Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T10:41:46.612Z Has data issue: false hasContentIssue false

Dissociation of early and late protective immunity to the nematode Nippostrongylus brasiliensis in Brown Norway and Fischer-344 rats

Published online by Cambridge University Press:  06 April 2009

R. Uchikawa
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
M. Yamada
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
S. Matsuda
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
T. Tegoshi
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
M. Nishida
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
I. Kamata
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
A. Kuroda
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan
N. Arizono
Affiliation:
Department of Medical Zoology, Kyoto Prefectural University of Medicine, Kyoto 602, Japan

Summary

Worm expulsion of, and IgE and interferon (IFN)-γ responses to, Nippostrongylus brasiliensis were studied in 2 rat strains, Brown Norway (BN) and Fischer (F)-344. BN rats expelled the majority of worms by day 14 post-infection (p.i.) with approximately 6% of worms surviving for at least 3 weeks. In F-344 rats, worm expulsion was delayed by 2 days relative to that in BN, while the numbers of residual worms were significantly fewer than in BN, suggesting that different immune mechanisms are involved in early and late phases of immunity. Total serum IgE, as well as in vitro IgE production by mesenteric lymph node (MLN) cells, was increased 2 weeks p.i., the levels being markedly higher in BN than in F-344 rats. Serum rat mast cell protease II was also increased more significantly in BN than in F-344 rats. In contrast, production of IgG2a and IFN-γ by MLN and spleen cells was found to be higher in F-344 than in BN rats. These results indicate that the early worm expulsion is correlated with the host IgE and mast cell responsiveness, whereas the persistence of infection in the late period may be controlled by different immune mechanisms.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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

