Abstract
Imprinted genes are preferentially expressed from either the maternally inherited allele or the paternally inherited allele. Most genes known to be imprinted have been identified and studied in the human and the mouse. There is only a small number of reported imprinted genes in cattle, which is probably because of the limited sequence and polymorphism information available for bovine genes. To study the imprinting status of cattle genes and assess their conservation among mammalian species, the expression patterns of COPG2, DCN, and SDHD genes were examined in a total of 128 fetal and adult tissues. Two single nucleotide polymorphisms (SNPs) were identified in COPG2, three SNPs in DCN, and one SNP in SDHD. These polymorphisms were used to distinguish between monoallelic and biallelic expression using a primer extension method and a sequencing-based approach. In all 128 tissues, COPG2, DCN, and SDHD transcripts showed biallelic expression. Other cattle genes examined to date have been found to be imprinted like their known counterparts in human and mouse. This is the first report of genes that are not imprinted in cattle while the corresponding genes in human or mouse are imprinted. Lack of conservation of imprinting among mammals suggests important biological, developmental, and regulatory consequences.
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Badenhop RF, Cherian S, Lord RS, Baysal BE, Taschner PE, et al. (2001) Novel mutations in the SDHD gene in pedigrees with familial carotid body paraganglioma and sensorineural hearing loss Genes Chromosomes Cancer 31: 255–263
Baysal BE, Ferrell RE, Willett–Brozick JE, Lawrence EC, Myssiorek D, et al. (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma Science 287: 848–851
Blagitko N, Mergenthaler S, Schulz U, Wollmann HA, Craigen W, et al. (1999) Human GRB10 is imprinted and expressed from the paternal and maternal allele in a highly tissue- and isoform-specific fashion Hum Mol Genet 9: 1587–1595
Bray NJ, Buckland PR, Owen MJ, O’Donovan MC (2003) Cis-acting variation in the expression of a high proportion of genes in human brain. Hum Genet 113: 149–153
Dindot SV, Kent KC, Evers B, Loskutoff N, Womack J (2004) Conservation of genomic imprinting at the XIST, IGF2, and GTL2 loci in the bovine Mamm Genome 15: 966–974
Gootwine E (2004) Placental hormones and fetal-placental development Anim Reprod Sci 82–83: 551–566
Kaneko–Ishino T, Kohda T, Ishino F (2003) The regulation and biological significance of genomic imprinting in mammals J Biochem 133: 699–711
Khatib H (2004) Imprinting of Nesp55 in cattle Mamm Genome 15: 663–667
Khatib H (2005a) Characterization and analysis of the imprinting status of the ovine SDHD and COPG2 genes Anim Genet 36: 186–188
Khatib H (2005b) Monoallelic expression of the protease inhibitor gene in humans, sheep, and cattle Mamm Genome 16: 50–58
Killian JK, Nolan CM, Wylie AA, Li T, Vu TH, et al. (2001) Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary Hum Mol Genet 10: 1721–1728
Kim J, Bergmann A, Lucas S, Stone R, Stubbs L (2004) Lineage-specific imprinting and evolution of the zinc-finger gene ZIM2 Genomics 84: 47–58
Lawton BR, Sevigny L, Obergfell C, Reznick D, O’Neill RJ, et al. (2005) Allelic expression of IGF2 in live-bearing, matrotrophic fishes Dev Genes Evol 215: 207–212
Lee YJ, Park CW, Hahn Y, Park J, Lee J, et al. (2000) Mit1/Lb9 and Copg2, new members of mouse imprinted genes closely linked to Peg1/Mest(1) FEBS Lett 472: 230–234
Malassine A, Frendo JL, Evain–Brion D (2003) A comparison of placental development and endocrine functions between the human and mouse model Hum Reprod Update 9: 531–539
Milunsky J, DeStefano AL, Huang XL, Baldwin CT, Michels VV, et al. (1997) Familial paragangliomas: linkage to chromosome 11q23 and clinical implications Am J Med Genet 72: 66–70
Mizuno Y, Sotomaru Y, Katsuzawa Y, Kono T, Meguro M, et al. (2002) Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray Biochem Biophys Res Commun 290: 1499–1505
Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war Trends Genet 7: 45–49
Murphy SK, Jirtle RL (2003) Imprinting evolution and the price of silence BioEssays 25: 577–588
Nishimura T, Futami E, Taneichi A, Mori T, Hattori A (2002) Decorin expression during development of bovine skeletal muscle and its role in morphogenesis of the intramuscular connective tissue Cells Tissues Organs 171: 199–214
Norton N, Williams NM, Williams HJ, Spurlock G, Kirov G, et al. (2002) Universal, robust, highly quantitative SNP allele frequency measurement in DNA pools Hum Genet 110: 471–478
Okamura K, Sakaki Y, Ito T (2005) Comparative genomics approach toward critical determinants for the imprinting of an evolutionarily conserved gene impact Biochem Biophys Res Commun 329: 824–830
Reik W, Santos F, Dean W (2003) Mammalian epigenomics: reprogramming the genome for development and therapy Theriogenology 59: 21–32
Ruddock NT, Wilson KJ, Cooney MA, Korfiatis NA, Tecirlioglu RT, et al. (2004) Analysis of imprinted messenger RNA expression during bovine preimplantation development Biol Reprod 70: 1131–1135
Yamasaki K, Hayashida S, Miura K, Masuzaki H, Ishimaru T, et al. (2000) The novel gene, gamma2-COP (COPG2), in the 7q32 imprinted domain escapes genomic imprinting Genomics 68: 330–335
Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW (2002) Allelic variation in human gene expression Science 297: 1143
Young LE, Fairburn HR (2000) Improving the safety of embryo technologies: possible role of genomic imprinting Theriogenology 53: 627–648
Zhang S, Kubota C, Yang L, Zhang Y, Page R, et al. (2004) Genomic imprinting of H19 in naturally reproduced and cloned cattle Biol Reprod 71: 1540–1544
Acknowledgments
This research was supported by Hatch grant No. WIS04736 from the University of Wisconsin– Madison. The author thanks Ms. Valerie Schutzkus and Mr. Ismail Zaitoun for their excellent technical assistance.
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Khatib, H. The COPG2, DCN, and SDHD genes are biallelically expressed in cattle. Mamm Genome 16, 545–552 (2005). https://doi.org/10.1007/s00335-005-0029-8
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DOI: https://doi.org/10.1007/s00335-005-0029-8