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Chasing the genes that control resistance to gastrointestinal nematodes

Published online by Cambridge University Press:  12 April 2024

J.M. Behnke ,
F. Iraqi ,
D. Menge ,
R.L. Baker ,
J. Gibson  and
D. Wakelin
J.M. Behnke*
Affiliation:
School of Life and Environmental Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK.
F. Iraqi
Affiliation:
International Livestock Research Institute, PO Box 30709, Nairobi, Kenya.
D. Menge
Affiliation:
International Livestock Research Institute, PO Box 30709, Nairobi, Kenya.
R.L. Baker
Affiliation:
International Livestock Research Institute, PO Box 30709, Nairobi, Kenya.
J. Gibson
Affiliation:
International Livestock Research Institute, PO Box 30709, Nairobi, Kenya.
D. Wakelin
Affiliation:
International Livestock Research Institute, PO Box 30709, Nairobi, Kenya.
*
* Fax: (0) 115 951 3251, E-mail: [email protected].
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Abstract

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The host-protective immune response to infection with gastrointestinal (GI) nematodes involves a range of interacting processes that begin with recognition of the parasite's antigens and culminate in an inflammatory reaction in the intestinal mucosa. Precisely which immune effectors are responsible for the loss of specific worms is still not known although many candidate effectors have been proposed. However, it is now clear that many different genes regulate the response and that differences between hosts (fast or strong versus slow or weak responses) can be explained by allelic variation in crucial genes associated with the gene cascade that accompanies the immune response and/or genes encoding constitutively expressed receptor/signalling molecules. Major histocompatibility complex (MHC) genes have been recognized for some time as decisive in controlling immunity, and evidence that non-MHC genes are equally, if not more important in this respect has also been available for two decades. Nevertheless, whilst the former have been mapped in mice, only two candidate loci have been proposed for non-MHC genes and relatively little is known about their roles. Now, with the availability of microsatellite markers, it is possible to exploit linkage mapping techniques to identify quantitative trait loci (QTL) responsible for resistance to GI nematodes. Four QTL for resistance to Heligmosomoides polygyrus, and additional QTL affecting faecal egg production by the worms and the accompanying immune responses, have been identified. Fine mapping and eventually the identification of the genes (and their alleles) underlying QTL for resistance/susceptibility will permit informed searches for homologues in domestic animals, and human beings, through comparative genomic maps. This information in turn will facilitate targeted breeding to improve resistance in domestic animals and, in human beings, focused application of treatment and control strategies for GI nematodes.

Type
Research Article
Information
Journal of Helminthology , Volume 77 , Issue 2 , June 2003 , pp. 99 - 109
Copyright
Copyright © Cambridge University Press 2003

References

Abe, T., Sugaya, H., Yoshimura, K. & Nawa, Y. (1992) Induction of the expulsion of Strongyloides ratti and retention of Nippostrongylus brasiliensis in athymic nude mice by repetitive administration of recombinant interleukin-3. Immunology 76, 10–14.Google ScholarPubMed
Ackert, J.E., Eisenbrandt, L.L., Glading, B. & Wilmoth, J.H. (1933) On the comparative resistance of six breeds of chickens to the nematode Ascaridia lineata (Schneider). Journal of Parasitology 20, 127.Google Scholar
Albers, G.A.A. & Gray, G.D. (1987) Breeding for worm resistance: a perspective. International Journal for Parasitology 17, 559–566.CrossRefGoogle ScholarPubMed
Allcock, R.J.N., Martin, A.M. & Price, P. (2000) The mouse as a model for the effects of MHC genes on human disease. Immunology Today 21, 328–334.CrossRefGoogle Scholar
