Skip to main content

Advertisement

SpringerLink
Log in

SNPs in the bovine IL-10 receptor are associated with somatic cell score in Canadian dairy bulls

  • Published:
Mammalian Genome Aims and scope Submit manuscript

Abstract

Altering the balance between pro- and anti-inflammatory responses can influence an animal’s susceptibility to acute or chronic inflammatory disease; bovine mastitis is no exception. Genetic variation in the form of single nucleotide polymorphisms (SNPs) may alter the function and expression of genes that regulate inflammation, making them important candidates for defining an animal’s risk of developing acute or chronic mastitis. The objective of the present study was to identify SNPs in genes that regulate anti-inflammatory responses and test their association with estimated breeding values (EBVs) for somatic cell score (SCS), a trait highly correlated with the incidence of mastitis. These genes included bovine interleukin-10 (IL-10) and its receptor (IL-10R), and transforming growth factor β1 (TGF-β1) and its receptor (TGF-βR). Sequencing-pooled DNA allowed for the identification of SNPs in IL-10 (n = 2), IL-10Rα (n = 6) and β (n = 2), and TGF-β1 (n = 1). These SNPs were subsequently genotyped in a cohort of Holstein (n = 500), Jersey (n = 83), and Guernsey (n = 50) bulls. Linear regression analysis identified significant SNP effects for IL-10Rα 1185C>T with SCS. Haplotype IL-10Rα AAT showed a significant effect on increasing SCS compared to the most common haplotype. The results presented here indicate that SNPs in IL-10Rα may contribute to variation in the SCS of dairy cattle. Although functional studies are necessary to ascertain whether these SNPs are causal polymorphisms or merely in linkage with the true causal SNP(s), a selection program incorporating these markers could have a beneficial influence on the average SCS and productivity of a dairy herd.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ansari-Mahyari S, Berg P (2008) Combined use of phenotypic and genotypic information in sampling animals for genotyping in detection of quantitative trait loci. J Anim Breed Genet 125:100–109

    Article  PubMed  CAS  Google Scholar 

  • Ashwell MS, Heyen DW, Sonstegard TS, Van Tassell CP, Da Y et al (2004) Detection of quantitative trait loci affecting milk production, health, and reproductive traits in Holstein cattle. J Dairy Sci 87:468–475

    Article  PubMed  CAS  Google Scholar 

  • Bannerman DD, Paape MJ, Chockalingam A (2006) Staphylococcus aureus intramammary infection elicits increased production of transforming growth factor-alpha, beta1, and beta2. Vet Immunol Immunopathol 112:309–315

    Article  PubMed  CAS  Google Scholar 

  • Bannerman DD, Paape MJ, Lee JW, Zhao X, Hope JC et al (2004) Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin Diagn Lab Immunol 11:463–472

    PubMed  Google Scholar 

  • Bingisser RM, Holt PG (2001) Immunomodulating mechanisms in the lower respiratory tract: nitric oxide mediated interactions between alveolar macrophages, epithelial cells, and T-cells. Swiss Med Wkly 131:171–179

    PubMed  CAS  Google Scholar 

  • Bloemhof S, de Jong G, de Haas Y (2008) Genetic parameters for clinical mastitis in the first three lactations of Dutch Holstein cattle. Vet Microbiol 134:165–171

    Article  PubMed  CAS  Google Scholar 

  • Boettcher PJ, Pagnacco G, Stella A (2004) A Monte Carlo approach for estimation of haplotype probabilities in half-sib families. J Dairy Sci 87:4303–4310

    PubMed  CAS  Google Scholar 

  • Brown KL, Cosseau C, Gardy JL, Hancock RE (2007) Complexities of targeting innate immunity to treat infection. Trends Immunol 28:260–266

    Article  PubMed  CAS  Google Scholar 

  • Carlen E, Schneider Mdel P, Strandberg E (2005) Comparison between linear models and survival analysis for genetic evaluation of clinical mastitis in dairy cattle. J Dairy Sci 88:797–803

    Article  PubMed  CAS  Google Scholar 

  • Cartmell T, Ball C, Bristow AF, Mitchell D, Poole S (2003) Endogenous interleukin-10 is required for the defervescence of fever evoked by local lipopolysaccharide-induced and Staphylococcus aureus-induced inflammation in rats. J Physiol 549:653–664

    Article  PubMed  CAS  Google Scholar 

  • Chamary JV, Hurst LD (2005) Evidence for selection on synonymous mutations affecting stability of mRNA secondary structure in mammals. Genome Biol 6:R75

    Article  PubMed  CAS  Google Scholar 

  • Chockalingam A, Paape MJ, Bannerman DD (2005) Increased milk levels of transforming growth factor-alpha, beta1, and beta2 during Escherichia coli-induced mastitis. J Dairy Sci 88:1986–1993

