Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-24T06:21:10.571Z Has data issue: false hasContentIssue false

Major Histocompatibility Complex DRB1 gene: its role in nematode resistance in Suffolk and Texel sheep breeds

Published online by Cambridge University Press:  08 June 2005

G. SAYERS
Affiliation:
Department of Animal Husbandry and Production, Faculty of Veterinary Medicine, UCD, Dublin 4
B. GOOD
Affiliation:
Teagasc, Sheep Research Centre, Athenry, Co. Galway
J. P. HANRAHAN
Affiliation:
Teagasc, Sheep Research Centre, Athenry, Co. Galway
M. RYAN
Affiliation:
Department of Animal Husbandry and Production, Faculty of Veterinary Medicine, UCD, Dublin 4
J. M. ANGLES
Affiliation:
Small Animal Clinical Studies, Faculty of Veterinary Medicine, UCD, Dublin 4
T. SWEENEY
Affiliation:
Department of Animal Husbandry and Production, Faculty of Veterinary Medicine, UCD, Dublin 4

Abstract

A potential control strategy for nematode infection in sheep is the implementation of a breeding programme to select for genes associated with resistance. The Texel breed is more resistant to gastrointestinal nematode infection than the Suffolk breed, based on faecal egg count, and this difference should enable the identification of some of the genes responsible for resistance. The objective of this study was to determine if variation at the ovine MHC-DRB1 locus was associated with variation in faecal egg count in Suffolk and Texel sheep. Ovar-DRB1 alleles and faecal egg count were determined for Texel (n=105) and Suffolk (n=71) lambs. Eight Ovar-DRB1 alleles, including 1 previously unknown allele, were identified in the Texel breed by sequence-base-typing. Seven Ovar-DRB1 alleles were identified in the Suffolk breed. Two Ovar-DRB1 alleles were common to both breeds, but were among the least frequent in the Suffolk population. In the Suffolk breed 1 Ovar-DRB1 allele was associated with a decrease in faecal egg count and 2 alleles with an increase in faecal egg count. This locus accounted for 14% of the natural variation in faecal egg count in Suffolks. There was no evidence for an association between Ovar-DRB1 alleles and faecal egg count in the Texel breed and the Ovar-DRB1 locus accounted for only 3% of the phenotypic variation in faecal egg count. These results suggest that the Ovar-DRB1 gene plays an important role in resistance to nematode infection in the Suffolk breed. The difference in faecal egg counts between these breeds may be attributable in part to the different allele profile at the Ovar-DRB1 locus.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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

