Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-28T05:31:02.514Z Has data issue: false hasContentIssue false
  • English
  • Français

Heligmosomoides bakeri: a model for exploring the biology and genetics of resistance to chronic gastrointestinal nematode infections

Published online by Cambridge University Press:  19 May 2009

J. M. BEHNKE ,
D. M. MENGE  and
H. NOYES
J. M. BEHNKE*
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
D. M. MENGE
Affiliation:
Center for Infectious Diseases and Microbiology Translational Research, University of Minnesota, MTRF 2001 6th St SE, Minneapolis MN 55455, USA
H. NOYES
Affiliation:
School of Biological Sciences, Biosciences Building, University of Liverpool, Crown Street, Liverpool L69 7ZB, UK
*
*Corresponding author. Tel: +44 (0)115 9513208. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The intestinal nematode Heligmosomoides bakeri has undergone 2 name changes during the last 4 decades. Originally, the name conferred on the organism in the early 20th century was Nematospiroides dubius, but this was dropped in favour of Heligmosomoides polygyrus, and then more recently H. bakeri, to distinguish it from a closely related parasite commonly found in wood mice in Europe. H. bakeri typically causes long-lasting infections in mice and in this respect it has been an invaluable laboratory model of chronic intestinal nematode infections. Resistance to H. bakeri is a dominant trait and is controlled by genes both within and outside the MHC. More recently, a significant QTL has been identified on chromosome 1, although the identity of the underlying genes is not yet known. Other QTL for resistance traits and for the accompanying immune responses were also defined, indicating that resistance to H. bakeri is a highly polygenic phenomenon. Hence marker-assisted breeding programmes aiming to improve resistance to GI nematodes in breeds of domestic livestock will need to be highly selective, focussing on genes that confer the greatest proportion of overall genetic resistance, whilst leaving livestock well-equipped genetically to cope with other types of pathogens and preserving important production traits.

Keywords

Heligmosomoides bakeriHeligmosomoides polygyrusNematospiroides dubiusimmunityresistancegeneticsquantitative trait loci
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1565 - 1580
Copyright
Copyright © Cambridge University Press 2009

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

Abu-Madi, M. A., Mohd-Zain, S. N., Lewis, J. W. and Reid, A. P. (2000). Genomic variability within laboratory and wild isolates of the trichostrongyle mouse nematode Heligmosomoides polygyrus. Journal of Helminthology 74, 195–201.CrossRefGoogle ScholarPubMed
Abu-Madi, M. A., Pleass, R. J. and Lewis, J. W. (1994). Metabolic labelling of wild and laboratory subspecies of the trichostrongyle nematode Heligmosomoides polygyrus. Veterinary Parasitology 55, 235–243.CrossRefGoogle ScholarPubMed
Ackert, J. E., Eisenbrandt, L. L., Wilmoth, J. H., Glading, B. and Pratt, I. (1935). Comparative resistance of five breeds of chickens to the nematode Ascaridia lineata (Schneider). Journal of Agricultural Research 50, 607–624.Google Scholar
Ali, N. M. H. and Behnke, J. M. (1983). Nematospiroides dubius: factors affecting the primary response to SRBC in infected mice. Journal of Helminthology 57, 343–353.CrossRefGoogle ScholarPubMed
Ali, N. M. H. and Behnke, J. M. (1984). Non-specific immunodepression by larval and adult Nematospiroides dubius. Parasitology 8, 153–162.CrossRefGoogle Scholar
Anonymous (2007). A mouse for all reasons. Cell 128, 9–13.CrossRefGoogle Scholar
Anthony, R. M., Urban, J. F. Jr., Alem, F., Hamed, H. A., Rozo, C. T., Boucher, J.-L., Rooijen, N. V. and Gause, W. C. (2006). Memory Th2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nature Medicine 12, 955–960.CrossRefGoogle ScholarPubMed
Asakawa, M. (1988). Genus Heligmosmoides Hall, 1916 (Heligmosomidae: Nematoda) from the Japanese wood mice, Apodemus spp. II. A review of the genus Heligmosomoides with the establishment of the phylogenetic lines of known species. Journal of the College of Dairying 12, 349–365.Google Scholar
Baker, N. F. (1954). Trichostrongylidosis – the mouse as an experimental animal. Proceedings of the American Veterinary Medical Association 91, 185–191.Google Scholar
Bancroft, A. J., Else, K. J. and Grencis, R. K. (1994). Low-level infection with Trichuris muris significantly affects the polarization of the CD4 response. European Journal of Immunology 24, 3113–3118.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1994). The food resource of adult Heligmosomoides polygyrus in the small intestine. Journal of Parasitology 80, 24–28.CrossRefGoogle ScholarPubMed
