Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-05T10:51:07.711Z Has data issue: false hasContentIssue false
  • English
  • Français

Single nucleotide polymorphisms at the imprinted bovine insulin-like growth factor 2 (IGF2) locus are associated with dairy performance in Irish Holstein-Friesian cattle

Published online by Cambridge University Press:  08 September 2010

Erik W Berkowicz ,
David A Magee ,
Klaudia M Sikora ,
Donagh P Berry ,
Dawn J Howard ,
Michael P Mullen ,
Ross D Evans ,
Charles Spillane  and
David E MacHugh
Erik W Berkowicz
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
David A Magee*
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland
Klaudia M Sikora
Affiliation:
Genetics and Biotechnology Laboratory, Department of Biochemistry, University College Cork, Cork, Ireland
Donagh P Berry
Affiliation:
Moorepark Dairy Production Research Centre, Teagasc, Fermoy, Co. Cork, Ireland
Dawn J Howard
Affiliation:
Animal Production Research Centre, Teagasc, Mellows Campus, Athenry, Co. Galway, Ireland
Michael P Mullen
Affiliation:
Animal Production Research Centre, Teagasc, Mellows Campus, Athenry, Co. Galway, Ireland
Ross D Evans
Affiliation:
Irish Cattle Breeding Federation, Highfield House, Bandon, Co. Cork, Ireland
Charles Spillane
Affiliation:
Genetics and Biotechnology Laboratory, Department of Biochemistry, University College Cork, Cork, Ireland
David E MacHugh
Affiliation:
Animal Genomics Laboratory, UCD School of Agriculture, Food Science and Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland UCD Conway Institute of Biomolecular and Biomedical Research, University College Dublin, Dublin 4, Ireland
*
*For correspondence; e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The imprinted insulin-like growth factor 2 gene (IGF2) encodes a fetal mitogenic hormone protein (IGF-II) and has previously been shown to be associated with performance in dairy cattle. In this study we assessed genotype-phenotype associations between four single nucleotide polymorphisms (SNPs) located within the bovine IGF2 locus on chromosome 29 and a range of performance traits related to milk production, animal growth and body size, fertility and progeny survival in 848 progeny-tested Irish Holstein-Friesian sires. Two of the four SNPs (rs42196909 and IGF2.g-3815A>G), which were in strong linkage disequilibrium (r2=0·995), were associated with milk yield (P⩽0·01) and milk protein yield (P⩽0·05); the rs42196901 SNP was also associated (P⩽0·05) with milk fat yield. Associations (P⩽0·05) with milk fat percentage and milk protein percentage were observed at the rs42196901 and IGF2.g-3815A>G SNPs, respectively. The rs42196909 and IGF2.g-3815A>G SNPs were also associated with progeny carcass conformation (P⩽0·05), while an association (P⩽0·01) with progeny carcass weight was observed at the rs42194733 SNP locus. None of the four SNPs were associated with body size, fertility and progeny survival. These findings support previous work which suggests that the IGF2 locus is an important biological regulator of milk production in dairy cattle and add to an accumulating body of research showing that imprinted genes influence many complex performance traits in cattle.

Keywords

Boscattlegenetic imprintingIGF2performance traitssingle nucleotide polymorphism
Type
Research Article
Information
Journal of Dairy Research , Volume 78 , Issue 1 , February 2011 , pp. 1 - 8
Copyright
Copyright © Proprietors of Journal of Dairy Research 2010