Andrews, S. J., Hole, N. J. K., Munn, E. A. and Rolph, T. P. ( 1995). Vaccination of sheep against haemonchosis with H11, a gut membrane-derived protective antigen from the adult parasite: prevention of the periparturient rise and colostral transfer of protective immunity. International Journal for Parasitology 25, 839846.CrossRefGoogle Scholar
Andrews, S. J., Rolph, T. P. and Munn, E. A. ( 1997). Duration of protective immunity against ovine haemonchosis following vaccination with the nematode gut membrane antigen H11. Research in Veterinary Science 62, 223227.CrossRefGoogle Scholar
Bird, J., Shulaw, W. P., Pope, W. F. and Bremer, C. A. ( 2001). Control of anthelmintic resistant endoparasites in a commercial sheep flock through parasite community replacement. Veterinary Parasitology 97, 219225.CrossRefGoogle Scholar
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, 255269.CrossRefGoogle Scholar
Blattman, A. N., Hulme, D. J., Kinghorn, B. P., Woolaston, R. R., Gray, G. D. and Beh, K. J. ( 1993). A search for associations between major histocompatibility complex restriction fragment length polymorphism bands and resistance to Haemonchus contortus infection in sheep. Animal Genetics 24, 277282.CrossRefGoogle Scholar
Buitkamp, J., Filmether, P., Stear, M. J. and 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, 693696.CrossRefGoogle Scholar
Coop, R. L. and Kyriazakis, I. ( 2001). Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325330.CrossRefGoogle Scholar
Coppin, H. L., Carmichael, P., Lombardi, G., L'faqihi, F. E., Salter, R., Parham, P., Lechler, R. I. and de Preval, C. ( 1993). Position 71 in the alpha helix of the DR beta domain is predicted to influence peptide binding and plays a central role in allorecognition. European Journal for Immunology 23, 343349.CrossRefGoogle Scholar
Datta, F. U., Nolan, J. V., Rowe, J. B., Gray, G. D. and Crook, B. J. ( 1999). Long-term effects of short-term provision of protein-enriched diets on resistance to nematode infection and live-weight gain and wool growth in sheep. International. Journal for Parasitology 29, 479488.CrossRefGoogle Scholar
Eady, S. J., Woolaston, R. R. and Barger, I. A. ( 2003). Comparison of genetic and nongenetic strategies for control of gastrointestinal nematodes of sheep. Livestock Production Science 81, 1123.CrossRefGoogle Scholar
Githigia, S. M., Thamsborg, S. M., Larsen, M., Kyvsgaard, N. C. and Nansen, P. ( 1997). The preventative effect of the fungus Duddingtonia flagrans on trichostrongyle infections of lambs on pasture. International Journal for Parasitology 27, 931939.CrossRefGoogle Scholar
Good, B., Hanrahan, J. P., Crowley, B. A. and Mulcahy, G. ( 2004). Texel sheep are more resistant than Suffolks to natural helminth challenge based on faecal egg count and nematode burden. Manuscript submitted to Parasitology.
Grain, F., Nain, M.-C., Labonne, M.-P., Lantier, F., Lechopier, P., Gebuhrer, L., Asso, J., Maddox, J. and Betuel, H. ( 1993). Restriction fragment length polymorphism of DQB and DRB class II genes of the ovine major histocompatibility complex. Animal Genetics 24, 377384.CrossRefGoogle Scholar
Groeneveld, E. ( 1990). PEST User's Manual, Version 3.1.
Hanrahan, J. P. and Crowley, B. A. ( 1999). Evidence for breed differences in resistance to nematode parasitism. Sheep and Goat Commission of European Association for Animal Production (50th Annual Meeting) Session IV, 4 pp.
Hulme, D. J., Windon, R. G., Nicholas, F. W. and Beh, K. J. ( 1991). Association between MHC Class II RFLP and Trichostrongylus resistance. In Breeding for Disease Resistance in Sheep (ed. Gray, G. D. & Woolaston, R. R.), pp. 115120. Australian Wool Corporation, Melbourne.
Kahn, L. P., Knox, M. R., Gray, G. D., Lea, J. M. and Walkden-Brown, S. W. ( 2003). Enhancing immunity to parasites in single-bearing Merino ewes through nutrition and genetic selection. Veterinary Parasitology 112, 211225.CrossRefGoogle Scholar
Knox, D. P., Redmond, D. L., Newlands, G. F., Skuce, P. J., Pettit, D. and Smith, W. D. ( 2003). The nature and prospects for gut membrane proteins as vaccine candidates for Haemonchus contortus and other ruminant trichotrongyloids. International Journal for Parasitology 33, 11291137.CrossRefGoogle Scholar