Bansemir, A. D. and Sukhdeo, M. V. K. (1996). Villus length influences habitat selection by Heligmosomoides polygyrus. Parasitology 113, 311–316.CrossRefGoogle ScholarPubMed
Bartlett, A. and Ball, P. A. J. (1972). Nematospiroides dubius in the mouse as a possible model of endemic human hookworm infection. Annals of Tropical Medicine and Parasitology 66, 129–134.CrossRefGoogle ScholarPubMed
Bartlett, A. and Ball, P. A. J. (1974). The immune response of the mouse to larvae and adults of Nematospiroides dubius. International Journal for Parasitology 4, 463–470.CrossRefGoogle ScholarPubMed
Baylis, H. A. (1926). On a trichostrongylid nematode from the wood mouse (Apodemus sylvaticus). Annals and Magazine of Natural History 18, 455–464.CrossRefGoogle Scholar
Baylis, H. A. (1927). A further note on Nematospiroides dubius Baylis 1926. Annals and Magazine of Natural History 20, 102–105.CrossRefGoogle Scholar
Beh, K. J., Hulme, D. J., Callaghan, M. J., Leish, Z., Lenane, I., Windon, R. G. and Maddox, J. F. (2002). A genome scan for quantitative trait loci affecting resistance to Trichostrongylus colubriformis in sheep. Animal Genetics 33, 97–106.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 1–71.CrossRefGoogle ScholarPubMed
Behnke, J. M., Bajer, A., Sinski, E. and Wakelin, D. (2001). Interactions involving intestinal nematodes of rodents: experimental and field studies. Parasitology 122, S39–S49.CrossRefGoogle ScholarPubMed
Behnke, J. M., Barnard, C. J. and Wakelin, D. (1992). Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology Invited review 22, 861–907.CrossRefGoogle ScholarPubMed
Behnke, J. M., Cabaj, W. and Wakelin, D. (1992). Susceptibility of adult Heligmosomoides polygyrus to intestinal inflammatory responses induced by heterologous infection. International Journal for Parasitology 22, 75–86.CrossRefGoogle ScholarPubMed
Behnke, J. M., Hannah, J. and Pritchard, D. I. (1983). Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397–408.CrossRefGoogle ScholarPubMed
Behnke, J. M., Keymer, A. E. and Lewis, J. W. (1991). Heligmosomoides polygyrus or Nematospiroides dubius? Parasitology Today 7, 177–179.CrossRefGoogle ScholarPubMed
Behnke, J. M., Iraqi, F., Menge, D., Baker, L., Gibson, J. and Wakelin, D. (2003). Chasing the genes that control resistance to gastrointestinal nematodes. Journal of Helminthology 77, 99–109.CrossRefGoogle ScholarPubMed
Behnke, J. M., Iraqi, F. A., Mugambi, J. M., Clifford, S., Nagda, S., Wakelin, D., Kemp, S. J., Baker, R. L. and Gibson, J. P. (2006 a). High resolution mapping of chromosomal regions controlling resistance to gastro-intestinal nematode infections in an advanced intercross line of mice. Mammalian Genome 17, 584–597.CrossRefGoogle Scholar
Behnke, J. M., Lowe, A., Clifford, S. and Wakelin, D. (2003). Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrys bakeri. Parasite Immunology 25, 333–340.CrossRefGoogle ScholarPubMed
Behnke, J. M., Mugambi, J. M., Clifford, S., Iraqi, F., Baker, R. L., Gibson, J. P. and Wakelin, D. (2006 b). Genetic variation in resistance to repeated infections with Heligmosomoides polygyrus bakeri, in inbred mouse strains selected for the Mouse Genome Project. Parasite Immunology 28, 85–94.CrossRefGoogle ScholarPubMed
Behnke, J. M. and Parish, H. A. (1979 a). Nematospiroides dubius: Arrested development of larvae in immune mice. Experimental Parasitology 47, 116–127.CrossRefGoogle ScholarPubMed
Behnke, J. M. and Parish, H. A. (1979 b). Expulsion of Nematospiroides dubius from the intestine of mice treated with immune serum. Parasite Immunology 1, 31–26.CrossRefGoogle ScholarPubMed
Behnke, J. M. and 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. and 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. and Wakelin, D. (1973). The survival of Trichuris muris in wild populations of its natural hosts. Parasitology 67, 157–164.CrossRefGoogle ScholarPubMed
Behnke, J. M. and 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., Williams, D. J., Hannah, J. and Pritchard, D. I. (1987). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): the capacity of adult worms to survive following transplantation to recipient mice. Parasitology 95, 569–581.CrossRefGoogle ScholarPubMed
Ben-Smith, A., Lammas, D. A. and Behnke, J. M. (2003). The relative involvement of Th1 and Th2 associated immune responses in the expulsion of a primary infection of Heligmosomoides polygyrus in mice of differing response phenotype. Journal of Helminthology 77, 133–146.CrossRefGoogle ScholarPubMed
