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Quantitative trait loci for resistance to Heligmosomoides bakeri and associated immunological and pathological traits in mice: comparison of loci on chromosomes 5, 8 and 11 in F2 and F6/7 inter-cross lines of mice

Published online by Cambridge University Press:  19 November 2009

J. M. BEHNKE ,
D. M. MENGE ,
S. NAGDA ,
H. NOYES ,
F. A. IRAQI ,
S. J. KEMP ,
R. J. M. MUGAMBI ,
R. L. BAKER ,
D. WAKELIN  and
J. P. GIBSON
J. M. BEHNKE*
Affiliation:
School of Biology, University of Nottingham, NottinghamNG7 2RD, UK
D. M. MENGE
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
S. NAGDA
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
H. NOYES
Affiliation:
School of Biological Sciences, University of Liverpool, LiverpoolL69 7ZB, UK
F. A. IRAQI
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
S. J. KEMP
Affiliation:
School of Biological Sciences, University of Liverpool, LiverpoolL69 7ZB, UK
R. J. M. MUGAMBI
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
R. L. BAKER
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
D. WAKELIN
Affiliation:
School of Biology, University of Nottingham, NottinghamNG7 2RD, UK
J. P. GIBSON
Affiliation:
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
*
*Corresponding author: School of Biology, University of Nottingham, NottinghamNG7 2RD, UK Tel: +44(0)115 951 3208. E-mail jerzy.behnke@nottingham.ac.uk
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Summary

A comparison of F2 and F6/7 inter-cross lines of mice, derived from CBA and SWR parental strains, has provided strong evidence for several previously undetected quantitative trait loci (QTL) for resistance to Heligmosomoides bakeri. Five QTL affecting average faecal egg counts and/or worm burdens in week 6 were detected on mouse chromosomes 5 (Hbnr9 and Hbnr10), 8 (Hbnr11) and 11 (Hbnr13 and Hbnr14). Three QTL for faecal egg counts in weeks 4 and 6 were found on both chromosomes 5 (Hbnr9) and 11 (Hbnr13 and Hbnr14). Two QTL for the mucosal mast cell protease 1 (MCPT1) response were located on chromosomes 8 (Hbnr11) and 11 (Hbnr13), two for the IgG1 antibody response to adult worms on chromosomes 5 (Hbnr10) and 8 (Hbnr11), two for PCV in week 6 on chromosomes 5 (Hbnr9) and 11 (Hbnr13), and two for the granulomatous response on chromosome 8 (Hbnr12) and 11 (Hbnr15). Our data emphasize that the control of resistance to H. bakeri is multigenic, and regulated by genes within QTL regions that have a complex range of hierarchical relationships.