Artis, D. & Grencis, R.K. (2001) T helper cytokine responses during intestinal nematode infection: induction, regulation and effector function. pp. 311–371 in Kennedy, M.W. & Harnett, W. (Eds) Parasitic nematodes: molecular biology, biochemistry and immunology. Wallingford, Oxon, CAB International.Google Scholar
Artis, D., Humphreys, N.E., Bancroft, A.J., Rothwell, N.J., Potten, C.S. & Grencis, R.K. (1999) Tumor necrosis factor a is a critical component of interleukin 13-mediated protective T helper cell Type 2 responses during helminth infection. Journal of Experimental Medicine 190, 953–962.CrossRefGoogle ScholarPubMed
Baker, R.L. (1998) A review of genetic resistance to gastrointestinal nematode parasites in sheep and goats in the tropics and evidence for resistance in some sheep and goat breeds in sub-humid coastal Kenya. Animal Genetics Resources Information Bulletin 24, 13–30.CrossRefGoogle Scholar
Baker, R.L., Lahlou Kassi, A., Rege, J.E.O., Reynolds, L., Bekele, T., Mukassa-Mugerwa, E. & Rey, B. (1992) A review of genetic resistance to endoparasites in small ruminants and an outline of ILCA's research programme in this area. Proceedings of the tenth scientific workshop of the small ruminant collaborative research support program, Nairobi 10, 97–104.Google Scholar
Baker, R.L., Mwamachi, D.M., Audho, J.O., Aduda, E.O. & Thorpe, W. (1999) Genetic resistance to gastro-intestinal nematode parasites in Red Maasai, Dorper and Maasai × Dorper ewes in the sub-humid tropics. Animal Science 69, 335–344.CrossRefGoogle Scholar
Baker, R.L., Nagda, S., Rodriguez-Zas, S.L., Southey, B.R., Audho, J.O., Aduda, E.O. & Thorpe, W. (2003) Resistance and resilience to gastro-intestinal nematode parasites and productivity of Red Maasai, Dorper and Red Maasai × Dorper crossbred lambs in the sub-humid tropics. Animal Science 76, 111–136.CrossRefGoogle Scholar
Bancroft, A.J., McKenzie, A.N.J. & Grencis, R.K. (1998) A critical role for IL-13 in resistance to intestinal nematode infection. Journal of Immunology 160, 3453–3461.CrossRefGoogle ScholarPubMed
Behnke, J.M. (1987) Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 1–70.CrossRefGoogle ScholarPubMed
Behnke, J.M., Lowe, A., Menge, D., Iraqi, F. & Wakelin, D. (2000) Mapping the genes for resistance to gastrointestinal nematodes. Acta Parasitologica 45, 1–13.Google Scholar
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, 235–253.CrossRefGoogle ScholarPubMed
Behnke, J.M. & Wahid, F.N. (1991) Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): H-2 genes determine worm survival. Parasitology 103, 157–164.CrossRefGoogle ScholarPubMed
Behnke, J.M. & Wakelin, D. (1977) Nematospiroides dubius: stimulation of acquired immunity in inbred strains of mice. Journal of Helminthology 51, 167–176.CrossRefGoogle ScholarPubMed
Behnke, J.M., Barnard, C.J. & Wakelin, D. (1992) Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.CrossRefGoogle ScholarPubMed
Bell, R.G. (1988) Genetic analysis of expulsion of adult Trichinella spiralis in NFS, C3H/He and B10.BR mice. Experimental Parasitology 74, 417–465.CrossRefGoogle Scholar
Bell, R.G. (1998) The generation and expression of immunity to Trichinella spiralis in laboratory rodents. Advances in Parasitology 41, 149–217.CrossRefGoogle ScholarPubMed
Betts, C.J. & Else, K.J. (1999) Mast cells, eosinophila and antibody-mediated cellular cytotoxicity are not critical in resistance to Trichuris muris . Parasite Immunology 21, 45–52.CrossRefGoogle Scholar
Brailsford, T.J. & Behnke, J.M. (1992) The dynamics of trickle infections with Heligmosomoides polygyrus in syngeneic strains of mice. International Journal for Parasitology 22, 351–359.CrossRefGoogle ScholarPubMed
Brindley, P.J. & Dobson, C. (1982) Nematospiroides dubius in mice selected for liability to infection: modification of parasite biology through host selection. International Journal for Parasitology 12, 573–578.CrossRefGoogle Scholar
