Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine
Genomic imprinting is theorized to exist in all placental mammals and some marsupials; however, extensive comparative analysis of animals aside from humans and mice remains incomplete. Here we report conservation of genomic imprinting in the bovine at the X chromosome inactivation–specific transcript (XIST), insulin-like growth factor 2 (IGF2), and gene trap locus 2 (GTL2) loci. Coding single nucleotide polymorphisms (SNPs) between Bos gaurus and Bos taurus were detected at the XIST, IGF2, and GTL2 loci, which have previously been identified as imprinted in either humans, mice, or sheep. Expression patterns of parental alleles in F1 hybrids indicated preferential paternal expression at the XIST locus solely in the chorion of females, whereas analysis of the IGF2 and GTL2 loci indicated preferential paternal and maternal expression of alleles, respectively, in both fetal and placental tissues. Comparative sequence analysis of the XIST locus and adjacent regions suggests that repression of the maternal allele in the bovine is controlled by a different mechanism than in mice, further reinforcing the importance of comparative analysis of imprinting.
KeywordsImprint Gene Comparative Sequence Analysis Allelic Expression Xist Gene Xist Locus
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
We thank Gary Hansen and members of Dr. Piedrahita’s laboratory for assistance with generating and maintenance of the experimental cattle. This research was supported by NIH grant HL51587 and a Texas A&M University, College of Veterinary Medicine Signature grant.
Allen, ND, Logan, K, Lally, G, Drage, DJ, Norris, ML, et al. 1995Distribution of parthenogenetic cells in the mouse brain and their influence on brain development and behaviorProc Natl Acad Sci USA921078210786Google Scholar Bidwell, CA, Shay, TL, Georges, M, Beever, JE, Berghmans, S, et al. 2001Differential expression of the GTL2 gene within the callipyge region of ovine chromosome 18Anim Genet32248256CrossRefGoogle Scholar Charlier, C, Segers, K, Wagenaar, D, Karim, L, Berghmans, S, et al. 2001Human–ovine comparative sequencing of a 250-kb imprinted domain encompassing the callipyge (clpg) locus and identification of six imprinted transcripts: DLK1, DAT, GTL2, PEG11, antiPEG11, and MEG8Genome Res11850860CrossRefPubMedGoogle Scholar Chureau, C, Prissette, M, Bourdet, A, Barbe, V, Cattolico, L, et al. 2002Comparative sequence analysis of the X-inactivation center region in mouse, human, and bovineGenome Res12894908PubMedGoogle Scholar Constancia, M, Pickard, B, Kelsey, G, Reik, W 1998Imprinting mechanismsGenome Res8881900Google Scholar Csankovszki, G, Nagy, A, Jaenisch, R 2001Synergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivationJ Cell Biol153773784CrossRefGoogle Scholar Dawson, WD 1971Postnatal development in Peromyscus maniculatus-polionotus hybrids. II. Tail and hind foot growthGrowth35359367Google Scholar Falls, JG, Pulford, DJ, Wylie, AA, Jirtle, RL 1999Genomic imprinting, implications for human diseaseAm J Pathol154635647Google Scholar Feil, R, Khosla, S, Cappai, P, Loi, P 1998Genomic imprinting in ruminants: allele specific gene expression in parthenogenetic sheepMamm Genome9831834CrossRefGoogle Scholar Gallagher, DS,Jr, Yang, YP, Burzlaff, JD, Womack, JE, Stelly, DM, et al. 1998Physical assignment of six type I anchor loci to bovine chromosome 19 by fluorescence in situ hybridizationAnim Genet29130134CrossRefGoogle Scholar Gao, Q, Womack, JE 1997A genetic map of bovine chromosome 7 with an interspecific hybrid backcross panelMamm Genome8258261CrossRefGoogle Scholar Graves, JA 1996Mammals that break the rules: genetics of marsupials and monotremesAnnu Rev Genet30233260CrossRefGoogle Scholar Hagemann, LJ, Peterson, AJ, Weilert, LL, Lee, RS, Tervit, HR 1998In vitro and early in vivo development of sheep gynogenomes and putative androgenonesMol Reprod Dev50154162CrossRefGoogle Scholar Hemberger, M, Redies, C, Krause, R, Oswald, J, Walter, J, et al. 1998H19 and Igf2 are expressed and differentially imprinted in neuroectoderm-derived cells in the mouse brainDev Genes Evol208393402CrossRefGoogle Scholar Hemberger, MC, Pearsall, RS, Zechner, U, Orth, A, Otto, S, et al. 1999Genetic dissection of X-linked interspecific hybrid placental dysplasia in congenic mouse strainsGenetics153383390PubMedGoogle Scholar Huntriss, J, Lorenzi, R, Purewal, A, Monk, M 1997A methylation-dependent DNA-binding activity recognising the methylated promoter region of the mouse Xist geneBiochem Biophys Res Commun235730738CrossRefGoogle Scholar Jeon, JT, Carlborg, O, Tornsten, A, Giuffra, E, Amarger, V, et al. 1999A paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locusNat Genet21157158CrossRefGoogle Scholar