New insights into establishment and maintenance of DNA methylation imprints in mammals

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1609, 2013, Pages

  Kelsey, Gavin ^a,b   Feil, Robert ^c  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

Author keywords

DNA methylation; Epigenomics; Genomic imprinting; Germ cells; Histone modifications

Indexed keywords

DEVELOPMENTAL BIOLOGY; DNA; EVOLUTIONARY BIOLOGY; GAMETOGENESIS; GENE EXPRESSION; GENOMICS; GERM CELL; MAMMAL; METHYLATION; PROTEIN;

HISTONE; SMALL INTERFERING RNA;

ANIMAL; ANIMAL EMBRYO; CYTOLOGY; DNA METHYLATION; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENETICS; GENOME IMPRINTING; MALE; MAMMAL; METABOLISM; OOCYTE; OOCYTE DEVELOPMENT; PRENATAL DEVELOPMENT; REVIEW; ZYGOTE;

ANIMALS; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; GENOMIC IMPRINTING; HISTONES; MALE; MAMMALS; OOCYTES; OOGENESIS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; ZYGOTE;

EID: 84876580247     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0336     Document Type: Review

References (135)

1. Ferguson-Smith AC. 2011 Genomic imprinting: the emergence of an epigenetic paradigm. Nat. Rev. Genet. 12, 565-575. (doi:10.1038/nrg3032)
2. McGrath J, Solter D. 1984 Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179-183. (doi:10.1016/0092-8674(84)90313-1)
3. Surani MA, Barton SC, Norris ML. 1984 Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308, 548-550. (doi:10.1038/308548a0)
4. Cattanach BM, Kirk M. 1985 Differential activity of maternal and paternally derived chromosome regions in mice. Nature 315, 496-498. (doi:10.1038/315496a0)
5. Barlow DP, Stoger R, Herrmann BG, Saito K, Schweifer N. 1991 The mouse insulin-like growth factor type-2 receptor is imprinted and closely linked to the Tme locus. Nature 349, 84-87. (doi:10.1038/349084a0)
6. DeChiara TM, Robertson EJ, Efstratiadis A. 1991 Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64, 849-859. (doi:10. 1016/0092-8674(91)90513-X)
7. Bartolomei MS, Zemel S, Tilghman SM. 1991 Parental imprinting of the mouse H19 gene. Nature 351, 153-155. (doi:10.1038/351153a0)
8. Henckel A, Arnaud P. 2010 Genome-wide identification of new imprinted genes. Brief. Funct. Genomics 9, 304-314. (doi:10.1093/bfgp/elq016)
9. Williamson CM, Blake A, Thomas S, Beechey CV, Hancock J, Cattanach BM, Peters J. 2012 MRC Harwell, Oxfordshire. World Wide Web Site-Mouse Imprinting Data and References. See http://www.har.mrc.ac.uk/research/genomic_imprinting/.
