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Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 linked genes determine worm survival

Published online by Cambridge University Press:  06 April 2009

J. M. Behnke
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
F. N. Wahid
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD

Extract

The course of primary infection was studied in BALB and B10 H-2 congenic mouse strains. The duration of infection, as assessed with regular faecal egg counts and worm burdens, was shorter in mice carrying the H-2s, H-2d or H-2q haplotypes when compared to mice with H-2b. Strains with H-2k were intermediate. An experiment was carried out to test the hypothesis proposed by Wassom, Krco & David (1987) predicting that the progeny of I–E+ve mouse strains crossed with I–E-ve strains, would show susceptibility rather than resistance to infection. This hypothesis was not substantiated by our data and we conclude that it does not apply to primary infections with Heligmosomoides polygyrus. It is proposed that the gene products of at least two loci within the H-2 (associated with the H-2b and H-2k haplotypes) are crucial in determining the response phenotype of mice to primary infection with H. polygyrus. One allele, (associated with the H-2b haplotype) may be preferentially affected by parasite-mediated immunosuppression.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1991

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References

Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 171.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Barnard, C. J. (1990). Coevolution of parasites and hosts: host–parasite arms races and their consequences. In Parasites: Immunity and Pathology (ed. Behnke, J. M.), pp. 1–22. London: Taylor and Francis.CrossRefGoogle Scholar
Behnke, J. M., Hannah, J. & Pritchard, D. I. (1983). Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397408.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Parish, H. A. (1979). Nematospiroides dubius: arrested development of larvae in immune mice. Experimental Parasitology 47, 116–27.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Robinson, M. (1985). Genetic control of immunity to Nematospiroides dubius: a 9-day anthelmintic abbreviated immunizing regime which separates weak and strong responder strains of mice. Parasite Immunology 7, 235–53.CrossRefGoogle ScholarPubMed
Crawford, C., Behnke, J. M. & Pritchard, D. I. (1989). Suppression of heterologous immunity by Nematospiroides dubius antigens in vitro. International Journal for Parasitology 19, 2934.CrossRefGoogle ScholarPubMed
Cypess, R. H., Lucia, H. L., Zidian, J. L. & Rivera-Ortiz, C. I. (1977). Heligmosomoides polygyrus: temporal, spatial and morphological population characteristics in LAF/J mice. Experimental Parasitology 42, 3443.CrossRefGoogle Scholar
Dobson, C. & Cayzer, C. J. R. (1982). Immunosuppressive activity in serum from mice infected with Nematospiroides dubius following passive transfer. International Journal for Parasitology 12, 561–6.CrossRefGoogle Scholar
Else, K. & 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 mice. Parasitology 96, 543–50.CrossRefGoogle ScholarPubMed
Enriquez, F. J., Brooks, B. O., Cypess, R. H., David, C. S. & Wassom, D. L. (1988 b). Nematospiroides dubius: two H-2-linked genes influence levels of resistance to infection in mice. Experimental Parasitology 67, 221–6.CrossRefGoogle ScholarPubMed
Enriquez, F. J., Zidian, J. L. & Cypess, R. H. (1988 a). Nematospiroides dubius: genetic control of immunity to infections in mice. Experimental Parasitology 67, 1219.CrossRefGoogle Scholar
Fleischer, B. (1989). Bacterial toxins as probes for the T-cell antigen receptor. Immunology Today 10, 262–4.CrossRefGoogle ScholarPubMed
Jenkins, S. N. & Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 71–8.CrossRefGoogle ScholarPubMed
Kappler, J. W., Roehm, N. & Marrack, P. (1987). T cell tolerance by clonal elimination in the thymus. Cell 49, 273–80.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Hiorns, R. W. (1986). Heligmosomoides polygyrus (Nematoda): the dynamics of primary and repeated infections in outbred mice. Proceedings of the Royal Society, B 229, 4767.Google ScholarPubMed
Klesius, P. H. (1988). Immunity to Ostertagia ostertagi. Veterinary Parasitology 27, 159–67.CrossRefGoogle ScholarPubMed
Marrack, P. & Kappler, J. (1987). The T cell receptor. Science 238, 1070–9.CrossRefGoogle ScholarPubMed
Monroy, F. G., Dobson, C. & Adams, J. H. (1989). Low molecular weight immunosuppressors secreted by adult Nematospiroides dubius. International Journal for Parasitology 19, 125–7.CrossRefGoogle ScholarPubMed
Pritchard, D. I. (1986). Antigens of gastrointestinal nematodes. Transactions of the Royal Society for Tropical Medicine and Hygiene 80, 728–34.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Ali, N. M. H. & Behnke, J. M. (1984). Analysis of the mechanism of immunodepression following heterologous antigenic stimulation during concurrent infection with Nematospiroides dubius. Immunology 51, 633–42.Google ScholarPubMed
Robinson, M., Wahid, F. N., Behnke, J. M. & Gilbert, F. S. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98, 115–24.CrossRefGoogle ScholarPubMed
Sokal, R. R. & Rohlf, F. J. (1969). Biometry. San Francisco: Freeman.Google Scholar
Wadee, A. A., Vickery, A. C. & Piessens, W. F. (1987). Characterization of immunosuppressive proteins of Brugia malayi microfilariae. Acta Tropica 44, 343–52.Google ScholarPubMed
Wahid, F. N., Robinson, M. & Behnke, J. M. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): expulsion of adult worms from fast responder syngeneic and hybrid strains of mice. Parasitology 98, 459–69.CrossRefGoogle ScholarPubMed
Wakelin, D. (1980). Genetic control of immunity to parasites. Infection with Trichinella spiralis in inbred and congenic mice showing rapid and slow responses to infection. Parasite Immunology 2, 8598.CrossRefGoogle Scholar
Wassom, D. L., Brooks, B. O., Babish, G. J. & David, C. S. (1983 b). A gene mapping between the S and D regions of the H-2 complex influences resistance to Trichinella spiralis infections in mice. Journal of Immunogenetics 10, 371–8.CrossRefGoogle Scholar
Wassom, D. L., Brooks, O. B., Cypess, R. H. & David, C. S. (1983 a). A survey of susceptibility to infection with Trichinella spiralis of inbred mouse strains sharing common H-2 alleles but different genetic backgrounds. Journal of Parasitology 69, 1033–7.CrossRefGoogle ScholarPubMed
Wassom, D. L. & Kelly, E. A. B. (1990). The role of the major histocompatibility complex in resistance to parasite infections. Critical Reviews in Immunology 10, 3152.Google ScholarPubMed
Wassom, D. L., Krco, C. J. & David, C. S. (1987). I–E expression and susceptibility to parasitic infection. Immunology Today 8, 3943.CrossRefGoogle Scholar
Wassom, D. L., Wakelin, D., Brooks, B. O., Krco, C. J. & David, C. S. (1984). Genetic control of immunity to 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