Abstract
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.
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References
ND Allen K Logan G Lally DJ Drage ML Norris et al. (1995) ArticleTitleDistribution of parthenogenetic cells in the mouse brain and their influence on brain development and behavior Proc Natl Acad Sci USA 92 10782–10786
CA Bidwell TL Shay M Georges JE Beever S Berghmans et al. (2001) ArticleTitleDifferential expression of the GTL2 gene within the callipyge region of ovine chromosome 18 Anim Genet 32 248–256 Occurrence Handle10.1046/j.1365-2052.2001.00776.x
C Charlier K Segers D Wagenaar L Karim S Berghmans et al. (2001) ArticleTitleHuman–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 MEG8 Genome Res 11 850–860 Occurrence Handle10.1101/gr.172701 Occurrence Handle1:CAS:528:DC%2BD3MXjs1Wmu78%3D Occurrence Handle11337479
C Chureau M Prissette A Bourdet V Barbe L Cattolico et al. (2002) ArticleTitleComparative sequence analysis of the X-inactivation center region in mouse, human, and bovine Genome Res 12 894–908 Occurrence Handle1:CAS:528:DC%2BD38Xks12hsrs%3D Occurrence Handle12045143
M Constancia B Pickard G Kelsey W Reik (1998) ArticleTitleImprinting mechanisms Genome Res 8 881–900
G Csankovszki A Nagy R Jaenisch (2001) ArticleTitleSynergism of Xist RNA, DNA methylation, and histone hypoacetylation in maintaining X chromosome inactivation J Cell Biol 153 773–784 Occurrence Handle10.1083/jcb.153.4.773
WD Dawson (1971) ArticleTitlePostnatal development in Peromyscus maniculatus-polionotus hybrids. II. Tail and hind foot growth Growth 35 359–367
JG Falls DJ Pulford AA Wylie RL Jirtle (1999) ArticleTitleGenomic imprinting, implications for human disease Am J Pathol 154 635–647
R Feil S Khosla P Cappai P Loi (1998) ArticleTitleGenomic imprinting in ruminants: allele specific gene expression in parthenogenetic sheep Mamm Genome 9 831–834 Occurrence Handle10.1007/s003359900876
DS Gallagher SuffixJr YP Yang JD Burzlaff JE Womack DM Stelly et al. (1998) ArticleTitlePhysical assignment of six type I anchor loci to bovine chromosome 19 by fluorescence in situ hybridization Anim Genet 29 130–134 Occurrence Handle10.1046/j.1365-2052.1998.00239.x
Q Gao JE Womack (1997) ArticleTitleA genetic map of bovine chromosome 7 with an interspecific hybrid backcross panel Mamm Genome 8 258–261 Occurrence Handle10.1007/s003359900405
JA Graves (1996) ArticleTitleMammals that break the rules: genetics of marsupials and monotremes Annu Rev Genet 30 233–260 Occurrence Handle10.1146/annurev.genet.30.1.233
LJ Hagemann AJ Peterson LL Weilert RS Lee HR Tervit (1998) ArticleTitleIn vitro and early in vivo development of sheep gynogenomes and putative androgenones Mol Reprod Dev 50 154–162 Occurrence Handle10.1002/(SICI)1098-2795(199806)50:2<154::AID-MRD5>3.0.CO;2-J
M Hemberger C Redies R Krause J Oswald J Walter et al. (1998) ArticleTitleH19 and Igf2 are expressed and differentially imprinted in neuroectoderm-derived cells in the mouse brain Dev Genes Evol 208 393–402 Occurrence Handle10.1007/s004270050195
MC Hemberger RS Pearsall U Zechner A Orth S Otto et al. (1999) ArticleTitleGenetic dissection of X-linked interspecific hybrid placental dysplasia in congenic mouse strains Genetics 153 383–390 Occurrence Handle1:CAS:528:DyaK1MXmsVWqtbc%3D Occurrence Handle10471720