Buitkamp, J., Filmether, P., Stear, M.J. & Epplen, J.T. (1996) Class I and class II major histocompatibility complex alleles are associated with faecal egg counts following natural, predominantly Ostertagia circumcincta infection. Parasitology Research 82, 693–696.CrossRefGoogle Scholar
Coles, G.C. (1998) Drug-resistant parasites of sheep: an emerging problem in Britain? Parasitology Today 14, 86–88.CrossRefGoogle Scholar
Coltman, D.W., Wilson, K., Pilkington, J.G., Stear, M.J. & Pemberton, J.M. (2001) A microsatellite polymorphism in a gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep. Parasitology 122, 571–582.CrossRefGoogle Scholar
Cooke, G.S. & Hill, A.V.S. (2000) Genetics of susceptibility to human infectious disease. Nature Reviews in Genetics 2, 967–977.CrossRefGoogle Scholar
Courtney, C.H., Parker, C.F., McClure, K.E. & Herd, R.P. (1985) Resistance of exotic and domestic lambs to experimental infection with Haemonchus contortus . International Journal for Parasitology 15, 101–109.CrossRefGoogle ScholarPubMed
Crawford, A.M. (2001) A review of QTL experiments in sheep. Proceedings of the Association for the Advancement of Animal Breedings and Genetics 14, 33–38.Google Scholar
Crawford, A.M. & McEwen, J.C. (1998) Identification of animals resistant to nematode parasite infection. New Zealand Provisional Patent (330201), New Zealand.Google Scholar
De Clercq, D., Sacko, M., Behnke, J., Gilbert, F., Dorny, P. & Vercruysse, J. (1997) Failure of mebendazole in treatment of human hookworm infections in the Southern Region of Mali. American Journal of Tropical Medicine and Hygiene 57, 25–30.CrossRefGoogle ScholarPubMed
Dietrich, W.F., Miller, J., Steen, R., Merchant, M.A., Damron-Boles, D., Husain, Z., Dredge, R., Daly, M.J., Ingalls, K.A., O'Connor, T.J., Evans, C.A., De Angelis, M.M., Levinson, D.M., Kruglyak, L., Goodman, N., Copeland, N.G., Jenkins, N.A., Hawkins, T.L., Stein, L., Page, D.C. & Lander, E.S. (1996) A comprehensive genetic map of the mouse genome. Nature 380, 149–152.CrossRefGoogle ScholarPubMed
Durette-Desset, M.C. (1985) Trichostrongylid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24, 239–306.CrossRefGoogle Scholar
Else, K.J. & deSchoolmeester, M.L. (2003) Immunity to Trichuris muris in the laboratory mouse. Journal of Helminthology 77.CrossRefGoogle ScholarPubMed
Else, K.J. & Finkelman, F.D. (1999) Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle 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 mice. Parasitology 96, 543–550.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 101, 61–67.CrossRefGoogle ScholarPubMed
Enriquez, F.J., Zidian, J.L. & Cypess, R.H. (1988a) Nematospiroides dubius: genetic control of immunity to infections of mice. Experimental Parasitology 67, 12–19.CrossRefGoogle ScholarPubMed
Enriquez, F.J., Brooks, B.O., Cypess, R.H., David, C.S. & Wassom, D.L. (1988b) Nematospiroides dubius: two H-2-linked genes influence levels of resistance to infection in mice. Experimental Parasitology> 67, 221–226.CrossRefGoogle ScholarPubMed
Finkelman, F.D., Pearce, E.J., Urban, J.F. & Sher, A. (1991) Regulation and biological function of helminth-induced cytokine responses. Immunology Today 12, A62–A66.CrossRefGoogle ScholarPubMed
Gasbarre, L.C. & Miller, J.E. (2000) Genetics of helminth resistance. pp. 129–152 in Axford, R.F.E., Bishop, S.C., Nicholas, F.W. & Owen, U.B. (Eds) Breeding for disease resistance in farm animals. 2nd edn, Wallingford, Oxon, CAB International.Google Scholar
Gray, G.D. (1987) Genetic resistance to haemonchosis in sheep. Parasitology Today 8, 253–255.CrossRefGoogle Scholar
Gray, G.D., Woolaston, R.R. & Eaton, B.T. (1995) Breeding for resistance to infectious diseases of small ruminants. Australian Centre for International Agricultural Research (ACIAR), Monograph No. 34. Canberra, Australia.Google Scholar
Greenwald, R.J., Urban, J.F., Ekkens, M.J., Chen, S.J., Nguyen, D., Fang, H., Finkelman, F.D., Sharpe, A.H. & Gause, W.C. (1999) B7-2 is required for the progression but not the initiation of the Type 2 response to a gastrointestinal nematode parasite. Journal of Immunology 162, 4133–4139.CrossRefGoogle Scholar