10. Fowden AL, Coan PM, Angiolini E, Burton GJ, Constancia M. 2011 Imprinted genes and the epigenetic regulation of placental phenotype. Prog. Biophys. Mol. Biol. 106, 281-288. (doi:10.1016/j. pbiomolbio.2010.11.005)
11. Charalambous M, da Rocha ST, Ferguson-Smith AC. 2007 Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr. Opin. Endocrinol. Diabetes Obes. 14, 3-12. (doi:10.1097/MED.0b013e328013daa2)
12. Frontera M, Dickins B, Plagge A, Kelsey G. 2008 Imprinted genes, postnatal adaptations and enduring effects on energy homeostasis. Adv. Exp. Med. Biol. 626, 41-61. (doi:10.1007/978-0-387-77576-0_4)
13. Wilkinson LS, Davies W, Isles AR. 2007 Genomic imprinting effects on brain development and function. Nat. Rev. Neurosci. 8, 832-843. (doi:10. 1038/nrn2235)
14. Wan LB, Bartolomei MS. 2008 Regulation of imprinting in clusters: noncoding RNAs versus insulators. Adv. Genet. 61, 207-223. (doi:10.1016/S0065-2660(07)00007-7)
15. Spahn L, Barlow DP. 2003 An ICE pattern crystallizes. Nat. Genet. 35, 11-12. (doi:10.1038/ng0903-11)
16. Tomizawa S, Sasaki H. 2012 Genomic imprinting and its relevance to congenital disease, infertility, molar pregnancy and induced pluripotent stem cell. J. Hum. Genet. 57, 84-91. (doi:10.1038/jhg. 2011.151)
17. Stöger R, Kubicka P, Liu CG, Kafri T, Razin A, Cedar H, Barlow DP. 1993 Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73, 61-71. (doi:10.1016/0092-8674(93)90160-R)
18. Wutz A, Smrzka OW, Schweifer N, Schellander K, Wagner EF, Barlow DP. 1997 Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature 389, 745-749. (doi:10.1038/39631)
19. Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, Kelsey G, Sasaki H. 2011 Dynamic stagespecific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 138, 811-820. (doi:10.1242/dev.061416)
20. Li E, Beard C, Jaenisch R. 1993 Role for DNA methylation in genomic imprinting. Nature 366, 362-365. (doi:10.1038/366362a0)
21. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. 2001 Dnmt3L and the establishment of maternal genomic imprints. Science 294, 2536-2539. (doi:10.1126/science.1065848)
22. Hata K, Okano M, Lei H, Li E. 2002 Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129, 1983-1993.
23. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. 2004 Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429, 900-903. (doi:10.1038/nature02633)
24. Neumann B, Kubicka P, Barlow DP. 1995 Characteristics of imprinted genes. Nat. Genet. 9, 12-13. (doi:10.1038/ng0195-12)
25. Shemer R, Hershko AY, Perk J, Mostoslavsky R, Tsuberi B, Cedar H, Buiting K, Razin A. 2000 The imprinting box of the Prader-Willi/Angelman syndrome domain. Nat. Genet. 26, 440-443. (doi:10.1038/82571)
26. Kantor B, Makedonski K, Green-Finberg Y, Shemer R, Razin A. 2004 Control elements within the PWS/AS imprinting box and their function in the imprinting process. Hum. Mol. Genet. 13, 751-762. (doi:10.1093/hmg/ddh085)
27. Ruf N, Bähring S, Galetzka D, Pliushch G, Luft FC, Nürnberg P, Haaf T, Kelsey G, Zechner U. 2007 Sequence-based bioinformatic prediction and QUASEP identify genomic imprinting of the KCNK9 potassium channel gene in mouse and human. Hum. Mol. Genet. 16, 2591-2599. (doi:10.1093/hmg/ddm216)
28. 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, e20. (doi:10.1371/journal.pgen.0030020)
29. Ooi SK et al. 2007 DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448, 714-717. (doi:10.1038/nature05987)
30. Chotalia M, Smallwood SA, Ruf N, Dawson C, Lucifero D, Frontera M, James K, Dean W, Kelsey G. 2009 Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 23, 105-117. (doi:10.1101/gad.495809)
31. Henckel A, Chebli K, Kota SK, Arnaud P, Feil R. 2011 Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J. 31, 606-615. (doi:10.1038/emboj. 2011.425)
32. Watanabe T et al. 2011 Role of piRNA and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332, 848-852. (doi:10.1126/science.1203919)
33. Smallwood SA et al. 2011 Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811-814. (doi:10.1038/ng.864)
34. Kobayashi H et al. 2012 Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 8, e1002440. (doi:10.1371/journal.pgen.1002440)
35. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, Meissner A. 2012 A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344. (doi:10.1038/nature10960)
36. Kota SK, Feil R. 2010 Epigenetic transitions in germ cell development and meiosis. Dev. Cell 19, 675-686. (doi:10.1016/j.devcel.2010.10.009)
37. Arnaud P. 2010 Genomic imprinting in germ cells: imprints are under control. Reproduction 140, 411-423. (doi:10.1530/REP-10-0173)
38. Kobayashi H, Suda C, Abe T, Kohara Y, Ikemura T, Sasaki H. 2006 Bisulfite sequencing and dinucleotide content analysis of 15 imprinted mouse differentially methylated regions (DMRs): paternally methylated DMRs contain less CpGs than maternally methylated DMRs. Cytogenet. Genome Res. 113, 130-137. (doi:10.1159/000090824)
39. Kobayashi H, Sakurai T, Sato S, Nakabayashi K, Hata K, Kono T. 2012 Imprinted DNA methylation reprogramming during early mouse embryogenesis at the Gpr1-Zdbf2 locus is linked to long cisintergenic transcription. FEBS Lett. 586, 827-833. (doi:10.1016/j.febslet.2012.01.059)
40. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, Pellegrini M, Jacobsen SE, Reik W. 2010 Genomewide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105. (doi:10.1038/nature08829)
41. Guibert S, Forné T, Weber M. 2012 Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 22, 633-641. (doi:10. 1101/gr.130997.111)
42. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, Reik W, Walter J, Surani MA. 2002 Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117, 15-23. (doi:10.1016/S0925-4773(02)00181-8)
43. Lee J, Inoue K, Ono R, Ogonuki N, Kohda T, Kaneko-Ishino T, Ogura A, Ishino F. 2002 Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129, 1807-1817.