Bishop, S. C. and Morris, C. A. (2007). Genetics of disease resistance in sheep and goats. Small Ruminant Research 70, 48–59.CrossRefGoogle Scholar
Bishop, S. C. and Stear, M. J. (2003). Modelling of host genetics and resistance to infectious diseases: understanding and controlling nematode infections. Veterinary Parasitology 115, 147–166.CrossRefGoogle ScholarPubMed
Bisset, S. A., Vlassoff, A., West, C. J. and Morrison, L. (1997). Epidemiology of nematodosis in Romney lambs selectively bred for resistance or susceptibility to nematode infection. Veterinary Parasitology 70, 255–269.CrossRefGoogle ScholarPubMed
Brailsford, T. J. and 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. and 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
Brindley, P. J., He, S., Sitepu, P., Pattie, W. A. and Dobson, C. (1986). Inheritance of immunity in mice to challenge infection with Nematospiroides polygyrus. Heredity 57, 53–58.CrossRefGoogle Scholar
Broman, K. W., Rowe, L. B., Churchill, G. A. and Paigen, K. (2002). Crossover interference in the mouse. Genetics 160, 1123–1131.CrossRefGoogle ScholarPubMed
Bryant, V. (1973). The life cycle of Nematospiroides dubius, Baylis, 1926 (Nematoda: Heligmosomidae). Journal of Helminthology 47, 263–268.CrossRefGoogle ScholarPubMed
Cable, J., Harris, P. D., Lewis, J. W. and Behnke, J. M. (2006). Molecular evidence that Heligmosomoides polygyrus from laboratory mice and wood mice are separate species. Parasitology 133, 111–122.CrossRefGoogle ScholarPubMed
Chehresa, A., Beech, R. N. and Scott, M. E. (1997). Life-history variation among lines isolated from a laboratory population of Heligmosomoides polygyrus bakeri. International Journal for Parasitology 27, 541–551.CrossRefGoogle ScholarPubMed
Colditz, G. I. (2004). Some mechanisms regulating nutrient utilization in livestock during immune activation: An overview. Australian Journal of Experimental Agriculture 44, 453–457.CrossRefGoogle Scholar
Colwell, D. A. and Wescott, R. B. (1973). Prolongation of egg production of Nippostrongylus brasiliensis in mice concurrently infected with Nematospiroides dubius. Journal of Parasitology 59, 216.CrossRefGoogle ScholarPubMed
Courtney, C. H. and Forrester, D. J. (1973). Interspecific interaction between Hymenolepis microstoma (Cestoda) and Heligmosomoides polygyrus (Nematoda) in mice. Journal of Parasitology 59, 480–483.CrossRefGoogle ScholarPubMed
Crandall, R. B., Crandall, C. A. and Franco, J. A. (1974). Heligmosomoides polygyrus (=Nematospiroides dubius): humoral and intestinal immunologic responses to infection in mice. Experimental Parasitology 35, 275–287.CrossRefGoogle ScholarPubMed
Crawford, C., Behnke, J. M. and Pritchard, D. I. (1989). Suppression of heterologous immunity by Nematospiroides dubius antigens in vitro. International Journal for Parasitology 19, 29–34.CrossRefGoogle ScholarPubMed
Cypess, R. H., Lucia, H. L., Dunsford, H. A. and Enriquez, F. J. (1988). The tissue reactions of mice to infection with Heligmosomoides polygyrus. Journal of Helminthology 62, 69–76.CrossRefGoogle Scholar
Cypess, R. H., Lucia, H. L., Zidian, J. L. and Rivera-Ortiz, C. I. (1977). Heligmosomoides polygyrus: temporal, spatial and morphological population characteristics in LAF1/J mice. Experimental Parasitology 42, 34–43.CrossRefGoogle ScholarPubMed
Cypess, R. H. and Zidian, J. L. (1975). Heligmosomoides polygyrus (=Nematospiroides dubius): the development of self-cure and/or protection in several strains of mice. Journal of Parasitology 61, 819–824.CrossRefGoogle ScholarPubMed
Darvasi, A. and Soller, M. (1992). Selective genotyping for determination of linkage between a molecular marker and a quantitative trait locus. Theoretical and Applied Genetics 85, 353–359.CrossRefGoogle Scholar
Davies, G., Stear, M. J., Benothman, M., Abuagob, O., Kerr, A., Mitchell, S. and Bishop, S. C. (2006). Quantitative trait loci associated with parasitic infection in Scottish blackface sheep. Heredity 96, 252–258.CrossRefGoogle ScholarPubMed
Day, K. P., Howard, J. R., Prowse, S. J., Chapman, C. B. and Mitchell, G. F. (1979). Studies on chronic versus transient intestinal nematode infections in mice. I. A comparison of responses to excretory/secretory (ES) products of Nippostrongylus brasiliensis and Nematospiroides dubius worms. Parasite Immunology 1, 217–239.CrossRefGoogle Scholar
