Transcription and histone methylation changes correlate with imprint acquisition in male germ cells

EMBO Journal

Volumn 31, Issue 3, 2012, Pages 606-615

  Henckel, Amandine ^a,b   Chebli, Karim ^a   Kota, Satya K ^a   Arnaud, Philippe ^a,c   Feil, Robert ^a  

^a CNRS   (France)

^b MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

DNA methylation; epigenetic; genomic imprinting; histone methylation; primordial germ cells

Indexed keywords

DNA; HISTONE H3; HISTONE H4;

ALLELE; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DNA METHYLATION; DNA SEQUENCE; EMBRYO; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC TRANSCRIPTION; GENOME IMPRINTING; HISTONE METHYLATION; HISTONE MODIFICATION; IMPRINTING CONTROL REGION; MALE; MOUSE; NONHUMAN; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROMOTER REGION; SPERMATOGENESIS;

ANIMALS; CELL SEPARATION; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; DROSOPHILA MELANOGASTER; FEMALE; FLOW CYTOMETRY; GENOMIC IMPRINTING; HISTONES; MALE; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 84856462767     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.425     Document Type: Article

References (48)

1. Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T, Surani MA (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8: 623-630 (Pubitemid 43827356)
2. Arnaud P (2010) Genomic imprinting in germ cells: imprints are under control. Reproduction 140: 411-423
3. Bartolomei MS (2009) Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev 23: 2124-2133
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A,Wernig M, Plath K, Jaenisch R,Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326
5. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536-2539 (Pubitemid 34027291)
6. 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
7. 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
8. Cranston MJ, Spinka TL, Elson DA, Bartolomei MS (2001) Elucidation of the minimal sequence required to imprint H19 transgenes. Genomics 73: 98-107 (Pubitemid 32382391)
9. Davis TL, Yang GL, 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
10. 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
11. Drewell RA, Arney KL, Arima T, Barton SC, Brenton JD, Surani MA (2002) Novel conserved elements upstream of the H19 gene are transcribed and act as mesodermal enhancers. Development 129: 1205-1213 (Pubitemid 34874143)
12. Fitzpatrick GV, Soloway PD, Higgins MJ (2002) Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat Genet 32: 426-431 (Pubitemid 35266120)
13. Guo R, Yu Z, Guan J, Ge Y, Ma J, Li S, Wang S, Xue S, Han D (2004) Stage-specific and tissue-specific expression characteristics of differentially expressed genes during mouse spermatogenesis. Mol Reprod Dev 67: 264-272 (Pubitemid 38140822)
14. 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 (Pubitemid 36158711)
15. 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 (Pubitemid 34874213)
16. Hellman A, Chess A (2007) Gene body-specific methylation on the active X chromosome. Science 315: 1141-1143 (Pubitemid 46328027)
17. 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
18. Hiura H, Sugawara A, Ogawa H, John RM, Miyauchi N, Miyanari Y, Horiike T, Li Y, Yaegashi N, Sasaki H, Kono T, Arima T (2010) A tripartite paternally methylated region within the Gpr1-Zdbf2 imprinted domain on mouse chromosome 1 identified by meDIP-on-chip. Nucleic Acids Res 38: 4929-4945
19. 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
20. 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 (Pubitemid 38843304)
21. Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M, Kohara Y, Okano M, Li E, Nozaki M, Sasaki H (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 (Pubitemid 47423893)
22. Koide T, Moriwaki K, Uchida K, Mita A, Sagai T, Yonekawa H, Katoh H, Miyashita N, Tsuchiya K, Nielsen TJ, Shiroishi T (1998) A new inbred strain JF1 established from Japanese fancy mouse carrying the classic piebald allele. Mamm Genome 9: 15-19 (Pubitemid 28158987)
23. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter J, Reik W (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93 (Pubitemid 36330631)