Iraqi, F. (2000) Fine mapping of quantitative trait loci using advanced intercross lines of mice and positional cloning of the corresponding genes. Journal of Experimental Lung Research 26, 641–649.CrossRefGoogle ScholarPubMed
Iraqi, F.A., Behnke, J.M., Menge, D.M., Lowe, A., Teale, A.J., Gibson, J.P., Baker, L.R. & Wakelin, D. (2003) Chromosomal regions controlling resistance to gastrointestinal nematode infections in mice. Mammalian Genome in press.Google ScholarPubMed
Iraqi, F., Clapcott, S.J., Kumari, P., Haley, C.J., Kemp, S.J. & Teale, A.J. (2000) Fine mapping of trypanosomiasis resistance loci in murine advanced intercross lines. Mammalian Genome 11, 645–648.CrossRefGoogle ScholarPubMed
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, 303–307.Google ScholarPubMed
Jackson, F. & Coop, R.L. (2000) The development of anthelmintic resistance in sheep nematodes. Parasitology 120, S95–S107.CrossRefGoogle ScholarPubMed
Jacobson, R.H. & Reed, N.D. (1974) The immune response of congenitally athymic (nude) mice to the intestinal nematode Nippostrongylus brasiliensis . Proceedings of the Society for Experimental Biology and Medicine 147, 667–670.CrossRefGoogle Scholar
Janeway, C.A. Jr., Travers, P., Hunt, S. & Walport, M. (1997) Immunobiology. The immune system in health and disease. Edinburgh, Churchill Livingstone.Google Scholar
Kemp, S.J. & Teale, A.J. (1998) Genetic basis of trypanotolerance in cattle and mice. Parasitology Today 14, 450–454.CrossRefGoogle ScholarPubMed
Kemp, S., Iraqi, F., Darvasi, A., Soller, M. & Teale, A.J. (1997) Localization of genes controlling resistance to trypanosomiasis in mice. Nature Genetics 16, 194–196.CrossRefGoogle ScholarPubMed
Kloosterman, A., Parmentier, H.K. & Ploeger, H.W. (1992) Breeding cattle and sheep for resistance to gastrointestinal nematodes. Parasitology Today 8, 330–335.CrossRefGoogle ScholarPubMed
Korstanje, R. & Paigen, B. (2002) From QTL to gene: the harvest begins. Nature Genetics 31, 235–236.CrossRefGoogle ScholarPubMed
Lawrence, R.A., Gray, C.A., Osborne, J. & Maizels, R.M. (1996) Nippostrongylus brasiliensis: cytokine responses and nematode expulsion in normal and IL-4 deficient mice. Experimental Parasitology 84, 65–73.CrossRefGoogle ScholarPubMed
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, 302–305.CrossRefGoogle Scholar
McDermott, J.R., Grencis, R.K. & Else, K.J. (2001) Leucocyte recruitment during enteric nematode infection. Immunology 103, 505–510.CrossRefGoogle ScholarPubMed
Meeusen, E.N.T. & Balic, A. (2000) Do eosinophils have a role in the killing of helminth parasites?. Parasitology Today 16, 95–101.CrossRefGoogle ScholarPubMed
Menge, D.M., Behnke, J.M., Iraqi, F., Lowe, A., Teale, A.J., Gibson, J.P., Wakelin, D. & Baker, R.L. (2002) Quantitative trait loci for resistance to gastro-intestinal nematode infections in mice. Proceedings of the 7th World Congress on Genetics Applied to Livestock Production 31, 707–710.Google Scholar
Miller, H.R.P. (1971) Immune reactions in mucous membranes II. The differentiation of intestinal mast cells during helminth expulsion in the rat. Laboratory Investigation 24, 339–347.Google ScholarPubMed
Monroy, F.G. & Enriquez, F.J. (1992) Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 49–54.CrossRefGoogle Scholar
Nawa, Y. & Miller, H.R.P. (1979) Adoptive transfer of the intestinal mast cell responses in rats infected with Nippostrongylus brasiliensis . Cellular Immunology 42, 225–239.CrossRefGoogle ScholarPubMed
Nawa, Y., Ishikawa, N., Tsuchiya, K., Hori, Y., Abe, T., Khan, A.I., Bing-Shi, , Itohi, T., Ide, H. & Uchiyama, F. (1994) Selective effector mechanisms for the expulsion of intestinal helminths. Parasite Immunology 16, 333–338.CrossRefGoogle ScholarPubMed
Nehls, M., Pfeifer, D., Schorpp, M., Hedrich, H. & Boehm, T. (1994) New member of the winged-helix protein family disrupted in mouse and rat nude mutations. Nature 372, 103–107.CrossRefGoogle ScholarPubMed