J Huntriss R Lorenzi A Purewal M Monk (1997) ArticleTitleA methylation-dependent DNA-binding activity recognising the methylated promoter region of the mouse Xist gene Biochem Biophys Res Commun 235 730–738 Occurrence Handle10.1006/bbrc.1997.6876
JT Jeon O Carlborg A Tornsten E Giuffra V Amarger et al. (1999) ArticleTitleA paternally expressed QTL affecting skeletal and cardiac muscle mass in pigs maps to the IGF2 locus Nat Genet 21 157–158 Occurrence Handle10.1038/5938
MT Jong AH Carey KA Caldwell MH Lau MA Handel et al. (1999) ArticleTitleImprinting of a RING zinc-finger encoding gene in the mouse chromosome region homologous to the Prader–Willi syndrome genetic region Hum Mol Genet 8 795–803 Occurrence Handle10.1093/hmg/8.5.795
JK Killian JC Byrd JV Jirtle BL Munday MK Stoskopf et al. (2000) ArticleTitleM6P/IGF2R imprinting evolution in mammals Mol cell 5 707–716 Occurrence Handle10.1016/S1097-2765(00)80249-X
JK Killian CM Nolan AA Wylie T Li TH Vu et al. (2001) ArticleTitleDivergent evolution m M6P/IGF2R imprinting from the Jurassic to the Quaternary Hum Mol Genet 10 1721–1728 Occurrence Handle10.1093/hmg/10.17.1721 Occurrence Handle1:CAS:528:DC%2BD3MXntFCitL0%3D Occurrence Handle11532981
W Mayer M Hemberger HG Frank R Grummer E Winterhager et al. (2000) ArticleTitleExpression of the imprinted genes MEST/Mest in human and murine placenta suggests a role in angiogenesis Dev Dyn 217 1–10 Occurrence Handle10.1002/(SICI)1097-0177(200001)217:1<1::AID-DVDY1>3.0.CO;2-4
RJ McLaren GW Montgomery (1999) ArticleTitleGenomic imprinting of the insulin-like growth factor 2 gene in sheep Mamm Genome 10 588–591 Occurrence Handle10.1007/s003359901050
BR Migeon (2003) ArticleTitleIs Tsix repression of Xist specific to mouse? Nat Genet 33 337–338 Occurrence Handle10.1038/ng0303-337a
BR Migeon AK Chowdhury JA Dunston I McIntosh (2001) ArticleTitleIdentification of TSIX, encoding an RNA antisense to human XIST, reveals differences from its murine counterpart: implications for X inactivation Am J Hum Genet 69 951–960 Occurrence Handle10.1086/324022
BR Migeon CH Lee AK Chowdhury H Carpenter (2002) ArticleTitleSpecies differences in TSIX/Tsix reveal the roles of these genes in X-chromosome inactivation Am J Hum Genet 71 286–293 Occurrence Handle10.1086/341605 Occurrence Handle12023758
C Nezer L Moreau B Brouwers W Coppieters J Detilleux et al. (1999) ArticleTitleAn imprinted QTL with major effect on muscle mass and fat deposition maps to the IGF2 locus in pigs Nat Genet 21 155–156 Occurrence Handle10.1038/5935 Occurrence Handle1:CAS:528:DyaK1MXpsVCltg%3D%3D Occurrence Handle9988262
CM Nolan JK Killian JN Petitte RL Jirtle (2001) ArticleTitleImprint status of M6P/IGF2R and IGF2 in chickens Dev Genes Evol 211 179–183 Occurrence Handle10.1007/s004270000132
NV Pham MT Nguyen JF Hu TH Vu AR Hoffman (1998) ArticleTitleDissociation of IGF2 and H19 imprinting in human brain Brain Res 810 1–8 Occurrence Handle10.1016/S0006-8993(98)00783-5
W Reik K Davies W Dean G Kelsey M Constancia (2001) ArticleTitleImprinted genes and the coordination of fetal and postnatal growth in mammals Novartis Found Symp 237 19–31
W Reik A Constancia M Fowden N Anderson W Dean (2003) ArticleTitleRegulation of supply and demand for maternal nutrients in mammals by imprinted genes J Physiol 547 35–44
JV Schmidt PG Matteson BK Jones XJ Guan S Tilghman (2000) ArticleTitleThe Dlk1 and Gtl2 genes are linked and reciprocally imprinted Genes Dev 14 1997–2002 Occurrence Handle1:CAS:528:DC%2BD3cXmtFShu74%3D Occurrence Handle10950864
