Molecular Genetics and Genomics

, Volume 287, Issue 8, pp 621–630 | Cite as

A survey of tissue-specific genomic imprinting in mammals

  • Adam R. Prickett
  • Rebecca J. OakeyEmail author


In mammals, most somatic cells contain two copies of each autosomal gene, one inherited from each parent. When a gene is expressed, both parental alleles are usually transcribed. However, a subset of genes is subject to the epigenetic silencing of one of the parental copies by genomic imprinting. In this review, we explore the evidence for variability in genomic imprinting between different tissue and cell types. We also consider why the imprinting of particular genes may be restricted to, or lost in, specific tissues and discuss the potential for high-throughput sequencing technologies in facilitating the characterisation of tissue-specific imprinting and assaying the potentially functional variations in epigenetic marks.


Imprinting Tissue-specific Genome-wide 



We would like to thank Dr Michael Cowley, Dr Reiner Schulz and Siobhan Hughes for their critical reading of this manuscript. We thank our funders the Wellcome Trust (RJO, Grant number 085448/Z/08/Z) and the British Heart Foundation (AP, Grant number FS/08/051/25748) for their support.


  1. Arnaud P, Monk D, Hitchins M, Gordon E, Dean W, Beechey CV, Peters J, Craigen W, Preece M, Stanier P, Moore GE, Kelsey G (2003) Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Hum Mol Genet 12(9):1005–1019PubMedCrossRefGoogle Scholar
  2. Cattanach BM (1986) Parental origin effects in mice. J Embryol Exp Morphol 97(Suppl):137–150PubMedGoogle Scholar
  3. Cattanach BM, Kirk M (1985) Differential activity of maternally and paternally derived chromosome regions in mice. Nature 315:496–498PubMedCrossRefGoogle Scholar
  4. Charalambous M, Smith FM, Bennett WR, Crew TE, Mackenzie F, Ward A (2003) Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc Natl Acad Sci USA 100(14):8292–8297. doi: 10.1073/pnas.15321751001532175100 PubMedCrossRefGoogle Scholar
  5. Charalambous M, Cowley M, Geoghegan F, Smith FM, Radford EJ, Marlow BP, Graham CF, Hurst LD, Ward A (2010) Maternally inherited Grb10 reduces placental size and efficiency. Dev Biol 337(1):1–8. doi: 10.1016/j.ydbio.2009.10.011 PubMedCrossRefGoogle Scholar
  6. Chen M, Wang J, Dickerson KE, Kelleher J, Xie T, Gupta D, Lai EW, Pacak K, Gavrilova O, Weinstein LS (2009) Central nervous system imprinting of the G protein G(s)alpha and its role in metabolic regulation. Cell Metab 9(6):548–555. doi: 10.1016/j.cmet.2009.05.004 PubMedCrossRefGoogle Scholar
  7. Choi JD, Underkoffler LA, Wood AJ, Collins JN, Williams PT, Golden JA, Schuster EF Jr, Loomes KM, Oakey RJ (2005) A novel variant of Inpp 5f is imprinted in brain, and its expression is correlated with differential methylation of an internal CpG island. Mol Cell Biol 25(13):5514–5522. doi: 10.1128/MCB.25.13.5514-5522.2005 PubMedCrossRefGoogle Scholar
  8. Clark L, Wei M, Cattoretti G, Mendelsohn C, Tycko B (2002) The Tnfrh1 (Tnfrsf23) gene is weakly imprinted in several organs and expressed at the trophoblast-decidua interface. BMC Genet 3:11PubMedCrossRefGoogle Scholar
  9. Cooper WN, Constancia M (2010) How genome-wide approaches can be used to unravel the remaining secrets of the imprintome. Brief Funct Genomics 9(4):315–328. doi: 10.1093/bfgp/elq018 PubMedCrossRefGoogle Scholar
  10. Curley JP, Barton S, Surani A, Keverne EB (2004) Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proc Biol Sci 271(1545):1303–1309. doi: 10.1098/rspb.2004.2725 PubMedCrossRefGoogle Scholar