    PubMed  CAS  Google Scholar 

  • de Haas Y, Ouweltjes W, ten Napel J, Windig JJ, de Jong G (2008) Alternative somatic cell count traits as mastitis indicators for genetic selection. J Dairy Sci 91:2501–2511

    Article  PubMed  CAS  Google Scholar 

  • Ding Y, Qin L, Zamarin D, Kotenko SV, Pestka S et al (2001) Differential IL-10R1 expression plays a critical role in IL-10-mediated immune regulation. J Immunol 167:6884–6892

    PubMed  CAS  Google Scholar 

  • Gasche C, Grundtner P, Zwirn P, Reinisch W, Shaw SH et al (2003) Novel variants of the IL-10 receptor 1 affect inhibition of monocyte TNF-alpha production. J Immunol 170:5578–5582

    PubMed  CAS  Google Scholar 

  • Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2006) ASReml user guide release 2.0. VSN International Ltd., Hemel Hempstead, UK

    Google Scholar 

  • Goddard ME, Hayes BJ (2007) Genomic selection. J Anim Breed Genet 124:323–330

    PubMed  CAS  Google Scholar 

  • Graffelman J, Camarena JM (2008) Graphical tests for Hardy-Weinberg equilibrium based on the ternary plot. Hum Hered 65:77–84

    Article  PubMed  Google Scholar 

  • Halasa T, Huijps K, Osteras O, Hogeveen H (2007) Economic effects of bovine mastitis and mastitis management: a review. Vet Q 29:18–31

    PubMed  CAS  Google Scholar 

  • Hillerton JE, Berry EA (2005) Treating mastitis in the cow—a tradition or an archaism. J Appl Microbiol 98:1250–1255

    Article  PubMed  CAS  Google Scholar 

  • Hillerton JE, West JG, Shearn MF (1992) The cost of summer mastitis. Vet Rec 131:315–317

    PubMed  CAS  Google Scholar 

  • Ho AS, Wei SH, Mui AL, Miyajima A, Moore KW (1995) Functional regions of the mouse interleukin-10 receptor cytoplasmic domain. Mol Cell Biol 15:5043–5053

    PubMed  CAS  Google Scholar 

  • Holtsmark M, Heringstad B, Madsen P, Odegard J (2008) Genetic relationship between culling, milk production, fertility, and health traits in Norwegian red cows. J Dairy Sci 91:4006–4012

    Article  PubMed  CAS  Google Scholar 

  • Kauf AC, Rosenbusch RF, Paape MJ, Bannerman DD (2007) Innate immune response to intramammary Mycoplasma bovis infection. J Dairy Sci 90:3336–3348

    Article  PubMed  CAS  Google Scholar 

  • Khatkar MS, Thomson PC, Tammen I, Raadsma HW (2004) Quantitative trait loci mapping in dairy cattle: review and meta-analysis. Genet Sel Evol 36:163–190

    Article  PubMed  CAS  Google Scholar 

  • Kossaibati MA, Esslemont RJ (1997) The costs of production diseases in dairy herds in England. Vet J 154:41–51

    Article  PubMed  CAS  Google Scholar 

  • Krawetz SA, Womble DD (2003) Introduction to bioinformatics: a theoretical and practical approach. Humana Press, Totowa, NJ

    Book  Google Scholar 

  • Lehner T (2008) Special regulatory T cell review: The resurgence of the concept of contrasuppression in immunoregulation. Immunology 123:40–44

    Article  PubMed  CAS  Google Scholar 

  • Lewis SE, Searle SM, Harris N, Gibson M, Lyer V et al (2002) Apollo: a sequence annotation editor. Genome Biol 3:RESEARCH0082

    Google Scholar 

  • MacDermott RP (1996) Alterations of the mucosal immune system in inflammatory bowel disease. J Gastroenterol 31:907–916

    Article  PubMed  CAS  Google Scholar 

  • Malo N, Libiger O, Schork NJ (2008) Accommodating linkage disequilibrium in genetic-association analyses via ridge regression. Am J Hum Genet 82:375–385

    Article  PubMed  CAS  Google Scholar 

  • Medzhitov R, Janeway CA Jr (1997) Innate immunity: impact on the adaptive immune response. Curr Opin Immunol 9:4–9

    Article  PubMed  CAS  Google Scholar 

  • Moore KW, de Waal Malefyt R, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765

    Article  PubMed  CAS  Google Scholar 

  • Oviedo-Boyso J, Valdez-Alarcon JJ, Cajero-Juarez M, Ochoa-Zarzosa A, Lopez-Meza JE et al (2007) Innate immune response of bovine mammary gland to pathogenic bacteria responsible for mastitis. J Infect 54:399–409