44. Lucifero D, Mann MR, Bartolomei MS, Trasler JM. 2004 Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 13, 839-849. (doi:10.1093/hmg/ddh104)
45. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T. 2006 Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11, 353-361. (doi:10.1111/j.1365-2443.2006.00943.x)
46. Obata Y, Kono T. 2002 Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 277, 5285-5289. (doi:10.1074/jbc.M108586200)
47. Bourc'his D, Proudhon C. 2008 Sexual dimorphism in parental imprint ontogeny and contribution to embryonic development. Mol. Cell. Endocrinol. 282, 87-94. (doi:10.1016/j.mce.2007.11.025)
48. Davis TL, Yang GJ, McCarrey JR, Bartolomei MS. 2000 The H19 methylation imprint is erased and re-established differentially on the parental alleles during male germ cell development. Hum. Mol. Genet. 9, 2885-2894. (doi:10.1093/hmg/9.19.2885)
49. Bourc'his D, Bestor TH. 2004 Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431, 96-99. (doi:10.1038/nature02886)
50. Kato Y et al. 2007 Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16, 2272-2280. (doi:10.1093/hmg/ddm179)
51. Hutter B, Helms V, Paulsen M. 2006 Tandem repeats in the CpG islands of imprinted genes. Genomics 88, 323-332. (doi:10.1016/j.ygeno.2006. 03.019)
52. 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, 1268-1282. (doi:10.1101/gad.1416906)
53. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X. 2007 Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251. (doi:10.1038/nature06146)
54. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, Smith AD. 2011 Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146, 1029-1041. (doi:10.1016/j.cell.2011.08.016)
55. Borgel J, Guibert S, Li Y, Chiba H, Schübeler D, Sasaki H, Forné T, Weber M. 2010 Targets and dynamics of promoter DNA methylation during early mouse development. Nat. Genet. 42, 1093-1100. (doi:10.1038/ng.708)
56. Mackay DJ et al. 2008 Hypomethylation of multiple imprinted loci in individuals with transient neonatal diabetes is associated with mutations in ZFP57. Nat. Genet. 40, 949-951. (doi:10.1038/ng.187)
57. Li X, Ito M, Zhou F, Youngson N, Zuo X, Leder P, Ferguson-Smith AC. 2008 A maternal-zygotic effect gene, Zfp57, maintains both maternal and paternal imprints. Dev. Cell 15, 547-557. (doi:10.1016/j. devcel.2008.08.014)
58. Quenneville S et al. 2011 In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol. Cell 44, 361-372. (doi:10.1016/j.molcel.2011.08.032)
59. Zhang Y et al. 2010 Chromatin methylation activity of Dnmt3a and Dnmt3a/3L is guided by interaction of the ADD domain with the histone H3 tail. Nucleic Acids Res. 38, 4246-4253. (doi:10.1093/nar/gkq147)
60. Bernstein BE et al. 2006 A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326. (doi:10. 1016/j.cell.2006.02.041)
61. Mikkelsen TS et al. 2007 Genome-wide maps of chromatin state in pluripotent and lineagecommitted cells. Nature 448, 553-560. (doi:10. 1038/nature06008)
62. Zhao XD et al. 2007 Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell. 1, 286-298. (doi:10.1016/j.stem.2007.08.004)
63. Ciccone DN, Su H, Hevi S, Gay F, Lei H, Bajko J, Xu G, Li E, Chen T. 2009 KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461, 415-418. (doi:10. 1038/nature08315)
64. Delaval K, Govin J, Cerqueira F, Rousseaux S, Khochbin S, Feil R. 2007 Differential histone modifications mark mouse imprinting control regions during spermatogenesis. EMBO J. 26, 720-729. (doi:10.1038/sj.emboj.7601513)
65. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. 2009 Distinctive chromatin in human sperm packages genes for embryo development. Nature 460, 473-478.