  11. da Rocha ST, Charalambous M, Lin SP, Gutteridge I, Ito Y, Gray D, Dean W, Ferguson-Smith AC (2009) Gene dosage effects of the imprinted delta-like homologue 1 (dlk1/pref1) in development: implications for the evolution of imprinting. PLoS Genet 5(2):e1000392. doi: 10.1371/journal.pgen.1000392 PubMedCrossRefGoogle Scholar
  12. de la Puente A, Hall J, Wu YZ, Leone G, Peters J, Yoon BJ, Soloway P, Plass C (2002) Structural characterization of Rasgrf1 and a novel linked imprinted locus. Gene 291(1–2):287–297 pii:S0378111902006017PubMedCrossRefGoogle Scholar
  13. DeChiara TM, Robertson EJ, Efstratiadis A (1991) Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–859PubMedCrossRefGoogle Scholar
  14. Deltour L, Vandamme J, Jouvenot Y, Duvillie B, Kelemen K, Schaerly P, Jami J, Paldi A (2004) Differential expression and imprinting status of Ins1 and Ins2 genes in extraembryonic tissues of laboratory mice. Gene Expr Patterns 5(2):297–300. doi: 10.1016/j.modgep.2004.04.013 PubMedCrossRefGoogle Scholar
  15. Deveale B, van der Kooy D, Babak T (2012) Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS Genet 8(3):e1002600. doi: 10.1371/journal.pgen.1002600 PubMedCrossRefGoogle Scholar
  16. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485(7398):376–380. doi: 10.1038/nature11082 PubMedCrossRefGoogle Scholar
  17. Engemann S, Strodicke M, Paulsen M, Franck O, Reinhardt R, Lane N, Reik W, Walter J (2000) Sequence and functional comparison in the Beckwith–Wiedemann region: implications for a novel imprinting centre and extended imprinting. Hum Mol Genet 9(18):2691–2706PubMedCrossRefGoogle Scholar
  18. Ferron SR, Charalambous M, Radford E, McEwen K, Wildner H, Hind E, Morante-Redolat JM, Laborda J, Guillemot F, Bauer SR, Farinas I, Ferguson-Smith AC (2011) Postnatal loss of Dlk1 imprinting in stem cells and niche astrocytes regulates neurogenesis. Nature 475(7356):381–385. doi: 10.1038/nature10229 PubMedCrossRefGoogle Scholar
  19. Garfield AS, Cowley M, Smith FM, Moorwood K, Stewart-Cox JE, Gilroy K, Baker S, Xia J, Dalley JW, Hurst LD, Wilkinson LS, Isles AR, Ward A (2011) Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature 469(7331):534–538. doi: 10.1038/nature09651 PubMedCrossRefGoogle Scholar
  20. Germain-Lee EL, Ding CL, Deng Z, Crane JL, Saji M, Ringel MD, Levine MA (2002) Paternal imprinting of Galpha(s) in the human thyroid as the basis of TSH resistance in pseudohypoparathyroidism type 1a. Biochem Biophys Res Commun 296(1):67–72. doi: S0006291X02008331 PubMedCrossRefGoogle Scholar
  21. Giddings SJ, King CD, Harman KW, Flood JF, Carnaghi LR (1994) Allele specific inactivation of insulin 1 and 2, in the mouse yolk sac, indicates imprinting. Nat Genet 6(3):310–313. doi: 10.1038/ng0394-310 PubMedCrossRefGoogle Scholar
  22. Gregg C, Zhang J, Butler JE, Haig D, Dulac C (2010a) Sex-specific parent-of-origin allelic expression in the mouse brain. Science 329(5992):682–685. doi: 10.1126/science.1190831 PubMedCrossRefGoogle Scholar
  23. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, Dulac C (2010b) High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329(5992):643–648. doi: 10.1126/science.1190830 PubMedCrossRefGoogle Scholar
  24. Hagiwara Y, Hirai M, Nishiyama K, Kanazawa I, Ueda T, Sakaki Y, Ito T (1997) Screening for imprinted genes by allelic message display: identification of a paternally expressed gene impact on mouse chromosome 18. Proc Natl Acad Sci USA 94(17):9249–9254PubMedCrossRefGoogle Scholar