REFERENCES

Arizono, N., Kasugai, T., Yamada, M., Okada, M., Morimoto, M., Tei, H., Newlands, G. F. J., Miller, H. R. p. & Kitamura, Y. (1993). Infection of Nippostrongylus brasiliensis induces development of mucosal-type but not connective tissue-type mast cells in genetically mast cell-deficient Ws/Ws rats. Blood 81, 2572–8.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., 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
Finkelman, F. D., Katona, I. M., Mosmann, T. R. & Coffman, R. L. (1988 a). IFN-γ regulates the isotypes of Ig secreted during in vivo humoral immune responses. Journal of Immunology 140, 1022–7.CrossRefGoogle ScholarPubMed
Finkelman, F. D., Katona, I. M., Urban, J. F. Jr., Holmes, J., Ohara, J., Tung, A. S., Sample, J. V. G. & Paul, W. E. (1988 b). IL-4 is required to generate and sustain in vivo IgE responses. Journal of Immunology 141, 2335–41.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 interleukin 12 on immune responses and host protection in mice infected with intestinal nematode parasites. Journal of Experimental Medicine 179, 1563–72.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
Haley, A. J. & Parker, J. C. (1961). Effect of population density on adult worm survival in primary Nippostrongylus brasiliensis infections in the rat. Proceedings of the Helminthological Society of Washington 28, 176–80.Google Scholar
Ishikawa, N., Horii, Y. & Nawa, Y. (1993). Immune-mediated alteration of the terminal sugars of goblet cell mucins in the small intestine of Nippostrongylus brasiliensis-infected rats. Immunology 78, 303–7.Google ScholarPubMed
Jarrett, E. E. E., Jarrett, W. F. H. & Urquhart, G. M. (1968). Quantitative studies on the kinetics of establishment and expulsion of intestinal nematode populations in susceptible and immune hosts. Nippostrongylus brasiliensis in the rat. Parasitology 58, 625–39.CrossRefGoogle ScholarPubMed
King, S. J. & Miller, H. R. P. (1984). Anaphylactic release of mucosal mast cell protease and its relationship to gut permeability in Nippostrongylus-primed rats. Immunology 51, 653–60.Google ScholarPubMed
Locksley, R. M. (1994). Th2 cells: help for helminths. Journal of Experimental Medicine 179, 1405–7.CrossRefGoogle ScholarPubMed
Matsuda, S., Uchikawa, R., Yamada, M. & Arizono, N. (1995). Cytokine mRNA expression profiles in rats infected with Nippostrongylus brasiliensis. Infection and Immunity 63 (in the Press).CrossRefGoogle ScholarPubMed
Miller, H. R. P. & Jarrett, W. F. H. (1971). Immune reaction in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20, 277–88.Google ScholarPubMed
Mosmann, T. R. & Coffman, R. L. (1989). Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology 7, 145–73.CrossRefGoogle ScholarPubMed
Murphey, S. M., Brown, S., Miklos, N. & Fireman, P. (1974). Reagin synthesis in inbred strains of rats. Immunology 27, 245–53.Google ScholarPubMed
Ogilvie, B. M. & Jones, V. E. (1971). Nippostrongylus brasiliensis: a review of immunity and the host/parasite relationship in the rat. Experimental Parasitology 29, 138–77.CrossRefGoogle ScholarPubMed
Perdue, M. H., Ramage, J. K., Burget, D., Marshall, J. & Masson, s. (1989). Intestinal mucosal injury is associated with mast cell activation and leukotriene generation during Nippostrongylus-induced inflammation in the rat. Digestive Diseases and Sciences 34, 724–31.CrossRefGoogle ScholarPubMed
Pond, L., Wassom, D. L. & Hayes, C. E. (1989). Evidence for differential induction of helper T cell subsets during Trichinella spiralis infection. Journal of Immunology 143, 4232–7.CrossRefGoogle ScholarPubMed
Pond, L., Wassom, D. L. & Hayes, C. E. (1992). Influence of resistant and susceptible genotype, IL-1, and lymphoid organ on Trichinella spiralis-induced cytokine secretion. Journal of Immunology 149, 957–65.CrossRefGoogle ScholarPubMed
Snapper, C. M. & Paul, W. E. (1987). Interferon-γ and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236, 944–7.CrossRefGoogle Scholar
Uchikawa, R., Yamada, M., Matsuda, S. & Arizono, N. (1993). IgE antibody responses induced by transplantation of the nematode Nippostrongylus brasiliensis in rats: a possible role of nematode excretory-secretory product in IgE production. Immunology 80, 541–5.Google ScholarPubMed
Uchikawa, R., Yamada, M., Matsuda, S., Kuroda, A. & Arizono, N. (1994). IgE antibody production is associated with suppressed interferon-γ levels in mesenteric lymph nodes of rats infected with the nematode Nippostrongylus brasiliensis. Immunology 82, 427–32.Google ScholarPubMed
Urban, J. F. Jr., Katona, I. M., Paul, W. E. & Finkelman, F. D. (1991). Interleukin 4 is important in protective immunity to a gastrointestinal nematode infection in mice. Proceedings of the National Academy of Sciences, USA 88, 5513–17.CrossRefGoogle ScholarPubMed
Urquhart, G. M., Mulligan, W., Eadie, R. M. & Jennings, F. w. (1965). Immunological studies on Nippostrongylus brasiliensis infection in the rat: the role of local anaphylaxis. Experimental Parasitology 17, 210–17.CrossRefGoogle ScholarPubMed
Wakelin, D. (1993). Allergic inflammation as a hypothesis for the expulsion of worms from tissue. Parasitology Today 9, 115–16.CrossRefGoogle Scholar
Woodbury, R. G., Miller, H. R. P., Huntley, J. F., Newlands, G. F. J., Palliser, A. C. & Wakelin, D. (1984). Mucosal mast cells are functionally active during spontaneous expulsion of intestinal nematode infection in rat. Nature, London 312, 450–2.CrossRefGoogle ScholarPubMed
Yamada, M., Nakazawa, M. & Arizono, N. (1993). IgE and IgG2a antibody responses are induced by different antigen groups of the nematode Nippostrongylus brasiliensis in rats. Immunology 78, 298302.Google ScholarPubMed
Yamada, M., Uchikawa, R., Nakazawa, M., Oda, M. & Arizono, N. (1993). Dissociation of specific and total IgE antibody responses following repeated low-level infections with Nippostrongylus brasiliensis in rats. Clinical and Experimental Immunology 93, 80–4.CrossRefGoogle ScholarPubMed