S Schwartz Z Zhang KA Frazer A Smit C Riemer et al. (2000) ArticleTitlePipMaker—a web server for aligning two genomic DNA sequences Genome Res 10 577–586 Occurrence Handle10.1101/gr.10.4.577 Occurrence Handle1:CAS:528:DC%2BD3cXjtVKrsLg%3D Occurrence Handle10779500
TL Shay S Berghmans K Segers S Meyers JE Beever et al. (2001) ArticleTitleFine-mapping and construction of a bovine contig spanning the ovine callipyge locus Mamm Genome 12 141–149 Occurrence Handle10.1007/s003350010248
RV Short (1997) ArticleTitleAn introduction to mammalian interspecific hybrids J Hered 88 355–357
MA Surani (2001) ArticleTitleReprogramming of genome function through epigenetic inheritance Nature 414 122–128 Occurrence Handle10.1038/35102186 Occurrence Handle1:CAS:528:DC%2BD3MXot1artLo%3D Occurrence Handle11689958
AJ Villar EM Eddy RA Pedersen (1995) ArticleTitleDevelopmental regulation of genomic imprinting during gametogenesis Dev Biol 172 264–271 Occurrence Handle10.1006/dbio.1995.0021
AJ Villar RA Pedersen (1997) ArticleTitleInterspecies approaches for the analysis of parental imprinting during mouse development J Hered 88 401–407
PB Vrana XJ Guan RS Ingram SM Tilghman (1998) ArticleTitleGenomic imprinting is disrupted in interspecific Peromyscus hybrids Nat Genet 20 362–365 Occurrence Handle10.1038/3833
PB Vrana JA Fossella P Matteson T Rio Particledel MJ O’Neill et al. (2000) ArticleTitleGenetic and epigenetic incompatibilities underlie hybrid dysgenesis in Peromyscus Nat Genet 25 120–124 Occurrence Handle10.1038/75518
AA Wylie SK Murphy TC Orton RL Jirtle (2000) ArticleTitleNovel imprinted DLK1/GTL2 domain on human chromosome 14 contains motifs that mimic those implicated in IGF2/H19 regulation Genome Res 10 1711–1718 Occurrence Handle10.1101/gr.161600 Occurrence Handle1:CAS:528:DC%2BD3cXosVWjtL8%3D Occurrence Handle11076856
F Xue XC Tian F Du C Kubota M Taneja et al. (2002) ArticleTitleAberrant patterns of X chromosome inactivation in bovine clones Nat Genet 31 216–266 Occurrence Handle10.1038/ng900
YP Yang JE Womack (1997) ArticleTitleConstruction of a bovine chromosome 19 linkage map with an interspecies hybrid backcross Mamm Genome 8 262–266 Occurrence Handle10.1007/s003359900406
A Yevtodiyenko MS Carr N Patel Jt Schmidt (2002) ArticleTitleAnalysis of candidate imprinted genes linked to Dlk1-Gtl2 using a congenic mouse line Mamm Genome 13 633–638 Occurrence Handle10.1007/s00335-002-2208-1
LE Young K Fernandes TG McEvoy SC Butterwith CG Gutierrez et al. (2001) ArticleTitleEpigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture Nat Genet 27 153–154 Occurrence Handle10.1038/84769
U Zechner M Hemberger M Constancia A Orth I Dragatsis et al. (2002) ArticleTitleProliferation and growth factor expression in abnormally enlarged placentas of mouse interspecific hybrids Dev Dyn 224 125–134 Occurrence Handle10.1002/dvdy.10094
Acknowledgments
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.
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Dindot, S.V., Kent, K.C., Evers, B. et al. Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine. Mamm Genome 15, 966–974 (2004). https://doi.org/10.1007/s00335-004-2407-z
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DOI: https://doi.org/10.1007/s00335-004-2407-z
Keywords
- Imprint Gene
- Comparative Sequence Analysis
- Allelic Expression
- Xist Gene
- Xist Locus