Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells

Genes and Development

Volumn 28, Issue 18, 2014, Pages 2041-2055

  Liu, Sheng ^a   Brind’Amour, Julie ^a   Karimi, Mohammad M ^a   Shirane, Kenjiro ^b   Bogutz, Aaron ^a   Lefebvre, Louis ^a   Sasaki, Hiroyuki ^b,c   Shinkai, Yoichi ^c,d   Lorincz, Matthew C ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b KYUSHU UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d RIKEN   (Japan)

Author keywords

DNA methylation; Endogenous retroviruses; Germ cell development; H3K27me3; H3K9me3; Setdb1

Indexed keywords

HISTONE H3; HISTONE METHYLTRANSFERASE; LYSINE; PROTEIN; SETDB1 PROTEIN; UNCLASSIFIED DRUG; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; SETDB1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; ENDOGENOUS RETROVIRUS; FEMALE; GAMETOGENESIS; GENE EXPRESSION; GERMLINE DEVELOPMENT; HISTONE MODIFICATION; LONG TERMINAL REPEAT; MALE; MOUSE; NONHUMAN; PRIMORDIAL GERM CELL; PROTEIN DEPLETION; RETROPOSON; SOMATIC CELL; SPERMATOGENESIS; TRANSCRIPTION INITIATION SITE; UPREGULATION; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; GENE DELETION; GENE INACTIVATION; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; GERM CELL; GERM CELL DEVELOPMENT; H3K27ME3; H3K9ME3; METABOLISM; SETDB1; VIROLOGY; VIRUS ACTIVATION;

DNA METHYLATION; ENDOGENOUS RETROVIRUSES; GERM CELL DEVELOPMENT; H3K27ME3; H3K9ME3; SETDB1;

ANIMALS; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; ENDOGENOUS RETROVIRUSES; FEMALE; GAMETOGENESIS; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GENE SILENCING; GERM CELLS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MALE; MICE; TRANSCRIPTION, GENETIC; VIRUS ACTIVATION;

EID: 84907157204     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.244848.114     Document Type: Article

References (66)