  25. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM (2000) CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405(6785):486–489. doi: 10.1038/35013106 PubMedCrossRefGoogle Scholar
  26. Hayward BE, Barlier A, Korbonits M, Grossman AB, Jacquet P, Enjalbert A, Bonthron DT (2001) Imprinting of the G(s)alpha gene GNAS1 in the pathogenesis of acromegaly. J Clin Invest 107(6):R31–R36. doi: 10.1172/JCI11887 PubMedCrossRefGoogle Scholar
  27. Hetts SW, Rosen KM, Dikkes P, Villa-Komaroff L, Mozell RL (1997) Expression and imprinting of the insulin-like growth factor II gene in neonatal mouse cerebellum. J Neurosci Res 50(6):958–966. doi: 10.1002/(SICI)1097-4547(19971215)50:6<958:AID-JNR6>3.0.CO;2-C PubMedCrossRefGoogle Scholar
  28. Higashimoto K, Soejima H, Yatsuki H, Joh K, Uchiyama M, Obata Y, Ono R, Wang Y, Xin Z, Zhu X, Masuko S, Ishino F, Hatada I, Jinno Y, Iwasaka T, Katsuki T, Mukai T (2002) Characterization and imprinting status of OBPH1/Obph1 gene: implications for an extended imprinting domain in human and mouse. Genomics 80(6):575–584. doi: S0888754302970060 PubMedCrossRefGoogle Scholar
  29. Hoshiya H, Meguro M, Kashiwagi A, Okita C, Oshimura M (2003) Calcr, a brain-specific imprinted mouse calcitonin receptor gene in the imprinted cluster of the proximal region of chromosome 6. J Hum Genet 48(4):208–211. doi: 10.1007/s10038-003-0006-6 PubMedCrossRefGoogle Scholar
  30. Kashiwagi A, Meguro M, Hoshiya H, Haruta M, Ishino F, Shibahara T, Oshimura M (2003) Predominant maternal expression of the mouse Atp10c in hippocampus and olfactory bulb. J Hum Genet 48(4):194–198. doi: 10.1007/s10038-003-0009-3 PubMedCrossRefGoogle Scholar
  31. Kayashima T, Yamasaki K, Joh K, Yamada T, Ohta T, Yoshiura K, Matsumoto N, Nakane Y, Mukai T, Niikawa N, Kishino T (2003) Atp10a, the mouse ortholog of the human imprinted ATP10A gene, escapes genomic imprinting. Genomics 81(6):644–647. doi: S0888754303000776 PubMedCrossRefGoogle Scholar
  32. Kelsey G, Bartolomei MS (2012) Imprinted genes and the number is? PLoS Genet 8 (3):e1002601. doi: 10.1371/journal.pgen.1002601
  33. Kim J, Bergmann A, Wehri E, Lu X, Stubbs L (2001) Imprinting and evolution of two Kruppel-type zinc-finger genes, ZIM3 and ZNF264, located in the PEG3/USP29 imprinted domain. Genomics 77(1–2):91–98. doi: 10.1006/geno.2001.6621 PubMedCrossRefGoogle Scholar
  34. Kobayashi S, Kohda T, Ichikawa H, Ogura A, Ohki M, Kaneko-Ishino T, Ishino F (2002) Paternal expression of a novel imprinted gene, Peg12/Frat3, in the mouse 7C region homologous to the Prader–Willi syndrome region. Biochem Biophys Res Commun 290(1):403–408. doi: 10.1006/bbrc.2001.6160 PubMedCrossRefGoogle Scholar
  35. Korostowski L, Raval A, Breuer G, Engel N (2011) Enhancer-driven chromatin interactions during development promote escape from silencing by a long non-coding RNA. Epigenetics Chromatin 4:21. doi: 1756-8935-4-2110.1186/1756-8935-4-21 PubMedCrossRefGoogle Scholar
  36. Lee YJ, Park CW, Hahn Y, Park J, Lee J, Yun JH, Hyun B, Chung JH (2000) Mit1/Lb9 and Copg2, new members of mouse imprinted genes closely linked to Peg1/Mest(1). FEBS Lett 472(2–3):230–234. doi: S0014579300014617 PubMedCrossRefGoogle Scholar
  37. Lin SP, Youngson N, Takada S, Seitz H, Reik W, Paulsen M, Cavaille J, Ferguson-Smith AC (2003) Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat Genet 35(1):97–102PubMedCrossRefGoogle Scholar
  38. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM (2006) Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 20(10):1268–1282. doi: 10.1101/gad.1416906 PubMedCrossRefGoogle Scholar