Keywords

Heligmosomoides bakeriHeligmosomoides polygyrusQTLresistancenematodesantibodyIgG1Mcpt1MCPT1granulomatous response
Type
Research Article
Information
Parasitology , Volume 137 , Issue 2 , February 2010 , pp. 311 - 320
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Albers, G. A. A. and Gray, G. D. (1987). Breeding for worm resistance: a perspective. International Journal for Parasitology 17, 559–566.CrossRefGoogle ScholarPubMed
Baker, R. L., Nagda, S., Rodriguez-Zas, S. L., Southey, B. R., Audho, J. O., Aduda, E. O. and Thorpe, W. (2003). Resistance and resilience to gastro-intestinal nematode parasites and relationships with productivity of Red Massai, Dorper and Red Massai x Dorper crossbred lambs in the sub-humid tropics. Animal Science 76, 119–136.Google Scholar
Behnke, J. M., Iraqi, F., Menge, D., Baker, L., Gibson, J. and Wakelin, D. (2003 a). Chasing the genes that control resistance to gastrointestinal nematodes. Journal of Helminthology 77, 99–109.Google Scholar
Behnke, J. M., Iraqi, F. A., Mugambi, J. M., Clifford, S., Nagda, S., Wakelin, D., Stephen, J., 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., Keymer, A. E. and Lewis, J. W. (1991). Heligmosomoides polygyrus or Nematospiroides dubius? Parasitology Today 7, 177–179.CrossRefGoogle ScholarPubMed
Behnke, J. M., Lowe, A., Clifford, S. and Wakelin, D. (2003 b). Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrus bakeri. Parasite Immunology 25, 333–340.Google Scholar
Behnke, J. M., Menge, D. and Noyes, H. (2009). Heligmosomoides bakeri: a model for exploring the biology and genetics of resistance to chronic gastrointestinal nematode infections. Parasitology 136 (in the Press).Google Scholar
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.Google Scholar
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
Ben-Smith, A., Lammas, D. A. and Behnke, J. M. (2002). Effect of oxygen radicals and differential expression of catalase and superoxide dismutase in adult Heligmosomoides polygyrus during primary infections in mice with differing response phenotypes. Parasite Immunology 24, 119–129.Google Scholar
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.Google Scholar
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
Dominik, S. (2005). Quantitative trait loci for internal nematode resistance in sheep: a review. Genetics Selection Evolution 37 (Suppl.1) S83–S96.CrossRefGoogle ScholarPubMed
Enriquez, F. J., Brooks, B. O., Cypess, R. H., David, C. S. and Wassom, D. L. (1988). Nematospiroides dubius: Two H-2 -linked genes influence levels of resistance to infection in mice. Experimental Parasitology 67, 221–226.CrossRefGoogle ScholarPubMed
Eppig, J. T. (2006). Mouse strain and genetic nomenclature: an abbreviated guide. In The Mouse in Biomedical Research, Vol. 1, 2nd Edn (ed. Fox, J., Barthold, S., Davvison, M., Newcomer, C., Quimby, F. and Smith, A.), pp. 79–98. Academic Press, London, UK.Google Scholar
Felsenstein, J. (2005). PHYLIP (Phylogeny Interference Package) version 3.6. http://evolution.genetics.washington.edu/phylip.htmlGoogle Scholar
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
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
Gilleard, J. S. (2006). Understanding anthelmintic resistance: the need for genomics and genetics. International Journal for Parasitology 36, 1227–1239.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.Google Scholar
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.Google Scholar
Kaplan, R. M. (2004). Drug resistance in nematodes of veterinary importance. Trends in Parasitology 20, 477–481.CrossRefGoogle ScholarPubMed
Kloosterman, A., Parmentier, H. K. and Ploeger, H. W. (1992). Breeding cattle and sheep for resistance to gastrointestinal nematodes. Parasitology Today 8, 330–335.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.Google Scholar
Liu, S. K. (1966). Genetic influence on resistance of mice to Nematospiroides dubius. Experimental Parasitology 18, 311–319.CrossRefGoogle Scholar
Mähler, M., Most, C., Schmidtke, S., Sundberg, J. P., Li, R., Hedrich, H. J. and Churchill, G. A. (2002). Genetics of colitis susceptibility in IL-10 deficient mice. Genomics 80, 274–282.CrossRefGoogle ScholarPubMed
McCoy, K. D., Stoel, M., Stettler, R., Merky, P., Fink, P., Senn, B. M., Schaer, C., Massacand, J., Odermatt, B., Oettgen, H. C., Zinkernagel, R. M., Bos, N. A., Hengartner, H., MacPherson, A. J. and Harris, N. L. (2008). Polyclonal and specific antibodies mediate protective immunity against enteric helminth infection. Cell Host Microbe 4, 362–373.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
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
Pritchard, D. I., Williams, D. J. L., Behnke, J. M. and Lee, T. D. G. (1983). The role of IgG1 hypergammaglobulinaemia in immunity to the gastrointestinal nematode Nematospiroides dubius. The immunochemical purification, antigen-specificity and in vivo anti-parasite effect of IgG1 from immune serum. Immunology 49, 353–365.Google Scholar
Spurlock, G. M. (1943). Observations on host-parasite relations between laboratory mice and Nematospiroides dubius. Journal of Parasitology 29, 303–311.Google Scholar
Stear, M. J., Doligalska, M. and Donskow-Schmelter, K. (2007). Alternatives to anthelmintics for the control of nematodes in livestock. Parasitology 134, 139–151.Google Scholar
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
Wahid, F. N. and Behnke, J. M. (1993). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): parasite specific IgG1 antibody responses and primary response phenotype. Parasite Immunology 15, 401–413.Google Scholar
Waller, P. J. (2006). From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Veterinary Parasitology 139, 1–14.Google Scholar
Wang, J., Van Praagh, A., Hamilton, E., Wang, Q., Zou, B., Muranjan, M., Murphy, N. B. and Black, S. J. (2002). Serum xanthine oxidase: origin, regulation, and contribution to control of trypanosome parasitemia. Antioxid Redox Signal 4, 161–178.Google Scholar
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