Dehlawi, M. S., Wakelin, D. and Behnke, J. M. (1987). Suppression of mucosal mastocytosis by infection with the intestinal nematode Nematospiroides dubius. Parasite Immunology 9, 187–194.CrossRefGoogle ScholarPubMed
Dehlawi, M. S. and Wakelin, D. (1988). Suppression of mucosal mastocytosis by Nematospiroides dubius results from an adult worm-mediated effect upon host lymphocytes. Parasite Immunology 10, 85–95.CrossRefGoogle ScholarPubMed
Della Bruna, C. and Xenia, B. (1976). Nippostrongylus brasiliensis in mice: reduction of worm burden and prolonged infection induced by presence of Nematospiroides dubius. Journal of Parasitology 62, 490–491.CrossRefGoogle ScholarPubMed
Dietrich, W., Katz, H., Lincoln, S. E., Shin, H.-S., Friedman, J., Dracopoli, N. C. and Lander, E. S. (1992). A genetic map of the mouse suitable for typing intraspecific crosses. Genetics 131, 423–447.CrossRefGoogle ScholarPubMed
Dietrich, W. F., Miller, J., Steen, R., Merchant, M. A., Damron-Boles, D. et al. (1996). A comprehensive genetic map of the mouse genome. Nature, London 380, 149–152.CrossRefGoogle ScholarPubMed
Diez-Tascón, C., Keane, O. M., Wilson, T., Zadissa, A., Hyndman, D. L., Baird, D. B., McEwan, J. C. and Crawford, A. M. (2005). Microarray analysis of selection lines from outbred populations to identify genes involved with nematode parasite resistance in sheep. Physiological Genomics 21, 59–69.CrossRefGoogle ScholarPubMed
Dobson, C. (1961). Certain aspects of the host-parasite relationship of Nematospiroides dubius (Baylis) I. Resistance of male and female mice to experimental infections. Parasitology 52, 173–179.CrossRefGoogle Scholar
Dobson, C. (1982). Passive transfer of immunity with serum in mice infected with Nematospiroides dubius: influence of quality and quantity of immune serum. International Journal for Parasitology 12, 207–213.CrossRefGoogle ScholarPubMed
Dobson, C., Sitepu, P. and Brindley, P. J. (1985). Influence of primary infection on the population dynamics of Nematospiroides dubius after challenge infections in mice. International Journal for Parasitology 15, 353–359.CrossRefGoogle ScholarPubMed
Dobson, C. and Tang, J. (1991). Genetic variation and host-parasite relations: Nematospiroides dubius in mice. Journal of Parasitology 77, 884–889.CrossRefGoogle ScholarPubMed
Doligalska, M., Rzepecka, J., Drela, N., Donskow, K. and Gerwel-Wronka, M. (2006). The role of TGF-β in mice infected with Heligmosomoides polygyrus. Parasite Immunology 28, 387–395.CrossRefGoogle ScholarPubMed
Dominik, S. (2005). Quantitative trait loci for internal nematode resistance in sheep: a review. Genetics Selection Evolution 37 (Suppl. 1), S83–S96.CrossRefGoogle ScholarPubMed
Dujardin, F. (1845). Histoire Naturelle des Helminthes ou vers Intestinaux. Librarie Encyclopédique de Roret, Paris, France.CrossRefGoogle Scholar
Durette-Desset, M. C., Kinsella, J. M. and Forrester, D. J. (1972). Arguments en faveur de la double origine des nematodes nearctiques du genre Heligmosomoides HALL, 1916. Annales de Parasitologie (Paris) 47, 365–382.Google Scholar
Ehrenford, F. A. (1954). The cycle of Nematospiroides dubius Baylis (Nematoda: Heligmosomidae). Journal of Parasitology 40, 480–481.CrossRefGoogle Scholar
Elliott, D. E., Setiawan, T., Metwali, A., Blum, A., Urban, J. F. and Weinstock, J. V. (2004). Heligmosomoides polygyrus inhibits established colitis in IL-10-defieient mice. European Journal of Immunology 34, 2690–2698.CrossRefGoogle ScholarPubMed
Else, K. J. and Finkelman, F. D. (1998). Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28, 1145–1158.CrossRefGoogle ScholarPubMed
Else, K. J. and 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. and Klein, J. (1990). The influence of genes mapping within the major histocompatibility complex on resistance to Trichuris muris infection of mice. Parasitology 101, 61–67.CrossRefGoogle Scholar
Enriquez, F. J., Brooks, B. O., Cypess, R. H., David, C. S. and Wassom, D. L. (1988 a). Nematospiroides dubius: Two H-2-linked genes influence levels of resistance to infection in mice. Experimental Parasitology 67, 221–226.CrossRefGoogle ScholarPubMed
Enriquez, F. J., Cypess, R. H. and Wassom, D. L. (1988 b). Influence of immunizing dose and presence or absence of adult worms on the development of resistance to Nematospiroides dubius challenge infections of mice. Journal of Parasitology 74, 409–414.CrossRefGoogle ScholarPubMed
Enriquez, F. J., Zidian, J. L. and Cypess, R. H. (1988 c). Nematospiroides dubius: Genetic control of immunity to infections of mice. Experimental Parasitology 67, 12–19.CrossRefGoogle ScholarPubMed