66. Brykczynska U et al. 2010 Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat. Struct. Mol. Biol. 17, 679-687. (doi:10.1038/nsmb.1821)
67. Tamaru H, Zhang X, McMillen D, Singh PB, Nakayama J, Grewal SI, Allis CD, Cheng X, Selker EU. 2003 Trimethylated lysine 9 of histone H3 is a mark for DNA methylation in Neurospora crassa. Nat. Genet. 34, 75-79. (doi:10.1038/ng1143)
68. Zhao Q et al. 2009 PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat. Struct. Mol. Biol. 16, 304-311. (doi:10.1038/nsmb.1568)
69. Jelinic P, Stehle JC, Shaw P. 2006 The testis-specific factor CTCFL cooperates with the protein methyltransferase PRMT7 in H19 imprinting control region methylation. PLoS Biol. 4, e355. (doi:10. 1371/journal.pbio.0040355)
70. Illingworth RS et al. 2010 Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 6, e1001134. (doi:10.1371/journal.pgen.1001134)
71. Maunakea AK et al. 2010 Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 466, 253-257. (doi:10.1038/nature09165)
72. Kanber D, Berulava T, Ammerpohl O, Mitter D, Richter J, Siebert R, Horsthemke B, Lohmann D, Buiting K. 2009 The human retinoblastoma gene is imprinted. PLoS Genet. 5, e1000790. (doi:10.1371/journal.pgen.1000790)
73. Horsthemke B, Wagstaff J. 2008 Mechanisms of imprinting of the Prader-Willi/Angelman region. Am. J. Med. Genet. A. 146A, 2041-2052. (doi:10. 1002/ajmg.a.32364)
74. Dittrich B et al. 1996 Imprint switching on human chromosome 15 may involve alternative transcripts of the SNRPN gene. Nat. Genet. 14, 163-170. (doi:10.1038/ng1096-163)
75. Mapendano CK, Kishino T, Miyazaki K, Kondo S, Yoshiura K, Hishikawa Y, Koji T, Niikawa N, Ohta T. 2006 Expression of the Snurf-Snrpn IC transcript in the oocyte and its putative role in the imprinting establishment of the mouse 7C imprinting domain. J. Hum. Genet. 51, 236-243. (doi:10.1007/s10038-005-0351-8)
76. Bastepe M, Fröhlich LF, Linglart A, Abu-Zahra HS, Tojo K, Ward LM, Jüppner H. 2005 Deletion of the NESP55 differentially methylated region causes loss of maternal GNAS imprints and pseudohypoparathyroidism type Ib. Nat. Genet. 37, 25-27. (doi:10.1038/ng1560)
77. Bastepe M et al. 2003 Autosomal dominant pseudohypoparathyroidism type Ib is associated with a heterozygous microdeletion that likely disrupts a putative imprinting control element of GNAS. J. Clin. Invest. 112, 1255-1263.