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

Akers, RM 2006 Major advances associated with hormone and growth factor regulation of mammary growth and lactation in dairy cows. Journal of Dairy Science 89 1222–1234CrossRefGoogle ScholarPubMed
Ashwell, MS, Heyen, DW, Sonstegard, TS, Van Tassell, CP, Da, Y, VanRaden, PM, Ron, M, Weller, JI & Lewin, HA 2004 Detection of quantitative trait loci affecting milk production, health, and reproductive traits in Holstein cattle. Journal of Dairy Science 87 468–475CrossRefGoogle ScholarPubMed
Bagnicka, E, Siadkowska, E, Strzalkowska, N, Zelazowska, B, Flisikowski, K, Krzyzewski, J & Zwierzchowski, L 2010 Association of polymorphisms in exons 2 and 10 of the insulin-like growth factor 2 (IGF2) gene with milk production traits in Polish Holstein-Friesian cattle. Journal of Dairy Research 77 37–42CrossRefGoogle ScholarPubMed
Barrett, JC, Fry, B, Maller, J & Daly, MJ 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 263–265CrossRefGoogle ScholarPubMed
Bartolomei, MS 2009 Genomic imprinting: employing and avoiding epigenetic processes. Genesand Development 23 2124–2133CrossRefGoogle ScholarPubMed
Bartolomei, MS, Zemel, S & Tilghman, SM 1991 Parental imprinting of the mouse H19 gene. Nature 351 153–155CrossRefGoogle ScholarPubMed
Berry, DP, Kearney, F & Harris, B 2009 Genomic selection in Ireland. In: Proceedings of the Interbull Workshop, Uppsala, SwedenGoogle Scholar
Berry, DP, Shalloo, L, Cromie, AR, Veerkamp, RF, Dillion, P, Amer, PR, Kearney, JF, Evans, RD & Wickham, B 2007 The economic breeding index: a generation on. Technical report to the Irish Cattle Breeding FederationGoogle Scholar
Butterfield, RM 1988 New Concepts of Sheep Growth. Sydney, Australia: Department of Veterinary, Univerisity of SydneyGoogle Scholar
Casas, E, Shackelford, SD, Keele, JW, Koohmaraie, M, Smith, TP & Stone, RT 2003 Detection of quantitative trait loci for growth and carcass composition in cattle. Journal of Animal Science 81 2976–2983CrossRefGoogle ScholarPubMed
Chao, W & D'Amore, PA 2008 IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Reviews 19 111–120CrossRefGoogle ScholarPubMed
Curchoe, C, Zhang, S, Bin, Y, Zhang, X, Yang, L, Feng, D, O'Neill, M & Tian, XC 2005 Promoter-specific expression of the imprinted IGF2 gene in cattle (Bos taurus). Biology of Reproduction 73 1275–1281CrossRefGoogle ScholarPubMed
DeChiara, TM, Robertson, EJ & Efstratiadis, A 1991 Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64 849–859CrossRefGoogle ScholarPubMed
Dindot, SV, Farin, PW, Farin, CE, Romano, J, Walker, S, Long, C & Piedrahita, JA 2004a Epigenetic and genomic imprinting analysis in nuclear transfer derived Bos gaurus/Bos taurus hybrid fetuses. Biology of Reproduction 71 470–478Google Scholar
Dindot, SV, Kent, KC, Evers, B, Loskutoff, N, Womack, J & Piedrahita, JA 2004b Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine. Mammalian Genome 15 966–974CrossRefGoogle ScholarPubMed
Estellé, J, Mercadé, A, Noguera, JL, Perez-Enciso, M, Ovilo, C, Sanchez, A & Folch, JM 2005 Effect of the porcine IGF2-intron3-G3072A substitution in an outbred Large White population and in an Iberian×Landrace cross. Journal of Animal Science 83 2723–2728CrossRefGoogle Scholar
Feil, R 2009 Epigenetic asymmetry in the zygote and mammalian development. International Journal of Developmental Biology 53 191–201Google Scholar
Feil, R, Khosla, S, Cappai, P & Loi, P 1998 Genomic imprinting in ruminants: allele-specific gene expression in parthenogenetic sheep. Mammalian Genome 9 831–834CrossRefGoogle ScholarPubMed