Okomo, M.A., Mugambi, J.M., Aduda, E.O., Hanotte, O., van Arendonk, J.A.M. & Baker, R.L. (2000) Mapping quantitative trait loci controlling resistance to gastro-intestinal nematode parasites in Red Maasai sheep. p.25 in Proceedings of the 27th International Conference on Animal Genetics, 22–26 July, University of Minnesota, USA. Conference Abstract Book.Google Scholar
Outteridge, P.M., Windon, R.G. & Dineen, J.K. (1985) An association between a lymphocyte antigen in sheep and the response to vaccination against the parasite Trichostrongylus colubriformis . International Journal for Parasitology 15, 121–127.CrossRefGoogle ScholarPubMed
Outteridge, P.M., Windon, R.G. & Dineen, J.K. (1988) An ovine lymphocyte antigen marker for acquired resistance to Trichostrongylus colubriformis . International Journal for Parasitology 18, 853–858.CrossRefGoogle ScholarPubMed
Paterson, K.A., McEwan, J.C., Dodds, K.G. & Crawford, A.M. (2001) Fine mapping a locus affecting host resistance to internal parasites of sheep. Proceedings of the Association for the Advancement of Animal Breeding and Genetics 14, 91–94.Google Scholar
Paterson, S., Wilson, K. & Pemberton, J.M. (1998) Major histocompatibility complex variation associated with juvenile survival and parasite resistance in a large unmanaged ungulate population (Ovis aries L.). Proceedings of the National Academy of Sciences, USA 95, 3714–3719.CrossRefGoogle Scholar
Preston, J.M. & Allonby, E.W. (1979) The influence of breed on the susceptibility of sheep to Haemonchus contortus infection in Kenya. Research in Veterinary Science 26, 134–139.CrossRefGoogle ScholarPubMed
Reynoldson, J.A., Behnke, J.M., Pallant, L.J., MacNish, M.G., Gilbert, F. & Thompson, R.A.C. (1997) Failure of pyrantel in treatment of human hookworm infections (Ancylostoma duodenale) in the Kimberley region of north west Australia. Acta Tropica 68, 301–312.CrossRefGoogle 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, 115–124.CrossRefGoogle ScholarPubMed
Schopf, L.R., Hoffman, K.F., Cheever, A.W., Urban, J.F. Jr & Wynn, T.A. (2002) IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. Journal of Immunology 168, 2383–2392.CrossRefGoogle ScholarPubMed
Schwaiger, F.W., Gostomski, D., Stear, M., Duncan, J.L., McKellar, Q.A., Epplen, J.T. & Buitkamp, J. (1995) An ovine major histocompatibility complex DRB1 allele is associated with low faecal egg count following natural, predominantly Ostertagia circumcincta infection. International Journal for Parasitology 25, 815–822.CrossRefGoogle ScholarPubMed
Stear, M.J. & Wakelin, D. (1998) Genetic resistance to parasitic infection. Revue Scientifique et Technique Office International des Epizooties 17, 143–153.CrossRefGoogle ScholarPubMed
Stear, M.J., Tierney, T.J., Baldock, F.C., Brown, S.C., Nicholas, F.W. & Rudder, T.H. (1988) Class I antigens of the bovine major histocompatibility system are weakly associated with variation in faecal worm egg counts in naturally infected cattle. Animal Genetics 19, 115–122.CrossRefGoogle ScholarPubMed
Stear, M.J., Bairden, K., Bishop, S.C., Buitkamp, J., Epplen, J.T., Gostomski, D., McKellar, Q.A., Schwaiger, F.W. & Wallace, D.S. (1996) An ovine lymphocyte antigen is associated with reduced faecal egg counts in four-month-old lambs following natural predominantly Ostertagia circumcincta infection. International Journal for Parasitology 26, 423–428.CrossRefGoogle ScholarPubMed
Stewart, M.A., Miller, R.F. & Douglas, J.R. (1937) Resistance of sheep of different breeds to infestations by Ostertagia circumcincta . Journal of Agricultural Research 55, 923–930.Google Scholar
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, 5513–5517.CrossRefGoogle ScholarPubMed
Urban, J.F. Jr., Noben-Trauth, N., Donaldson, D.D., Maddens, K.B., Morris, S.C., Collins, M. & Finkelman, F.D. (1998) IL-13, IL-4Ra, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis . Immunity 8, 255–264.CrossRefGoogle Scholar