  39. Mantovani G, Ballare E, Giammona E, Beck-Peccoz P, Spada A (2002) The gsalpha gene: predominant maternal origin of transcription in human thyroid gland and gonads. J Clin Endocrinol Metab 87(10):4736–4740PubMedCrossRefGoogle Scholar
  40. McGrath J, Solter D (1984) Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37:179–183PubMedCrossRefGoogle Scholar
  41. Menheniott TR, Woodfine K, Schulz R, Wood AJ, Monk D, Giraud AS, Baldwin HS, Moore GE, Oakey RJ (2008) Genomic imprinting of Dopa decarboxylase in heart and reciprocal allelic expression with neighboring Grb10. Mol Cell Biol 28(1):386–396. doi: 10.1128/MCB.00862-07 PubMedCrossRefGoogle Scholar
  42. Mizuno Y, Sotomaru Y, Katsuzawa Y, Kono T, Meguro M, Oshimura M, Kawai J, Tomaru Y, Kiyosawa H, Nikaido I, Amanuma H, Hayashizaki Y, Okazaki Y (2002) Asb4, Ata3, and Dcn are novel imprinted genes identified by high-throughput screening using RIKEN cDNA microarray. Biochem Biophys Res Commun 290(5):1499–1505. doi: 10.1006/bbrc.2002.6370 PubMedCrossRefGoogle Scholar
  43. Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C (2010) Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development 137(15):2493–2499. doi: 10.1242/dev.048181 PubMedCrossRefGoogle Scholar
  44. Monk D, Wagschal A, Arnaud P, Muller PS, Parker-Katiraee L, Bourc’his D, Scherer SW, Feil R, Stanier P, Moore GE (2008) Comparative analysis of human chromosome 7q21 and mouse proximal chromosome 6 reveals a placental-specific imprinted gene, TFPI2/Tfpi2, which requires EHMT2 and EED for allelic-silencing. Genome Res 18(8):1270–1281. doi: 10.1101/gr.077115.108 PubMedCrossRefGoogle Scholar
  45. Moore T, Haig D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7:45–49PubMedGoogle Scholar
  46. Morison IM, Paton CJ, Cleverley SD (2001) The imprinted gene and parent of origin effect database: Nucleic Acids Res 29:275–276
  47. Murrell A, Heeson S, Reik W (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36(8):889–893. doi: 10.1038/ng1402 PubMedCrossRefGoogle Scholar
  48. Ono R, Shiura H, Aburatani H, Kohda T, Kaneko-Ishino T, Ishino F (2003) Identification of a large novel imprinted gene cluster on mouse proximal chromosome 6. Genome Res 13(7):1696–1705. doi: 10.1101/gr.90680313/7/1696 PubMedCrossRefGoogle Scholar
  49. Paulsen M, Davies KR, Bowden LM, Villar AJ, Franck O, Fuermann M, Dean WL, Moore TF, Rodrigues N, Davies KE, Hu RJ, Feinberg AP, Maher ER, Reik W, Walter J (1998) Syntenic organization of the mouse distal chromosome 7 imprinting cluster and the Beckwith–Wiedemann syndrome region in chromosome 11p15.5. Hum Mol Genet 7 (7):1149–1159. pii:ddb146Google Scholar
  50. Paulsen M, El-Maarri O, Engemann S, Strodicke M, Franck O, Davies K, Reinhardt R, Reik W, Walter J (2000) Sequence conservation and variability of imprinting in the Beckwith–Wiedemann syndrome gene cluster in human and mouse. Hum Mol Genet 9(12):1829–1841PubMedCrossRefGoogle Scholar
  51. Peters J, Williamson CM (2007) Control of imprinting at the Gnas cluster. Epigenetics 2(4):207–213. pii:5380PubMedCrossRefGoogle Scholar
  52. Peters J, Wroe SF, Wells CA, Miller HJ, Bodle D, Beechey CV, Williamson CM, Kelsey G (1999) A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2. Proc Nat Acad Sci 96(7):3830–3835PubMedCrossRefGoogle Scholar
  53. Piras G, El Kharroubi A, Kozlov S, Escalante-Alcalde D, Hernandez L, Copeland NG, Gilbert DJ, Jenkins NA, Stewart CL (2000) Zac1 (Lot1), a potential tumor suppressor gene, and the gene for epsilon-sarcoglycan are maternally imprinted genes: identification by a subtractive screen of novel uniparental fibroblast lines. Mol Cell Biol 20(9):3308–3315PubMedCrossRefGoogle Scholar