Fahmy, M. A. M. (1956). An investigation on the life cycle of Nematospiroides dubius (Nematoda: Heligmosomidae) with special reference to the free-living stages. Zeitschrift für Parasitenkunde 17, 394–399.CrossRefGoogle Scholar
Fakae, B. B., Harrison, L. J. and Sewell, M. M. M. (2000). The intensity and duration of primary Heligmosomoides polygyrus infection in TO mice modify acquired immunity to secondary challenge. Journal of Helminthology 74, 225–231.CrossRefGoogle ScholarPubMed
Finney, C. A., Taylor, M. D., Wilson, M. S. and Maizels, R. M. (2007). Expansion and activation of CD4(+)CD25(+) regulatory T cells in Heligmosomoides polygyrus infection. European Journal of Immunology 37, 1874–1886.CrossRefGoogle ScholarPubMed
Fisher, P., Hedeler, C., Wolstencroft, K., Hulme, H., Noyes, H., Kemp, S., Stevens, R. and Brass, A. (2007). A systematic strategy for large-scale analysis of genotype phenotype correlations: identification of candidate genes involved in African trypanosomiasis. Nucleic Acids Research 35, 5625–5633.CrossRefGoogle ScholarPubMed
Flint, J., Valdar, W., Shifman, S. and Mott, R. (2005). Strategies for mapping and cloning quantitative trait genes in rodents. Nature Reviews Genetics 6, 271–286.CrossRefGoogle ScholarPubMed
Foote, S. J., Iraqi, F. and Kemp, S. J. (2005). Controlling malaria and African trypanosomiasis: the role of the mouse. Briefings in Functional Genomics and Proteomics 4, 214–224.CrossRefGoogle ScholarPubMed
Forrester, D. J. (1971). Heligmosomoides polygyrus (=Nematospiroides dubius) from wild rodents of Northern California: natural infections, host-specificity, and strain characteristics. Journal of Parasitology 57, 498–503.CrossRefGoogle ScholarPubMed
Forrester, D. J. and Neilson, J. T. MCL. (1973). Comparative infectivity of Heligmosomoides polygyrus (=Nematospiroides dubius) in three species of Peromyscus. Journal of Parasitology 59, 251–255.CrossRefGoogle ScholarPubMed
Fox, J. G., Beck, P., Dangler, C. A., Whary, M. T., Wang, T. C., Shi, H. N. and Nagler-Anderson, C. (2000). Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces Helicobacter-induced gastric atrophy. Nature Medicine 6, 536–542.CrossRefGoogle ScholarPubMed
Frazer, K. A., Eskin, E., Kang, H. M., Bogue, M. A., Hinds, D. A., Beilharz, E. J., Gupta, R. V., Montgomery, J., Morenzoni, M. M., Nilsen, G. B., Pethiyagoda, C. L., Stuve, L. L., Johnson, F. M., Daly, M. J., Wade, C. M. and Cox, D. R. (2007). A sequence-based variation map of 8·27 million SNPs in inbred mouse strains. Nature, London 448, 1050–1053.CrossRefGoogle ScholarPubMed
Gause, W. C., Urban, J. F. Jr. and Stadecker, M. J. (2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269–277.CrossRefGoogle ScholarPubMed
Hernandez, A. D. and Sukhdeo, M. V. (1995). Host grooming and transmission strategy of Heligmosomoides polygyrus. Journal of Parasitology 81, 865–869.CrossRefGoogle ScholarPubMed
Hernandez-Valladares, M., Naessens, J., Gibson, J. P., Musoke, A. J., Nagda, S., Rihet, P., Ole-MoiYoi, O. K. and Iraqi, F. A. (2004). Confirmation and dissection of QTL controlling resistance to malaria in mice. Mammalian Genome 15, 390–398.CrossRefGoogle ScholarPubMed
Hill, N. J., Lyons, P. A., Armitage, N., Todd, J. A., Wicker, L. S. and Peterson, L. B. (2000). NOD Idd5 locus controls insulitis and diabetes and overlaps the orthologous CTLA4/IDDM12 and NRAMP1 loci in humans. Diabetes 49, 1744–1747.CrossRefGoogle ScholarPubMed
Hunter, K. W. and Crawford, N. P. S. (2008). The future of mouse QTL mapping to diagnose disease in mice in the age of whole-genome association. Annual Reviews in Genetics 42, 131–141.CrossRefGoogle ScholarPubMed
Iraqi, F. A., Behnke, J. M., Menge, D. M., Lowe, A., Teale, A. J., Gibson, J. P., Baker, L. R. and Wakelin, D. (2003). Chromosomal regions controlling resistance to gastro-intestinal nematode infections in mice. Mammalian Genome 14, 184–191.CrossRefGoogle ScholarPubMed
Iraqi, F., Clapcott, S. J., Kumar, P., Haley, C. S., Kemp, S. J. and Teale, A. (2000). Fine mapping of trypanosomiasis resistance loci in murine advanced intercross lines. Mammalian Genome 11, 645–648.CrossRefGoogle ScholarPubMed
Iraqi, F. A., Churchill, G. and Mott, R. (2008). The Collaborative Cross, developing a resource for mammalian systems genetics: a status report of the Wellcome Trust cohort. Mammalian Genome 19, 379–381.CrossRefGoogle Scholar
Jenkins, D. C. and Phillipson, R. F. (1971). The kinetics of repeated low-level infections of Nippostrongylus brasiliensis in the laboratory rat. Parasitology 62, 457–465.CrossRefGoogle ScholarPubMed