    Article  PubMed  Google Scholar 

  • Pant SD, Schenkel FS, Leyva-Baca I, Sharma BS, Karrow NA (2007) Identification of single nucleotide polymorphisms in bovine CARD15 and their associations with health and production traits in Canadian Holsteins. BMC Genomics 8:421

    Article  PubMed  Google Scholar 

  • Pyorala S (2002) New strategies to prevent mastitis. Reprod Domest Anim 37:211–216

    Article  PubMed  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Reents R, Jamrozik J, Schaeffer LR, Dekkers JC (1995) Estimation of genetic parameters for test day records of somatic cell score. J Dairy Sci 78:2847–2857

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Rupp R, Boichard D (1999) Genetic parameters for clinical mastitis, somatic cell score, production, udder type traits, and milking ease in first lactation Holsteins. J Dairy Sci 82:2198–2204

    Article  PubMed  CAS  Google Scholar 

  • Rupp R, Boichard D (2003) Genetics of resistance to mastitis in dairy cattle. Vet Res 34:671–688

    Article  PubMed  Google Scholar 

  • Salomons GS, Bok LA, Struys EA, Pope LL, Darmin PS et al (2007) An intriguing “silent” mutation and a founder effect in antiquitin (ALDH7A1). Ann Neurol 62:414–418

    Article  PubMed  CAS  Google Scholar 

  • Shah JH, Maguire DJ, Munce TB, Cotterill A (2008) Alanine in HI: a silent mutation cries out!. Adv Exp Med Biol 614:145–150

    Article  PubMed  CAS  Google Scholar 

  • Sharma BS, Leyva I, Schenkel F, Karrow NA (2006) Association of toll-like receptor 4 polymorphisms with somatic cell score and lactation persistency in Holstein bulls. J Dairy Sci 89:3626–3635

    Article  PubMed  CAS  Google Scholar 

  • Slinker BK, Glantz SA (1985) Multiple regression for physiological data analysis: the problem of multicollinearity. Am J Physiol 249:R1–R12

    PubMed  CAS  Google Scholar 

  • Tamassia N, Calzetti F, Menestrina N, Rossato M, Bazzoni F et al (2008) Circulating neutrophils of septic patients constitutively express IL-10R1 and are promptly responsive to IL-10. Int Immunol 20:535–541

    Article  PubMed  CAS  Google Scholar 

  • Tuite A, Gros P (2006) The impact of genomics on the analysis of host resistance to infectious disease. Microbes Infect 8:1647–1653

    Article  PubMed  CAS  Google Scholar 

  • Wei SH, Ming-Lum A, Liu Y, Wallach D, Ong CJ et al (2006) Proteasome-mediated proteolysis of the interleukin-10 receptor is important for signal downregulation. J Interferon Cytokine Res 26:281–290

    Article  PubMed  CAS  Google Scholar 

  • Winfrey M, Rott M, Wortman A (1997) Unraveling DNA: molecular biology for the laboratory. Prentice Hall, Upper Saddle River, NJ

    Google Scholar 

  • Zhu Y, Magnusson U, Fossum C, Berg M (2008) Escherichia coli inoculation of porcine mammary glands affects local mRNA expression of Toll-like receptors and regulatory cytokines. Vet Immunol Immunopathol 125:182–189

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We acknowledge the generous funding from the Canadian Dairy Commission, the Natural Science and Engineering Research Council, and represented by the Canadian Bovine Mastitis Research Network: Alberta Milk, Dairy Farmers of New Brunswick, Nova Scotia, Ontario, and Prince Edward Island, Novalait Inc., Dairy Farmers of Canada, Canadian Dairy Network, AAFC, PHAC, Technology PEI Inc., Université de Montréal, and University of Prince Edward Island. We also thank the Semex Alliance for providing semen samples for this study, and Mehdi Sargolzaei and Jalal Fatehi for providing EBVs and pedigree information on the bull population.

Author information

Authors and Affiliations

  1. Department of Animal and Poultry Science, Centre for Genetic Improvement of Livestock, University of Guelph, Guelph, N1G 2W1, ON, Canada

    Chris P. Verschoor, Sameer D. Pant, Flavio S. Schenkel, Bhawani S. Sharma & Niel A. Karrow

Authors
  1. Chris P. Verschoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sameer D. Pant
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Flavio S. Schenkel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bhawani S. Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Niel A. Karrow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Niel A. Karrow.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verschoor, C.P., Pant, S.D., Schenkel, F.S. et al. SNPs in the bovine IL-10 receptor are associated with somatic cell score in Canadian dairy bulls. Mamm Genome 20, 447–454 (2009). https://doi.org/10.1007/s00335-009-9198-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00335-009-9198-1

Keywords

Search

Navigation