Flisikowski, K, Adamowicz, T, Strabel, T, Jankowski, T, Switonski, M & Zwierzchowski, L 2007 An InDel polymorphism in exon 6 of IGF2 associated with the breeding value of Polish Holstein-Friesian bulls. Biochemical Genetics 45 139–143Google Scholar
Giannoukakis, N, Deal, C, Paquette, J, Goodyer, CG & Polychronakos, C 1993 Parental genomic imprinting of the human IGF2 gene. Nature Genetics 4 98–101CrossRefGoogle ScholarPubMed
Gilmour, AR, Cullis, BR, Welham, SJ & Thompson, R 2009 ASREML Reference Manual. Orange Agricultural Institute, Orange: New South Wales Agriculture.Google Scholar
Goodall, JJ & Schmutz, SM 2003 Linkage mapping of IGF2 on cattle chromosome 29. Animal Genetics 34 313CrossRefGoogle ScholarPubMed
Goodall, JJ & Schmutz, SM 2007 IGF2 gene characterization and association with rib eye area in beef cattle. Animal Genetics 38 154–161CrossRefGoogle ScholarPubMed
Heuven, HC, van Wijk, RH, Dibbits, B, van Kampen, TA, Knol, EF & Bovenhuis, H 2009 Mapping carcass and meat quality QTL on Sus scrofa chromosome 2 in commercial finishing pigs. Genetics Selection Evolution 41 4Google Scholar
Hill, WG & Robertson, A 1968 Linkage disequilibrium in finite populations. Theoretical Applied Genetics 38 226–231Google Scholar
Hou, G, Wang, D, Guan, S, Zeng, H, Huang, X & Ma, Y 2010 Associated analysis of single nucleotide polymorphisms of IGF2 gene's exon 8 with growth traits in Wuzhishan pig. Molecular Biology Reports 37 497–500CrossRefGoogle ScholarPubMed
Hovey, RC, Harris, J, Hadsell, DL, Lee, AV, Ormandy, CJ & Vonderhaar, BK 2003 Local insulin-like growth factor-II mediates prolactin-induced mammary gland development. Molecular Endocrinology 17 460–471CrossRefGoogle ScholarPubMed
Jeon, JT, Carlborg, O, Tornsten, A, Giuffra, E, Amarger, V, Chardon, P, Andersson-Eklund, L, Andersson, K, Hansson, I, Lundstrom, K & Andersson, L 1999 A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locus. Nature Genetics 21 157–158Google Scholar
Jungerius, BJ, van Laere, AS, Te Pas, MF, van Oost, BA, Andersson, L & Groenen, MA 2004 The IGF2-intron3-G3072A substitution explains a major imprinted QTL effect on backfat thickness in a Meishan×European white pig intercross. Genetics Research 84 95–101Google Scholar
Lewontin, RC 1964 The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49 49–67CrossRefGoogle ScholarPubMed
Li, C, Bin, Y, Curchoe, C, Yang, L, Feng, D, Jiang, Q, O'Neill, M, Tian, XC & Zhang, S 2008 Genetic imprinting of H19 and IGF2 in domestic pigs (Sus scrofa). Animal Biotechnology 19 22–27Google ScholarPubMed
Magee, DA, Berkowicz, EW, Sikora, KM, Berry, DP, Park, SDE, Kelly, AK, Sweeney, T, Kenny, DA, Evans, RD, Wickham, BW, Spillane, C & MacHugh, DE 2010 A catalogue of validated single nucleotide polymorphisms in bovine orthologs of mammalian imprinted genes and associations with beef production traits. Animal [Epub ahead of print]Google Scholar
McGrath, J & Solter, D 1984 Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37 179–183CrossRefGoogle ScholarPubMed
McLaren, RJ & Montgomery, GW 1999 Genomic imprinting of the insulin-like growth factor 2 gene in sheep. Mammalian Genome 10 588–591CrossRefGoogle ScholarPubMed
Nezer, C, Moreau, L, Brouwers, B, Coppieters, W, Detilleux, J, Hanset, R, Karim, L, Kvasz, A, Leroy, P & Georges, M 1999 An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs. Nature Genetics 21 155–156CrossRefGoogle Scholar
Nezer, C, Moreau, L, Wagenaar, D & Georges, M 2002 Results of a whole genome scan targeting QTL for growth and carcass traits in a Pietrain×Large White intercross. Genetics Selection Evolution 34 371–387Google Scholar