24. Lee D-H, Singh P, Tsai SY, Oates N, Spalla A, Spalla C, Brown L, Rivas G, Larson G, Rauch TA, Pfeifer GP, Szabó PE (2010) CTCFdependent chromatin bias constitutes transient epigenetic memory of the mother at the H19-Igf2 imprinting control region in prospermatogonia. PLOS Genet 6: e1001224
25. Li BZ, Huang Z, Cui QY, Song XH, Du L, Jeltsch A, Chen P, Li G, Li E, Xu GL (2011) Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res 21: 1172-1181
26. 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: 97-102 (Pubitemid 37048602)
27. 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
28. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, BrockmanW, Kim TK, Koche RP, LeeW, Mendenhall E, O0Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C et al (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560 (Pubitemid 47206934)
29. O'Neill LP, VerMilyea MD, Turner BM (2006) Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nat Genet 38: 835-841 (Pubitemid 43980607)
30. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717 (Pubitemid 47236857)
31. Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, Shirakawa M (2009) Structural basis for recognition of H4K4 methylation status by DNA methyltransferase 3A ATRX-DNMT3-DNMTL domain. EMBO Rep 10: 1235-1241
32. Pannetier M, Julien E, Schotta G, Tardat M, Sardet C, Jenuwein T, Feil R (2008) PR-SET7 and SUV4-20H regulate H4 lysine-20 methylation at imprinting control regions in the mouse. EMBO Rep 9: 998-1005
33. Schoenfelder S, Smits G, Fraser P, ReikW, Paro R (2007) Non-coding transcripts in the H19 imprinting control region mediate gene silencing in transgenic Drosophila. EMBO Rep 8: 1068-1073 (Pubitemid 350042343)
34. Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24: 2264-2269
35. Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y (2005) Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev Biol 278: 440-458 (Pubitemid 40175041)
36. Shemer R, Birger Y, Riggs AD, Razin A (1997) Structure of the imprinted mouse Snrpn gene and establishment of its parental-specific methylation pattern. Proc Natl Acad Sci USA 94: 10267-10272 (Pubitemid 27407030)
37. Shoji M, Tanaka T, Hosokawa M, Reuter M, Stark A, Kato Y, Kondoh G, Okawa K, Chujo T, Suzuki T, Hata K, Martin SL, Noce T, Kuramochi-Miyagawa S, Nakano T, Sasaki H, Pillai RS, Nakatsuji N, Chuma S (2009) The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 17: 775-787
38. 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 (Pubitemid 36548794)
39. Tremblay KD, Saam JR, Ingram RS, Tilghman SM, Bartolomei MS (1995) A paternal-specific methylation imprint marks the alleles of the mouse H19 gene. Nat Genet 9: 407-413
40. 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: 1296-1300 (Pubitemid 39577938)
41. Verona RI, Thorvaldsen JT, Reese KJ, Bartolomei MS (2008) The transcriptional status but not the imprinting control region determines allele-specific histone modifications at the imprinted H19 Locus. Mol Cell Biol 28: 71-82
42. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, Minami N, Imai H (2006) Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 20: 1732-1743 (Pubitemid 43992882)
43. Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, Kuramochi-Miyagawa S, Iida N, Hoki Y, Murphy PJ, Toyoda A, Gotoh K, Hiura H, Arima T, Fujiyama A, Sado T, Shibata T, Nakano T, Lin H, Ichiyanagi K, Soloway PD et al (2011) Role of piRNA and non-coding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332: 848-852
44. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444-448
45. Yoshimizu T, Sugiyama N, De Felice M, Yeom YI, Ohbo K, Masuko K, Obinata M, Abe K, Scholer HR, Matsui Y (1999) Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice. Dev Growth Differ 41: 675-684 (Pubitemid 30026664)
46. Zhang Y., Jurkowska R, Soeroes S, Rajavelu A, Dhayalan A, Bock I, Rathert P, Brandt O, Reinhardt R, Fischle W, Jeltsch A (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
47. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, Cerruti L, Curtis DJ, Patel DJ, Allis CD, Cunningham JM, Jane SM (2009) PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 16: 304-311
48. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA, Bourque G, Oh S, Ruan Y, Ng HH, Wei CL (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 (Pubitemid 47370914)