Jones, C. E. and Rubin, R. (1974). Nematospiroides dubius: mechanisms of host immunity. I. Parasite counts, histopathology and serum transfer involving orally or subcutaneously sensitized mice. Experimental Parasitology 35, 434–452.CrossRefGoogle ScholarPubMed
Kemp, S. J., Iraqi, F., Darvasi, A., Soller, M. and Teale, A. J. (1997). Localization of genes controlling resistance to trypanosomiasis in mice. Nature Genetics 16, 194–196.CrossRefGoogle ScholarPubMed
Kerboeuf, D. (1978). The effects of time and temperature of storage on the infectivity of third-stage larvae of Heligmosomoides polygyrus (=Nematospiroides dubius) 1. Effects on the development to the adult stage in mice. Annales de Recherches Veterinaires 9, 153–159.Google Scholar
Khan, I. A., Hakak, R., Eberle, K., Sayles, P., Weiss, L. M. and Urban, J. F. Jr. (2008). Coinfection with Heligmosomoides polygyrus fails to establish CD8+ T-cell immunity against Toxoplasma gondii. Infection and Immunity 76, 1305–1313.CrossRefGoogle ScholarPubMed
Koudandé, O. D., van Arendonk, J. A. M and Iraqi, F. (2005). Marker-assisted introgression of trypanotolerance QTL in mice. Mammalian Genome 16, 112–119.CrossRefGoogle ScholarPubMed
Lewis, J. and Bryant, V. (1976). The distribution of Nematospiroides dubius within small intestine of laboratory mice. Journal of Helminthology 50, 163–171.CrossRefGoogle ScholarPubMed
Liu, S. K. (1965). Pathology of Nematospiroides dubius. I Primary infections in C3H and Webster mice. Experimental Parasitology 17, 123–135.CrossRefGoogle ScholarPubMed
Liu, S. K. (1966). Genetic influence on resistance of mice to Nematospiroides dubius. Experimental Parasitology 18, 311–319.CrossRefGoogle Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle ScholarPubMed
McEwan, J. C., Dodds, K. G., Greer, G. J., Bain, W. E., Duncan, S. J., Wheeler, R., Knowler, K. J., Reid, P. J., Green, R. S. and Douch, P. G. C. (1995). Genetic estimates for parasite resistance traits in sheep and their correlations with production traits. New Zealand Journal of Zoology 22, 177.Google Scholar
Menge, D. M., Behnke, J. M., Lowe, A., Gibson, J. P., Iraqi, F. A., Baker, L. and Wakelin, D. (2003). Mapping of chromosomal regions influencing immunological responses to gastrointestinal nematode infections in mice. Parasite Immunology 25, 341–349.CrossRefGoogle ScholarPubMed
Mitchell, G. F., Anders, R. F., Brown, G. V., Handman, E., Roberts-Thomson, I. C., Chapman, C. B., Forsyth, K. P., Kahl, L. P. and Cruise, K. M. (1982). Analysis of infection characteristics and antiparasite immune responses in resistant compared with susceptible hosts. Immunological Reviews 61, 137–188.CrossRefGoogle ScholarPubMed
Mitchell, G. F. and Prowse, S. J. (1979). Three consequences of infection with Nematospiroides dubius in three inbred strains of mice. Journal of Parasitology 65, 820–822.CrossRefGoogle ScholarPubMed
Monroy, F. G. and Enriquez, F. J. (1992). Heligmosomoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 49–54.CrossRefGoogle Scholar
Morimoto, M., Morimoto, M., Whitmire, J., Xiao, S., Anthony, R. M., Mirakami, H., Star, R. A., Urban, J. F. Jr. and Gause, W. C. (2004). Peripheral CD4 T cells rapidly accumulate at the host: parasite interface during an inflammatory Th2 memory response. Journal of Immunology 172, 2424–2430.CrossRefGoogle ScholarPubMed
Njoroge, J. M., Scott, M. E. and Jalili, F. (1997). The efficacy of ivermectin against laboratory strains of Heligmosomoides polygyrus (Nematoda). International Journal for Parasitology 27, 439–442.CrossRefGoogle ScholarPubMed
Oliver, M. K., Telfer, S. and Piertney, S. B. (2009). Major histocompatibility complex (MHC) heterozygote superiority to natural multi-parasite infections in the water vole (Arvicola terrestris). Proceedings of the Royal Society of London, B 276, 1119–1128.Google ScholarPubMed
Panter, H. C. (1969). Host/parasite relationship of Nematospiroides dubius in the mouse. Journal of Parasitology 55, 33–37.CrossRefGoogle Scholar
Penn, D. J., Damjanovich, K. and Potts, W. K. (2002). MHC heterozygosity confers a selective advantage against multiple-strain infections. Proceedings of the National Academy of Sciences, USA 99, 11260–11264.CrossRefGoogle ScholarPubMed
Peters, L. L., Robledo, R. F., Bult, C. J., Churchill, G. A., Paigen, B. J. and Svenson, K. L. (2007). The mouse as a model for human biology: a resource guide for complex trait analysis. Nature Reviews Genetics 8, 58–69.CrossRefGoogle Scholar
