Journal of Experimental Medicine 180, 693–8.CrossRefGoogle Scholar
Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F. & Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–805.CrossRefGoogle ScholarPubMed
Mosmann, T. R. & Coffman, R. L. (1989). Thl and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145–73.CrossRefGoogle Scholar
Pritchard, D. I., Quinnell, R. J. & Walsh, E. A. (1995). Immunity of Necator americanus: IgE, parasite weight and fecundity. Parasite Immunology 17, 71–75.CrossRefGoogle ScholarPubMed
Schad, G. A. & Anderson, R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 1537–40.CrossRefGoogle ScholarPubMed
Schild, H., Mavaddat, N., Litzenberger, C., Ehrich, E. W., Davies, M. M., Bluestone, J. A., Matis, L., Draper, R. K. & Chien, Y. (1994). The nature of major histocompatibility complex recognition by γδ T cells. Cell 76, 29–37.CrossRefGoogle Scholar
Seder, R. A. & Paul, w. E. (1994). Acquisition of lymphokine-producing phenotype by CD4+T cells. Annual Review of Immunology 12, 635–74.CrossRefGoogle ScholarPubMed
Simpson, R. J. & Renauld, J. C. (1994). Interleukin 9. In Guidebook to Cytokines and Their Receptors (ed. Nicola, N. A.), pp. 79–81. Oxford: Oxford University Press.Google Scholar
Stockinger, B., Zal, T., Zal, A. & Gray, D. (1996). B cells solicit their own help from T cells. Journal of Experimental Medicine. In Press.CrossRefGoogle ScholarPubMed
Urban, J. F. Jr., Katona, I. M. & Finkelman, F. D. (1991). Heligmosomoides polygyrus: CD4+ cells but not CD8+ T cells regulate the IgE response and protective immunity in mice. Experimental Parasitology 73, 500–6.CrossRefGoogle Scholar
Urban, J. F. Jr., Katona, I. M., Paul, W. E. & Finkelman, F. D. (1992). Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proceedings of the National Academy of Sciences, USA 88, 513–18.Google Scholar
Urban, J. F. Jr., Maliszewski, C. R., Madden, K. B., Katona, I. M. & Finkelman, F. D. (1995). IL-4 treatment can cure established gastrointestinal nematode infection in immunocompetent and immunodeficient mice. Journal of Immunology 154, 4675–80.CrossRefGoogle ScholarPubMed
Wahid, F. N. & Behnke, j. M. (1993). Immunological relationships during primary infection with Heligmosomoides polygyrus. Regulation of fast response phenotype by H-2 and non-H-2 genes. Parasitology 107, 343–50.CrossRefGoogle ScholarPubMed
Wakelin, D. (1988). Helminth infections. In Genetics of Resistance to Bacterial and Parasitic Infection (ed. Blackwell, J. M. & Wakelin, D.), pp. 153–225. London: Taylor & Francis.Google Scholar
Wassom, D. L., Wakelin, D., Brooks, B. O., Krco, C. J. & David, c. s. (1984). Genetic control to infection with Trichinella spiralis infections of mice. Hypothesis to explain the role of H-2 genes in primary and challenge infections. Immunology 51, 625–31.Google ScholarPubMed