Jong, MT, Carey, AH, Caldwell, KA, Lau, MH, Handel, MA, et al. 1999Imprinting of a RING zinc-finger encoding gene in the mouse chromosome region homologous to the Prader–Willi syndrome genetic regionHum Mol Genet8795803CrossRefGoogle Scholar Killian, JK, Byrd, JC, Jirtle, JV, Munday, BL, Stoskopf, MK, et al. 2000M6P/IGF2R imprinting evolution in mammalsMol cell5707716CrossRefGoogle Scholar Killian, JK, Nolan, CM, Wylie, AA, Li, T, Vu, TH, et al. 2001Divergent evolution m M6P/IGF2R imprinting from the Jurassic to the QuaternaryHum Mol Genet1017211728CrossRefPubMedGoogle Scholar Mayer, W, Hemberger, M, Frank, HG, Grummer, R, Winterhager, E, et al. 2000Expression of the imprinted genes MEST/Mest in human and murine placenta suggests a role in angiogenesisDev Dyn217110CrossRefGoogle Scholar McLaren, RJ, Montgomery, GW 1999Genomic imprinting of the insulin-like growth factor 2 gene in sheepMamm Genome10588591CrossRefGoogle Scholar Migeon, BR 2003Is Tsix repression of Xist specific to mouse?Nat Genet33337338CrossRefGoogle Scholar Migeon, BR, Chowdhury, AK, Dunston, JA, McIntosh, I 2001Identification of TSIX, encoding an RNA antisense to human XIST, reveals differences from its murine counterpart: implications for X inactivationAm J Hum Genet69951960CrossRefGoogle Scholar Migeon, BR, Lee, CH, Chowdhury, AK, Carpenter, H 2002Species differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivationAm J Hum Genet71286293CrossRefPubMedGoogle Scholar Nezer, C, Moreau, L, Brouwers, B, Coppieters, W, Detilleux, J, et al. 1999An imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigsNat Genet21155156CrossRefPubMedGoogle Scholar Nolan, CM, Killian, JK, Petitte, JN, Jirtle, RL 2001Imprint status of M6P/IGF2R and IGF2 in chickensDev Genes Evol211179183CrossRefGoogle Scholar Pham, NV, Nguyen, MT, Hu, JF, Vu, TH, Hoffman, AR 1998Dissociation of IGF2 and H19 imprinting in human brainBrain Res81018CrossRefGoogle Scholar Reik, W, Davies, K, Dean, W, Kelsey, G, Constancia, M 2001Imprinted genes and the coordination of fetal and postnatal growth in mammalsNovartis Found Symp2371931Google Scholar Reik, W, Constancia, A, Fowden, M, Anderson, N, Dean, W 2003Regulation of supply and demand for maternal nutrients in mammals by imprinted genesJ Physiol5473544Google Scholar Schmidt, JV, Matteson, PG, Jones, BK, Guan, XJ, Tilghman, S 2000The Dlk1 and Gtl2 genes are linked and reciprocally imprintedGenes Dev1419972002PubMedGoogle Scholar Schwartz, S, Zhang, Z, Frazer, KA, Smit, A, Riemer, C, et al. 2000PipMaker—a web server for aligning two genomic DNA sequencesGenome Res10577586CrossRefPubMedGoogle Scholar Shay, TL, Berghmans, S, Segers, K, Meyers, S, Beever, JE, et al. 2001Fine-mapping and construction of a bovine contig spanning the ovine callipyge locusMamm Genome12141149CrossRefGoogle Scholar Short, RV 1997An introduction to mammalian interspecific hybridsJ Hered88355357Google Scholar Surani, MA 2001Reprogramming of genome function through epigenetic inheritanceNature414122128CrossRefPubMedGoogle Scholar Villar, AJ, Eddy, EM, Pedersen, RA 1995Developmental regulation of genomic imprinting during gametogenesisDev Biol172264271CrossRefGoogle Scholar Villar, AJ, Pedersen, RA 1997Interspecies approaches for the analysis of parental imprinting during mouse developmentJ Hered88401407Google Scholar Vrana, PB, Guan, XJ, Ingram, RS, Tilghman, SM 1998Genomic imprinting is disrupted in interspecific Peromyscus hybridsNat Genet20362365CrossRefGoogle Scholar Vrana, PB, Fossella, JA, Matteson, P, Rio, T, O’Neill, MJ, et al. 2000Genetic and epigenetic incompatibilities underlie hybrid dysgenesis in PeromyscusNat Genet25120124CrossRefGoogle Scholar Wylie, AA, Murphy, SK, Orton, TC, Jirtle, RL 2000Novel imprinted DLK1/GTL2 domain on human chromosome 14 contains motifs that mimic those implicated in IGF2/H19 regulationGenome Res1017111718CrossRefPubMedGoogle Scholar Xue, F, Tian, XC, Du, F, Kubota, C, Taneja, M, et al. 2002Aberrant patterns of X chromosome inactivation in bovine clonesNat Genet31216266CrossRefGoogle Scholar Yang, YP, Womack, JE 1997Construction of a bovine chromosome 19 linkage map with an interspecies hybrid backcrossMamm Genome8262266CrossRefGoogle Scholar Yevtodiyenko, A, Carr, MS, Patel, N, Schmidt, Jt 2002Analysis of candidate imprinted genes linked to Dlk1-Gtl2 using a congenic mouse lineMamm Genome13633638CrossRefGoogle Scholar Young, LE, Fernandes, K, McEvoy, TG, Butterwith, SC, Gutierrez, CG, et al. 2001Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo cultureNat Genet27153154CrossRefGoogle Scholar Zechner, U, Hemberger, M, Constancia, M, Orth, A, Dragatsis, I, et al. 2002Proliferation and growth factor expression in abnormally enlarged placentas of mouse interspecific hybridsDev Dyn224125134CrossRefGoogle Scholar
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