  54. Plagge A, Gordon E, Dean W, Boiani R, Cinti S, Peters J, Kelsey G (2004) The imprinted signaling protein XL alpha s is required for postnatal adaptation to feeding. Nat Genet 36(8):818–826. doi: 10.1038/ng1397 PubMedCrossRefGoogle Scholar
  55. Redrup L, Branco MR, Perdeaux ER, Krueger C, Lewis A, Santos F, Nagano T, Cobb BS, Fraser P, Reik W (2009) The long noncoding RNA Kcnq1ot1 organises a lineage-specific nuclear domain for epigenetic gene silencing. Development 136(4):525–530. doi: 10.1242/dev.031328 PubMedCrossRefGoogle Scholar
  56. Reik W, Walter J (1998) Imprinting mechanisms in mammals. Curr Opin Genet Dev 8(2):154–164PubMedCrossRefGoogle Scholar
  57. Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2(1):21–32. doi: 10.1038/35047554 PubMedCrossRefGoogle Scholar
  58. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293(5532):1089–1093. doi: 10.1126/science.1063443293/5532/1089 PubMedCrossRefGoogle Scholar
  59. Sandell LL, Guan XJ, Ingram R, Tilghman SM (2003) Gatm, a creatine synthesis enzyme, is imprinted in mouse placenta. Proc Natl Acad Sci USA 100(8):4622–4627. doi: 10.1073/pnas.0230424100 PubMedCrossRefGoogle Scholar
  60. Sanz LA, Chamberlain S, Sabourin JC, Henckel A, Magnuson T, Hugnot JP, Feil R, Arnaud P (2008) A mono-allelic bivalent chromatin domain controls tissue-specific imprinting at Grb10. EMBO J 27(19):2523–2532. doi: 10.1038/emboj.2008.142 PubMedCrossRefGoogle Scholar
  61. Schulz R, Menheniott TR, Woodfine K, Wood AJ, Choi JD, Oakey RJ (2006) Chromosome-wide identification of novel imprinted genes using microarrays and uniparental disomies. Nucleic Acids Res 34(12):e88. doi: 10.1093/nar/gkl461 PubMedCrossRefGoogle Scholar
  62. Schulz R, Woodfine K, Menheniott TR, Bourc’his D, Bestor T, Oakey RJ (2008) WAMIDEX: a web atlas of murine genomic imprinting and differential expression. Epigenetics 3(2):89–96. pii:5900PubMedCrossRefGoogle Scholar
  63. Schulz R, McCole RB, Woodfine K, Wood AJ, Chahal M, Monk D, Moore GE, Oakey RJ (2009) Transcript- and tissue-specific imprinting of a tumour suppressor gene. Hum Mol Genet 18(1):118–127. doi: ddn32210.1093/hmg/ddn322 PubMedCrossRefGoogle Scholar
  64. Schulz R, Proudhon C, Bestor TH, Woodfine K, Lin CS, Lin SP, Prissette M, Oakey RJ, Bourc’his D (2010) The parental non-equivalence of imprinting control regions during mammalian development and evolution. PLoS Genet 6(11):e1001214. doi: 10.1371/journal.pgen.1001214 PubMedCrossRefGoogle Scholar
  65. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, Sato S, Hata K, Andrews SR, Kelsey G (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43(8):811–814. doi: 10.1038/ng.864ng.864 PubMedCrossRefGoogle Scholar
  66. Smith FM, Holt LJ, Garfield AS, Charalambous M, Koumanov F, Perry M, Bazzani R, Sheardown SA, Hegarty BD, Lyons RJ, Cooney GJ, Daly RJ, Ward A (2007) Mice with a disruption of the imprinted Grb10 gene exhibit altered body composition, glucose homeostasis, and insulin signaling during postnatal life. Mol Cell Biol 27(16):5871–5886. doi: 10.1128/MCB.02087-06 PubMedCrossRefGoogle Scholar
  67. Surani A, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550PubMedCrossRefGoogle Scholar
  68. Tanaka M, Puchyr M, Gertsenstein M, Harpal K, Jaenisch R, Rossant J, Nagy A (1999) Parental origin-specific expression of Mash2 is established at the time of implantation with its imprinting mechanism highly resistant to genome-wide demethylation. Mech Dev 87(1–2):129–142. pii:S0925-4773(99)00158-6PubMedCrossRefGoogle Scholar