Pleass, R. J. and Bianco, A. E. (1994). The role of adult worms in suppressing functional protective immunity to Heligmosomoides polygyrus bakeri challenge infections. Parasite Immunology 16, 619–628.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Ali, N. M. H. and Behnke, J. M. (1984). Analysis of the mechanism of immunodepression following heterologous antigenic stimulation during concurrent infection with Nematospiroides dubius. Immunology 51, 633–642.Google ScholarPubMed
Pritchard, D. I. and Behnke, J. M. (1985). The suppression of homologous immunity by soluble adult antigens of Nematospiroides dubius. Journal of Helminthology 59, 251–256.CrossRefGoogle ScholarPubMed
Prowse, S. J., Mitchell, G. F., Ey, P. L. and Jenkin, C. R. (1979). The development of resistance in different inbred strains of mice to infections with Nematospiroides dubius. Parasite Immunology 1, 277–288.CrossRefGoogle ScholarPubMed
Quinnell, R., Behnke, J. M. and Keymer, A. E. (1991). Host specificity of and cross-immunity between two strains of Heligmosomoides polygyrus. Parasitology 102, 419–427.CrossRefGoogle ScholarPubMed
Rhodes, M., Straw, R., Fernando, S., Evans, A., Lacey, T., Dearlove, A., Greystrong, J., Walker, J., Watson, P., Weston, P., Kelly, M., Taylor, D., Gibson, K., Mundy, C., Bourgade, F., Poirier, C., Simon, D., Brunialti, A. L., Montagutelli, X., Gu'enet, J. L., Haynes, A. and Brown, S. D. (1998). A high-resolution microsatellite map of the mouse genome. Genome Research 8, 531–542.CrossRefGoogle ScholarPubMed
Rice, M. C. and O'Brien, S. J. (1980). Genetic variance of laboratory outbred Swiss mice. Nature, London 283, 157–161.CrossRefGoogle ScholarPubMed
Robinson, M., Behnke, J. M. and Williams, D. J. L. (1988). Immunity to adult Heligmosomoides polygyrus (Nematospiroides dubius): survival or rejection of adult worms following transplantation to mice refractory to larval challenge. Journal of Helminthology 62, 221–231.CrossRefGoogle ScholarPubMed
Robinson, M., Wahid, F. N., Behnke, J. M. and 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
Rzepecka, J., Donskow-Schmelter, K. and Doligalska, M. (2007). Heligmosomoides polygyrus infection down-regulates eotaxin concentration and CCR3 expression on lung eosinophils in murine allergic pulmonary inflammation. Parasite Immunology 29, 405–413.CrossRefGoogle ScholarPubMed
Rzepecka, J., Lucius, R., Doligalska, M., Beck, S., Rausch, S. and Hartmann, S. (2006). Screening for immunomodulatory proteins of the intestinal parasitic nematode Heligmosomoides polygyrus. Parasite Immunology 28, 463–472.CrossRefGoogle ScholarPubMed
Sakai, T., Kikkawa, Y., Miura, I., Inoue, T., Moriwaki, K., Shiroishi, T., Satta, Y., Takahata, N. and Yonekawa, H. (2005). Origins of mouse inbred strains deduced from whole-genome scanning by polymorphic microsatellite loci. Mammalian Genome 16, 11–19.CrossRefGoogle ScholarPubMed
Segura, M., Su, Z., Piccirillo, C. and Stevenson, M. M. (2007). Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression. European Journal of Immunology 37, 1887–1904.CrossRefGoogle ScholarPubMed
Shimp, R. G., Crandall, R. B. and Crandall, C. A. (1975). Heligmosomoides polygyrus (=Nematospiroides dubius): Suppression of antibody response to orally administered sheep erythrocytes in infected mice. Experimental Parasitology 38, 257–269.CrossRefGoogle ScholarPubMed
Silver, L. (1995). Mouse Genetics. Oxford University Press, Oxford, UK. http://www.complextrait.org/archive/2001/HTML/silverbook/index.shtmlGoogle Scholar
Silver, L. (2008). Mouse Genetics; Concepts and Applications. The Jackson Laboratory, Bar Harbor, Maine, USA. http://www.informatics.jax.org/silverbook/Google Scholar
Spurlock, G. M. (1943). Observations on host-parasite relations between laboratory mice and Nematospiroides dubius. Journal of Parasitology 29, 303–311.CrossRefGoogle Scholar
Stear, M. J., Innocent, G. T. and Buitkamp, J. (2005). The evolution and maintenance of polymorphism in the major histocompatibility complex. Veterinary Immunology and Immunopathology 108, 53–57.CrossRefGoogle ScholarPubMed
Sukhdeo, M. V. K., O'Grady, R. T. and Hsu, S. C. (1984). The site selected by the larvae of Heligmosomoides polygyrus. Journal of Helminthology 58, 19–23.CrossRefGoogle ScholarPubMed
Suzuki, T., Ishih, A., Kino, H., Muregi, F. W., Takabayashi, S., Nishikawa, T., Takagi, H. and Terada, M. (2006). Chromosomal mapping of host resistance loci to Trichinella spiralis nematode infection in rats. Immunogenetics 58, 26–30.CrossRefGoogle ScholarPubMed
Tang, J., Dobson, C. and McManus, D. P. (1995). Phenotypes of Heligmosomoides polygyrus selected to survive protective immunity in Quackenbush mice. Journal of Parasitology 81, 900–904.CrossRefGoogle ScholarPubMed