Konnai, S., Nagaoka, Y., Takesima, S., Onuma, M. and Aida, Y. ( 2003 a). Sequences and diversity of 17 new Ovar-DRB1 alleles from three breeds of sheep. European Journal for Immunogenetics 30, 275282.Google Scholar
Konnai, S., Nagaoka, Y., Takesima, S., Onuma, M. and Aida, Y. ( 2003 b). Technical note: DNA typing for ovine MHC DRB1 using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP). Journal of Dairy Science 86, 33623365.Google Scholar
Kostia, S., Kantanen, J., Kolkkala, M. and Varvio, S. L. ( 1998). Applicability of SSCP analysis for MHC genotyping: fingerprinting of Ovar-DRB1 exon 2 alleles from Finnish and Russian breeds. Animal Genetics 29, 453455.CrossRefGoogle Scholar
Krieger, J. I., Karr, R. W., Grey, M., Yu, W.-Y., O'Sullivan, D., Batovsky, L., Zheng, Z.-L., Colon, S. M., Gaeta, F. C. A., Sidney, J., Albertson, M., Del Guercio, M.-F., Chesnut, R. W. and Sette, A. ( 1991). Single amino acid changes in DR and antigen define residues critical for peptide-MHC binding and T cell recognition. Journal of Immunology 146, 23312340.Google Scholar
Larsen, M., Faedo, M., Waller, P. J. and Hennessy, D. R. ( 1998). The potential of nematophagous fungi to control the free-living stages of nematode parasites of sheep: Studies with Duddingtonia flagrans. Veterinary Parasitology 76, 121128.CrossRefGoogle Scholar
MINISTRY OF AGRICULTURE, FISHERIES AND FOOD ( 1986) Manual of Veterinary Parasitological Laboratory Techniques, 3rd Edn.
Niezen, J. H., Robertson, H. A., Waghorn, G. C. and Charleston, W. A. ( 1998). Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 1527.CrossRefGoogle Scholar
Outteridge, P. M., Andersson, L., Douch, P. G., Green, R. S., Gwakisa, P. S., Hohenhaus, M. A. and Mikko, S. ( 1996). The PCR typing of MHC-DRB genes in the sheep using primers for an intronic microsatellite: application to nematode parasite resistance. Immunology and Cell Biology 74, 330336.CrossRefGoogle Scholar
Pena, M. T., Miller, J. E., Fontenot, M. E., Gillespie, A. and Larsen, M. ( 2002). Evaluation of Duddingtonia flagrans in reducing infective larvae of Haemonchus contortus in faeces of sheep. Veterinary Parasitology 103, 259265.CrossRefGoogle Scholar
SAS ( 1989). SAS/STAT User's Guide, Version 6, Fourth Edition, Vol. 2. SAS Institute Inc., Cary, NC, USA.
Sauermann, U., Stahl-Hennig, C., Stolte, N., Muhl, T., Krawczak, M., Spring, M., Fuchs, D., Kaup, F. J., Hunsmann, G. and Sopper, S. ( 2000). Homozygosity for a conserved MHC class II DQ-DRB haplotype is associated with rapid disease progression in simian immunodeficiency virus-infected macaques: results from a prospective study. Journal of Infectious Diseases 182, 716724.CrossRefGoogle Scholar
Schwaiger, F.-W., Buitkamp, J., Weyers, E. and Epplen, J. T. ( 1993). Typing of the artiodactyl MHC-DRB genes with the help of intronic simple repeated DNA sequences. Molecular Ecology 2, 5559.CrossRefGoogle Scholar
Schwaiger, F.-W., Gostomski, D., Stear, M. J., Duncan, J. L., McKellar, Q. A., Epplen, J. T. and Buitkamp, J. ( 1995). An ovine major histocompatibility complex DRB1 allele is associated with low faecal egg counts following natural, predominantly Ostertagia circumcincta infection. International Journal for Parasitology 25, 815822.CrossRefGoogle Scholar
Stear, M. J., Bairden, K., Bishop, S. C., Buitkamp, J., Epplen, J. T., Gostomski, D., McKellar, A. Q., Schwaiger, F.-W. and 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, 423428.CrossRefGoogle Scholar
Steel, R. G. D. and Torrie, J. H. ( 1960). Principles and Procedures of Statistics. McGraw-Hill Book Company Inc., New York.
Stern, L. J., Brown, J. H., Jardetzky, T. S., Gorga, J. C., Urban, R. G., Strominger, J. L. and Wiley, D. C. ( 1994). Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature, London 368, 215221.CrossRefGoogle Scholar
Thorsby, E. ( 1999). MHC structure and function. Transplantation Proceedings 31, 713716.CrossRefGoogle Scholar
Thursz, M. R., Thomas, H. C., Greenwood, B. M. and Hill, A. V. ( 1997). Heterozygote advantage for HLA class-II type in hepatitis B virus infection. Nature Genetics 17, 1112.CrossRefGoogle Scholar
Walling, G. A., Wilson, A. D., McTeir, T. L. and Bishop, S. C. ( 2004). Increased heterozygosity and allelic variants are seen in Texels compared to Suffolk sheep. Heredity 92, 102109.CrossRefGoogle Scholar