  69. Tang F, Barbacioru C, Nordman E, Li B, Xu N, Bashkirov VI, Lao K, Surani MA (2010) RNA-Seq analysis to capture the transcriptome landscape of a single cell. Nat Protoc 5(3):516–535. doi: 10.1038/nprot.2009.236 PubMedCrossRefGoogle Scholar
  70. Thorvaldsen J, Duran JL, Bartolomei MS (1998) Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Gene Dev 12:3693–3702PubMedCrossRefGoogle Scholar
  71. Umlauf D, Goto Y, Cao R, Cerqueira F, Wagschal A, Zhang Y, Feil R (2004) Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes. Nat Genet 36(12):1296–1300. doi: 10.1038/ng1467 PubMedCrossRefGoogle Scholar
  72. Wang Y, Joh K, Masuko S, Yatsuki H, Soejima H, Nabetani A, Beechey CV, Okinami S, Mukai T (2004) The mouse Murr1 gene is imprinted in the adult brain, presumably due to transcriptional interference by the antisense-oriented U2af1-rs1 gene. Mol Cell Biol 24(1):270–279PubMedCrossRefGoogle Scholar
  73. Williamson CM, Ball ST, Nottingham WT, Skinner JA, Plagge A, Turner MD, Powles N, Hough T, Papworth D, Fraser WD, Maconochie M, Peters J (2004) A cis-acting control region is required exclusively for the tissue-specific imprinting of Gnas. Nat Genet 36(8):894–899. doi: 10.1038/ng1398 PubMedCrossRefGoogle Scholar
  74. Williamson CM, Blake A, Thomas S, Beechey CV, Hankcock J, Cattanach BM, Peters J (2012) Mouse imprinting data and references.
  75. Wood AJ, Roberts RG, Monk D, Moore GE, Schulz R, Oakey RJ (2007) A screen for retrotransposed imprinted genes reveals an association between x chromosome homology and maternal germ-line methylation. PLoS Genet 3 (2 e20):192–203Google Scholar
  76. Wood AJ, Schulz R, Woodfine K, Koltowska K, Beechey CV, Peters J, Bourc’his D, Oakey RJ (2008) Regulation of alternative polyadenylation by genomic imprinting. Genes Dev 22(9):1141–1146. doi: 10.1101/gad.473408 PubMedCrossRefGoogle Scholar
  77. Xie W, Barr CL, Kim A, Yue F, Lee AY, Eubanks J, Dempster EL, Ren B (2012) Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 148(4):816–831. doi: 10.1016/j.cell.2011.12.035 PubMedCrossRefGoogle Scholar
  78. Yamasaki K, Joh K, Ohta T, Masuzaki H, Ishimaru T, Mukai T, Niikawa N, Ogawa M, Wagstaff J, Kishino T (2003) Neurons but not glial cells show reciprocal imprinting of sense and antisense transcripts of Ube3a. Hum Mol Genet 12(8):837–847PubMedCrossRefGoogle Scholar
  79. Yamasaki Y, Kayashima T, Soejima H, Kinoshita A, Yoshiura K, Matsumoto N, Ohta T, Urano T, Masuzaki H, Ishimaru T, Mukai T, Niikawa N, Kishino T (2005) Neuron-specific relaxation of Igf2r imprinting is associated with neuron-specific histone modifications and lack of its antisense transcript Air. Hum Mol Genet 14(17):2511–2520. doi: 10.1093/hmg/ddi255 PubMedCrossRefGoogle Scholar
  80. Yu S, Yu D, Lee E, Eckhaus M, Lee R, Corria Z, Accili D, Westphal H, Weinstein LS (1998) Variable and tissue-specific hormone resistance in heterotrimeric Gs protein alpha-subunit (Gsalpha) knockout mice is due to tissue-specific imprinting of the gsalpha gene. Proc Natl Acad Sci USA 95(15):8715–8720PubMedCrossRefGoogle Scholar
  81. Zwart R, Sleutels F, Wutz A, Schinkel AH, Barlow DP (2001) Bidirectional action of the Igf2r imprint control element on upstream and downstream imprinted genes. Genes Dev 15(18):2361–2366. doi: 10.1101/gad.206201 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of Medical and Molecular GeneticsKing’s College LondonLondonUK

Personalised recommendations