Telford, G., Wheeler, D. J., Appleby, P., Bowen, J. G. and Pritchard, D. I. (1989). Heligmosomoides polygyrus immunomodulatory factor (IMF) targets T-lymphocytes. Parasite Immunology 20, 601–611.CrossRefGoogle Scholar
Tenora, F. and Barus, V. (2001). Synonymy of the nematode Heligmosomoides polygyrus (Heligmosomidae) and notes on the validity of related species. Helminthologia 38, 176.Google Scholar
Tenora, F., Barus, V. and Prokes, M. (2003). Notes to the species Heligmosomoides polygyrus (Dujardin, 1845) (Nematoda, Heligmosomidae), parasitizing rodentia. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 51, 7–18.Google Scholar
The Wellcome Trust Case Control Consortium (2007). Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature, London 447, 661–678.CrossRefGoogle Scholar
Tsang, S., Sun, Z., Luke, B., Stewart, C., Lum, N., Gregory, M., Wu, X., Subleski, M., Jenkins, N. A., Copeland, N. G. and Munroe, D. J. (2005). A comprehensive SNP-based genetic analysis of inbred mouse strains. Mammalian Genome 16, 476–480.CrossRefGoogle ScholarPubMed
van Zandt, P. D. (1961). Studies on the immunity relationship in white mice given infections with Nematospiroides dubius Baylis, 1926 (Nematoda: Heligmosomidae). Journal of the Elisha Mitchell Scientific Society 77, 300–309.Google Scholar
Wahid, F. N. and Behnke, J. M. (1992). Stimuli for acquired resistance to Heligmosomoides polygyrus from intestinal tissue resident L3 and L4 larvae. International Journal for Parasitology 22, 699–710.CrossRefGoogle ScholarPubMed
Wahid, F. N. and 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, 343–350.CrossRefGoogle ScholarPubMed
Wahid, F. N. and Behnke, J. M. (1996). Genetic control of acquired resistance to Heligmosomoides polygyrus: overcoming genetically determined weak responder status by strategic immunization with ivermectin-abbreviated infections. Journal of Helminthology 70, 159–168.CrossRefGoogle ScholarPubMed
Wahid, F. N., Behnke, J. M., Grencis, R. K., Else, K. J. and 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
Wahid, F. N., Robinson, M. and 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
Wakelin, D. (1978). Genetic control of susceptibility and resistance to parasitic infection. Advances in Parasitology 16, 219–308.CrossRefGoogle ScholarPubMed
Wakelin, D. and Blackwell, J. M. (1988). Genetics of Resistance to Bacterial and Parasitic Infections. Taylor and Francis, London, UK.Google Scholar
Wassom, D. L., Brooks, B. O., Cypess, R. H. and David, C. S. (1983). 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, 1033–1037.CrossRefGoogle ScholarPubMed
Wassom, D. L. and Kelly, E. A. B. (1990). The role of the histocompatibility complex in resistance to parasite infections. Critical Reviews in Immunology 10, 31–52.Google ScholarPubMed
Wassom, D. L., Wakelin, D., Brooks, B. O., Krco, C. J. and 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 ScholarPubMed
Watanabe, N., Ishiwata, K., Kaneko, S., Oku, Y., Kamiya, M. and Katakura, K. (1993). Immune defense and eosinophilia in congenitally IgE-deficient SJA/9 mice infected with Angiostrongylus costaricensis. Parasitology Research 79, 431–434.CrossRefGoogle ScholarPubMed
Wegner, K. M., Reusch, T. B. H. and Kalbe, M. (2003). Multiple parasites are driving major histocompatibility complex polymorphism in the wild. Journal of Evolutionary Biology 16, 224–232.CrossRefGoogle ScholarPubMed
Wicker, L. S., Chamberlain, G., Hunter, K., Rainbow, D., Howlett, S., Tiffen, P., Clark, J., Gonzalez-Munoz, A., Cumiskey, A. M., Rosa, R. L., Howson, J. M., Smink, L. J., Kingsnorth, A., Lyons, P. A., Gregory, S., Rogers, J., Todd, J. A. and Peterson, L. B. (2004). Fine mapping, gene content, comparative sequencing, and expression analyses support Ctla4 and Nramp1 as candidates for Idd5.1 and Idd5.2 in the nonobese diabetic mouse. Journal of Immunology 173, 164–173.CrossRefGoogle ScholarPubMed
Wilson, M. S., Taylor, M. D., Balic, A., Finney, C. A., Lamb, J. R. and Maizels, R. M. (2005). Suppression of allergic airway inflammation by helminth-induced regulatory T cells. Journal of Experimental Medicine 202, 1199–1212.CrossRefGoogle ScholarPubMed
Zaralis, K., Tolkamp, B. J., Houdijk, J. G. M., Wylie, A. R. G. and Kyriazakis, I. (2008). Changes in food intake and circulating leptin due to gastrointestinal parasitism in lambs of two breeds. Journal of Animal Science 86, 1891–1903.CrossRefGoogle ScholarPubMed
Zhong, S. and Dobson, C. (1996). Heligmosomoides polygyrus: resistance in inbred, outbred and selected mice. Experimental Parasitology 82, 122–131.CrossRefGoogle ScholarPubMed