78. Fröhlich LF, Mrakovcic M, Steinborn R, Chung UI, Bastepe M, Jüppner H. 2010 Targeted deletion of the Nesp55 DMR defines another Gnas imprinting control region and provides a mouse model of autosomal dominant PHP-Ib. Proc. Natl Acad. Sci. USA 107, 9275-9280. (doi:10.1073/pnas. 0910224107)
79. Williamson CM et al. 2011 Uncoupling antisensemediated silencing and DNA methylation in the imprinted Gnas cluster. PLoS Genet. 7, e1001347. (doi:10.1371/journal.pgen.1001347)
80. Smith EY, Futtner CR, Chamberlain SJ, Johnstone KA, Resnick JL. 2011 Transcription is required to establish maternal imprinting at the Prader-Willi syndrome and Angelman syndrome locus. PLoS Genet. 7, e1002422. (doi:10.1371/journal.pgen.1002422)
81. Smallwood SA, Kelsey G. 2012 De novo DNA methylation: a germ cell perspective. Trends Genet. 28, 33-42. (doi:10.1016/j.tig.2011.09.004)
82. O'Doherty AM, Rutledge CE, Sato S, Thakur A, Lees-Murdock DJ, Hata K, Walsh CP. 2011 DNA methylation plays an important role in promoter choice and protein production at the mouse Dnmt3L locus. Dev. Biol. 356, 411-420. (doi:10.1016/j. ydbio.2011.05.665)
83. Kaneda M, Hirasawa R, Chiba H, Okano M, Li E, Sasaki H. 2010 Genetic evidence for Dnmt3adependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15, 169-179. (doi:10.1111/j. 1365-2443.2009.01374.x)
84. Dhayalan A, Rajavelu A, Rathert P, Tamas R, Jurkowska RZ, Ragozin S, Jeltsch A. 2010 The Dnmt3a PWWP domain reads histone 3 lysine 36 trimethylation and guides DNA methylation. J. Biol. Chem. 285, 26114-26120. (doi:10.1074/jbc.M109. 089433)
85. Wagner EJ, Carpenter PB. 2012 Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell. Biol. 13, 115-126. (doi:10.1038/nrm3274)
86. Yoh SM, Lucas JS, Jones KA. 2008 The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev. 22, 3422-3434. (doi:10.1101/gad.1720008)
87. Xie L, Pelz C, Wang W, Bashar A, Varlamova O, Shadle S, Impey S. 2011 KDM5B regulates embryonic stem cell self-renewal and represses cryptic intragenic transcription. EMBO J. 30, 1473-1484. (doi:10.1038/emboj.2011.91)
88. Fang R et al. 2010 Human LSD2/KDM1b/AOF1 regulates gene transcription by modulating intragenic H3K4me2 methylation. Mol. Cell 39, 222-233. (doi:10.1016/j.molcel.2010.07.008)
89. Blackledge NP, Zhou JC, Tolstorukov MY, Farcas AM, Park PJ, Klose RJ. 2010 CpG islands recruit a histone H3 lysine 36 demethylase. Mol. Cell 38, 179-190. (doi:10.1016/j.molcel.2010.04.009)
90. Yoon BJ, Herman H, Sikora A, Smith LT, Plass C, Soloway PD. 2002 Regulation of DNA methylation of Rasgrf1. Nat. Genet. 30, 92-96. (doi:10.1038/ng795)
91. Aravin AA, Bourc'his D. 2008 Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev. 22, 970-975. (doi:10.1101/gad. 1669408)
92. Augui S, Nora EP, Heard E. 2011 Regulation of X-chromosome inactivation by the X-inactivation centre. Nat. Rev. Genet. 12, 429-442. (doi:10.1038/nrg2987)
93. Mak W, Nesterova TB, de Napoles M, Appanah R, Yamanaka S, Otte AP, Brockdorff N. 2004 Reactivation of the paternal X chromosome in early mouse embryos. Science 303, 666-669. (doi:10. 1126/science.1092674)
94. Patrat C, Okamoto I, Diabangouaya P, Vialon V, Le Baccon P, Chow J, Heard E. 2009 Dynamic changes in paternal X-chromosome activity during imprinted X-chromosome inactivation in mice. Proc. Natl Acad. Sci. USA 106, 5198-5203. (doi:10.1073/pnas.0810683106)
95. Goto Y, Takagi N. 2000 Maternally inherited X chromosome is not inactivated in mouse blastocysts due to parental imprinting. Chromosome Res. 8, 101-109. (doi:10.1023/A:1009234217981)