O'Dell, SD & Day, IN 1998 Insulin-like growth factor II (IGF-II). International Journal of Biochemistry and Cell Biology 30 767–771CrossRefGoogle ScholarPubMed
Oczkowicz, M, Tyra, M, Walinowicz, K, Rozycki, M & Rejduch, B 2009 Known mutation (A3072G) in intron 3 of the IGF2 gene is associated with growth and carcass composition in Polish pig breeds. Journal of Applied Genetics 50 257–259Google Scholar
Prosser, CG, Davis, SR, Farr, VC, Moore, LG & Gluckman, PD 1994 Effects of close-arterial (external pudic) infusion of insulin-like growth factor-II on milk yield and mammary blood flow in lactating goats. Journal of Endocrinology 142 93–99Google Scholar
Rachmilewitz, J, Goshen, R, Ariel, I, Schneider, T, de Groot, N & Hochberg, A 1992 Parental imprinting of the human H19 gene. FEBS Letters 309 25–28Google Scholar
Reik, W, Constancia, M, Dean, W, Davies, K, Bowden, L, Murrell, A, Feil, R, Walter, J & Kelsey, G 2000 Igf2 imprinting in development and disease. International Journal of Developmental Biology 44 145–50Google ScholarPubMed
Rodriguez, S, Gaunt, TR & Day, IN 2007 Molecular genetics of human growth hormone, insulin-like growth factors and their pathways in common disease. Human Genetics 122 1–21Google Scholar
Schmutz, SM & Goodall, JJ 2005 Polymorphism of the IGF2 gene and improving production characteristics of cattle. International Patent Number WO 2005/007881. European Patent OfficeGoogle Scholar
Sherman, EL, Nkrumah, JD, Murdoch, BM, Li, C, Wang, Z, Fu, A & Moore, SS 2008 Polymorphisms and haplotypes in the bovine neuropeptide Y, growth hormone receptor, ghrelin, insulin-like growth factor 2, and uncoupling proteins 2 and 3 genes and their associations with measures of growth, performance, feed efficiency, and carcass merit in beef cattle. Journal of Animal Science 86 1–16Google Scholar
Stinckens, A, Mathur, P, Janssens, S, Bruggeman, V, Onagbesan, OM, Schroyen, M, Spincemaille, G, Decuypere, E, Georges, M & Buys, N 2010 Indirect effect of IGF2 intron3 g.3072G>A mutation on prolificacy in sows. Animal Genetics [Epub ahead of print]A+mutation+on+prolificacy+in+sows.+Animal+Genetics+[Epub+ahead+of+print]>Google Scholar
Stinckens, A, Van den Maagdenberg, K, Luyten, T, Georges, M, De Smet, S & Buys, N 2007 The RYR1 g.1843C>T mutation is associated with the effect of the IGF2 intron3-g.3072G>A mutation on muscle hypertrophy. Animal Genetics 38 67–71Google Scholar
Surani, MA, Barton, SC & Norris, ML 1984 Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308 548–550Google Scholar
Tamura, K, Dudley, J, Nei, M & Kumar, S 2007 MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology of Evolution 24 1596–1599CrossRefGoogle ScholarPubMed
Van Laere, AS, Nguyen, M, Braunschweig, M, Nezer, C, Collette, C, Moreau, L, Archibald, AL, Haley, CS, Buys, N, Tally, M, Andersson, G, Georges, M & Andersson, L 2003 A regulatory mutation in IGF2 causes a major QTL effect on muscle growth in the pig. Nature 425 832–836Google Scholar
Vykoukalova, Z, Knoll, A, Dvorak, J & Cepica, S 2006 New SNPs in the IGF2 gene and association between this gene and backfat thickness and lean meat content in Large White pigs. Journal of Animal Breeding and Genetics 123 204–207Google Scholar
Waters, SM, McCabe, MS, Howard, DJ, Giblin, L, Magee, DA, MacHugh, DE & Berry, DP 2010 Associations between newly discovered polymorphisms in the Bos taurus growth hormone receptor gene and performance traits in Holstein-Friesian dairy cattle. Animal Genetics [Epub ahead of print]Google Scholar
Zhang, S, Kubota, C, Yang, L, Zhang, Y, Page, R, O'Neill, M, Yang, X & Tian, XC 2004 Genomic imprinting of H19 in naturally reproduced and cloned cattle. Biology of Reproduction 71 1540–1544Google Scholar