Urban, J.F. Jr, Schopf, L., Morris, S.C., Orekhova, T., Madden, K.B., Betts, C.J., Gamble, H.R., Byrd, C., Donaldson, D., Else, K. & Finkelman, F.D. (2000) Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. Journal of Immunology 164, 2046–2052.CrossRefGoogle 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, 459–469.CrossRefGoogle ScholarPubMed
Wahid, F.N., Behnke, J.M., Grencis, R.K., Else, K.J. & Ben-Smith, A.W. (1994) Immunological relationships during primary infection with Heligmosomoides polygyrus: Th2 cytokines and primary response phenotype. Parasitology 108, 461–471.CrossRefGoogle ScholarPubMed
Wakelin, D. (1975) Genetic control of immune responses to parasites: selection for responsiveness and non-responsiveness to Trichuris muris in random-bred mice. Parasitology 71, 377–384.CrossRefGoogle ScholarPubMed
Wakelin, D. (1978) Genetic control of suceptibility and resistance to parasitic infection. Advances in Parasitology 16, 217–308.Google Scholar
Wakelin, D. (1985) Genetic control of immunity to helminth infections. Parasitology Today 1, 17–23.CrossRefGoogle ScholarPubMed
Wakelin, D. (1988) Helminth infections. pp. 153–224 in Wakelin, D. & Blackwell, J.M. (Eds) Genetics of resistance to bacterial and parasitic infection. London, Taylor & Francis.Google Scholar
Wakelin, D. (2000) Rodent models of genetic resistance to parasitic infections. pp. 107–126 in Axford, R.F.E., Bishop, S.C., Nicholas, F.W. & Owen, U.B. (Eds) Breeding for Disease Resistance in Farm Animals. 2nd edn. Wallingford, Oxon, CAB International.Google Scholar
Wakelin, D. & Blackwell, J.M. (Eds) (1988) Genetics of resistance to bacterial and parasitic infection. London, Taylor & Francis.Google Scholar
Waller, P.J. (1986) Anthelmintic resistance in nematode parasites of sheep. Agricultural Zoology Reviews 1, 333–373.Google Scholar
Waller, P.J. (1997) Anthelmintic resistance. Veterinary Parasitology 72, 391–412.CrossRefGoogle ScholarPubMed
Wassom, D.L., David, C.S. & Gleich, G.J. (1979) Genes within the major histocompatibility complex influence susceptibility to Trichinella spiralis in the mouse. Immunogenetics 9, 491–496.CrossRefGoogle Scholar
Wassom, D.L., Brooks, B.O., Babisch, J.G. & David, C.S. (1983) 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, 371–378.CrossRefGoogle Scholar
Wassom, D.L., Wakelin, D., Brooks, B.O., Krco, C.J. & David, C.S. (1984) Genetic control of immunity to Trichinella spiralis infection of mice. Hypothesis to explain the role of H-2 genes in primary and challenge infections. Immunology 51, 625–631.Google Scholar
Wassom, D.L., Krco, C.J. & David, C.S. (1987) I-E expression and susceptibility to parasite infection. Immunology Today 8, 39–43.CrossRefGoogle Scholar
Wells, P.D. (1962) Mast cell, eosinophil and histamine levels in Nippostrongylus brasiliensis infected rats. Experimental Parasitology 12, 82–101.CrossRefGoogle ScholarPubMed
Whitlock, J.H. (1955) A study of inheritance of resistance to trichostrongylidosis in sheep. Cornell Veterinarian 45, 422–439.Google ScholarPubMed
Williams-Blangero, S., Van de Berg, J.L., Subedi, J., Aivaliotis, M.J., Rai, D.R., Upadhayay, R.P., Jha, B. & Blangero, J. (2002) Genes on chromosomes 1 and 13 have significant effects on Ascaris infection. Proceedings of the National Academy of Sciences, USA 99, 5533–5538.CrossRefGoogle ScholarPubMed
Windon, R.G. & Dineen, J.K. (1984) Parasitological and immunological competence of lambs selected for high and low responsiveness to vaccination with irradiated Trichostrongylus colubriformis larvae. pp. 13–28 in Dineen, J.K. & Outteridge, P.M. (Eds) Immunogenetic approaches to the control of endoparasites. Melbourne, CSIRO, Division of Animal Health.Google Scholar
Zadissa, A., Dodds, K.G. & McEwan, J.C. (2001) Computational comparative mapping between mammalian species. Proceedings of the Association for the Advancement of Animal Breeding and Genetics 14, 99–102.Google Scholar