96. Chiba H, Hirasawa R, Kaneda M, Amakawa Y, Li E, Sado T, Sasaki H. 2008 De novo DNA methylation independent establishment of maternal imprint on X chromosome in mouse oocytes. Genesis 46, 768-774. (doi:10.1002/dvg.20438)
97. Okae H et al. 2012 Re-investigation and RNA sequencing-based identification of genes with placenta-specific imprinted expression. Hum. Mol. Genet. 21, 548-558. (doi:10.1093/hmg/ddr488)
98. Wang Q et al. 2011 Recent acquisition of imprinting at the rodent Sfmbt2 locus correlates with insertion of a large block of miRNAs. BMC Genomics 12, 204. (doi:10.1186/1471-2164-12-204)
99. Arnaud P, Hata K, Kaneda M, Li E, Sasaki H, Feil R, Kelsey G. 2006 Stochastic imprinting in the progeny of Dnmt3L-/-females. Hum. Mol. Genet. 15, 589-598. (doi:10.1093/hmg/ddi475)
100. Henckel A, Nakabayashi K, Sanz LA, Feil R, Hata K, Arnaud P. 2009 Histone methylation is mechanistically linked to DNA methylation at imprinting control regions in mammals. Hum. Mol. Genet. 18, 3375-3383. (doi:10.1093/hmg/ddp277)
101. Tanimoto K, Shimotsuma M, Matsuzaki H, Omori A, Bungert J, Engel JD, Fukamizu A. 2005 Genomic imprinting recapitulated in the human beta-globin locus. Proc. Natl Acad. Sci. USA 102, 10 250-10 255. (doi:10.1073/pnas.0409541102)
102. Matsuzaki H, Okamura E, Shimotsuma M, Fukamizu A, Tanimoto K. 2009 A randomly integrated transgenic H19 imprinting control region acquires methylation imprinting independently of its establishment in germ cells. Mol. Cell. Biol. 29, 4595-4603. (doi:10.1128/MCB.00275-09)
103. Shoji M et al. 2009 The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev. Cell 17, 775-787. (doi:10.1016/j.devcel.2009.10.012)
104. Murdoch S et al. 2006 Mutations in NALP7 cause recurrent hydatidiform moles and reproductive wastage in humans. Nat. Genet. 38, 300-302. (doi:10.1038/ng1740)
105. Meyer E, Lim D, Pasha S, Tee LJ, Rahman F, Yates JR, Woods CG, Reik W, Maher ER. 2009 Germline mutation in NLRP2 (NALP2) in a familial imprinting disorder (Beckwith-Wiedemann Syndrome). PLoS Genet. 5, e1000423. (doi:10.1371/journal.pgen. 1000423)
106. Parry DA et al. 2011 Mutations causing familial biparental hydatidiform mole implicate c6orf221 as a possible regulator of genomic imprinting in the human oocyte. Am. J. Hum. Genet. 89, 451-458. (doi:10.1016/j.ajhg.2011.08.002)
107. Nakamura T et al. 2007 PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 64-71. (doi:10.1038/ncb1519)
108. Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. 2012 Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335, 1499-1502. (doi:10.1126/science.1216154)
109. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, Jaenisch R, Sasaki H. 2008 Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22, 1607-1616. (doi:10.1101/gad.1667008)
110. Howell CY, Bestor TH, Ding F, Latham KE, Mertineit C, Trasler JM, Chaillet JR. 2001 Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104, 829-838. (doi:10. 1016/S0092-8674(01)00280-X)
111. Sharif J et al. 2007 The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912. (doi:10. 1038/nature06397)
112. Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, Stein A, Woodcock CL, Skoultchi AI. 2005 Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199-1212. (doi:10.1016/j.cell.2005.10.028)
113. Reese KJ, Lin S, Verona RI, Schultz RM, Bartolomei MS. 2007 Maintenance of paternal methylation and repression of the imprinted H19 gene requires MBD3. PLoS Genet. 3, e137. (doi:10.1371/journal.pgen.0030137)
114. Ma P, Lin S, Bartolomei MS, Schultz RM. 2010 Metastasis tumor antigen 2 (MTA2) is involved in proper imprinted expression of H19 and Peg3 during mouse preimplantation development. Biol. Reprod. 83, 1027-1035. (doi:10.1095/biolreprod. 110.086397)
115. Wu MY, Tsai TF, Beaudet AL. 2006 Deficiency of Rbbp1/Arid4a and Rbbp1l1/Arid4b alters epigenetic modifications and suppresses an imprinting defect in the PWS/AS domain. Genes Dev. 20, 2859-2870. (doi:10.1101/gad.1452206)
116. Schoenherr CJ, Levorse JM, Tilghman SM. 2003 CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33, 66-69. (doi:10.1038/ng1057)
117. Kim JD, Kim H, Ekram MB, Yu S, Faulk C, Kim J. 2011 Rex1/Zfp42 as an epigenetic regulator for genomic imprinting. Hum. Mol. Genet. 20, 1353-1362. (doi:10.1093/hmg/ddr017)
118. 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, 816-831. (doi:10.1016/j.cell.2011.12.035)
119. Reik W. 2007 Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432. (doi:10.1038/nature05918)
120. Liu YJ, Nakamura T, Nakano T. 2011 Essential role of DPPA3 for chromatin condensation in mouse oocytogenesis. Biol. Reprod. 86, 40. (doi:10.1095/biolreprod.111.095018)
121. Wossidlo M et al. 2011 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2, 241. (doi:10. 1038/ncomms1240)
122. Yuan P et al. 2009 Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507-2520. (doi:10.1101/gad.1831909)
123. Engel N, Thorvaldsen JL, Bartolomei MS. 2006 CTCF binding sites promote transcription initiation and prevent DNA methylation on the maternal allele at the imprinted H19/Igf2 locus. Hum. Mol. Genet. 15, 2945-2954. (doi:10.1093/hmg/ddl237)
124. Stadler MB et al. 2011 DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495. (doi:10.1038/nature10716)
125. Branco MR, Ficz G, Reik W. 2011 Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 13, 7-13. (doi:10.1038/nrn3125)
126. Tahiliani M et al. 2009 Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935. (doi:10.1126/science.1170116)
127. Gu TP et al. 2011 The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606-610. (doi:10.1038/nature10443)
128. Gregg C, Zhang J, Weissbourd B, Luo S, Schroth GP, Haig D, Dulac C. 2010 High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329, 643-648. (doi:10.1126/science.1190830)
129. DeVeale B, van der Kooy D, Babak T. 2012 Critical evaluation of imprinted gene expression by RNASeq: a new perspective. PLoS Genet. 8, e1002600. (doi:10.1371/journal.pgen.1002600)
130. Fauque P, Jouannet P, Lesaffre C, Ripoche MA, Dandolo L, Vaiman D, Jammes H. 2007 Assisted Reproductive Technology affects developmental kinetics, H19 Imprinting Control Region methylation and H19 gene expression in individual mouse embryos. BMC Dev. Biol. 7, 116. (doi:10.1186/1471-213X-7-116)
131. Market-Velker BA, Zhang L, Magri LS, Bonvissuto AC, Mann MR. 2010 Dual effects of superovulation: loss of maternal and paternal imprinted methylation in a dose-dependent manner. Hum. Mol. Genet. 19, 36-51. (doi:10.1093/hmg/ddp465)
132. Kim JM, Ogura A. 2009 Changes in allele-specific association of histone modifications at the imprinting control regions during mouse preimplantation development. Genesis 47, 611-616. (doi:10.1002/dvg.20541)
133. Choo JH, Kim JD, Chung JH, Stubbs L, Kim J. 2006 Allele-specific deposition of macroH2A1 in imprinting control regions. Hum. Mol. Genet. 15, 717-724. (doi:10.1093/hmg/ddi485)
134. Mann MR, Lee SS, Doherty AS, Verona RI, Nolen LD, Schultz RM, Bartolomei MS. 2004 Selective loss of imprinting in the placenta following preimplantation development in culture. Development 131, 3727-3735. (doi:10.1242/dev. 01241)
135. Moore T, Haig D. 1991 Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 7, 45-49.