1. Abe M, Tsai SY, Jin S-G, Pfeifer GP, Szabó PE. 2011. Sex-specific dynamics of global chromatin changes in fetal mouse germ cells. PLoS ONE 6: e23848.
2. Alder O, Lavial F, Helness A, Brookes E, Pinho S, Chandrashekran A, Arnaud P, Pombo A, O’Neill L, Azuara V. 2010. Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development 137: 2483-2492.
3. An J, Zhang X, Qin J, Wan Y, Hu Y, Liu T, Li J, Dong W, Du E, Pan C, et al. 2014. The histone methyltransferase ESET is required for the survival of spermatogonial stem/progenitor cells in mice. Cell Death Dis 5: e1196.
4. Aravin AA, Sachidanandam R, Bourc’his D, Schaefer C, Pezic D, Toth KF, Bestor T, Hannon GJ. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799.
5. Blaschke K, Ebata KT, Karimi MM, Zepeda-Martínez JA, Goyal P, Mahapatra S, Tam A, Laird DJ, Hirst M, Rao A, et al. 2013. Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature 500: 222-226.
6. Bourc’his D, Bestor TH. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96-99.
7. Bulut-Karslioglu A, La Rosa-Velázquez De IA, Ramirez F, Barenboim M, Onishi-Seebacher M, Arand J, Galán C, Winter GE, Engist B, Gerle B, et al. 2014. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol Cell 55: 277-290.
8. Cammas F, Mark M, Dolle P, Dierich A, Chambon P, Losson R. 2000. Mice lacking the transcriptional corepressor TIF1b are defective in early postimplantation development. Development 127: 2955-2963.
9. Castel SE, Martienssen RA. 2013. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14: 100-112.
10. Clough E, Moon W, Wang S, Smith K, Hazelrigg T. 2007. Histone methylation is required for oogenesis in Drosophila. Development 134: 157-165.
11. Dodge JE, Kang Y-K, Beppu H, Lei H, Li E. 2004. Histone H3-K9 methyltransferase ESET is essential for early development. Mol Cell Biol 24: 2478-2486.
12. Donertas D, Sienski G, Brennecke J. 2013. Drosophila Gtsf1 is an essential component of the Piwi-mediated transcriptional silencing complex. Genes Dev 27: 1693-1705.
13. Dudley JP. 1987. Discrete high molecular weight RNA transcribed from the long interspersed repetitive element L1Md. Nucleic Acids Res 15: 2581.
14. Dupressoir A, Heidmann T. 1996. Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol Cell Biol 16: 4495-4503.
15. Durcova-Hills G, Tokunaga T, Kurosaka S, Yamaguchi M, Takahashi S, Imai H. 1999. Immunomagnetic isolation of primordial germ cells and the establishment of embryonic germ cell lines in the mouse. Cloning 1: 217-224.
16. Falconer E, Hills M, Naumann U, Poon SSS, Chavez EA, Sanders AD, Zhao Y, Hirst M, Lansdorp PM. 2012. DNA template strand sequencing of single-cells maps genomic rearrangements at high resolution. Nat Methods 9: 1107-1112.
17. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA, Surani MA. 2013. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339: 448-452.
18. 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.
19. Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, Cesari F, Lee C, Almouzni G, Schneider R, Surani MA. 2008. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452: 877-881.
20. Henckel A, Chebli K, Kota SK, Arnaud P, Feil R. 2012. Transcription and histone methylation changes correlate with imprint acquisition in male germ cells. EMBO J 31: 606-615.
21. Ishizu H, Siomi H, Siomi MC. 2012. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev 26: 2361-2373.
22. Jameson SA, Natarajan A, Cool J, DeFalco T, Maatouk DM, Mork L, Munger SC, Capel B. 2012. Temporal transcriptional profiling of somatic and germ cells reveals biased lineage priming of sexual fate in the fetal mouse gonad. PLoS Genet 8: e1002575.
23. Jern P, Coffin JM. 2008. Effects of retroviruses on host genome function. Annu Rev Genet 42: 709-732.
24. 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.
25. Karimi MM, Goyal P, Maksakova IA, Bilenky M, Leung D, Tang JX, Shinkai Y, Mager DL, Jones S, Hirst M, et al. 2011. DNA methylation and SETDB1/H3K9me3 regulate predominantly distinct sets of genes, retroelements, and chimeric transcripts in mESCs. Cell Stem Cell 8: 676-687.
26. 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.
27. Kaustov L, Ouyang H, Amaya M, Lemak A, Nady N, Duan S, Wasney GA, Li Z, Vedadi M, Schapira M, et al. 2011. Recognition and specificity determinants of the human cbx chromodomains. J Biol Chem 286: 521-529.
28. Kim VN, Han J, Siomi MC. 2009. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139.
29. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, Sato S, Nakabayashi K, Hata K, Sotomaru Y, et al. 2012. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8: e1002440.
30. Kobayashi H, Sakurai T, Miura F, Imai M, Mochiduki K, Yanagisawa E, Sakashita A, Wakai T, Suzuki Y, Ito T, et al. 2013. High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res 23: 616-627.
31. Krueger F, Andrews SR. 2011. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27: 1571-1572.
32. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, Asada N, Kojima K, Yamaguchi Y, Ijiri TW, et al. 2008. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917.
33. Kurimoto K, Yabuta Y, Ohinata Y, Shigeta M, Yamanaka K, Saitou M. 2008. Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev 22: 1617-1635.
34. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, Walter JR, Reik W. 2003. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93.
35. Lees-Murdock DJ, De Felici M, Walsh CP. 2003. Methylation dynamics of repetitive DNA elements in the mouse germ cell lineage. Genomics 82: 230-237.
36. Leung D, Du T, Wagner U, Xie W, Lee AY, Goyal P, Li Y, Szulwach KE, Jin P, Lorincz MC, et al. 2014. Regulation of DNA methylation turnover at LTR retrotransposons and imprinted loci by the histone methyltransferase Setdb1. Proc Natl Acad Sci 111: 6690-6695.
37. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
38. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
39. Lomelí H, Ramos-Mejía V, Gertsenstein M, Lobe CG, Nagy A. 2000. Targeted insertion of Cre recombinase into the TNAP gene: excision in primordial germ cells. Genesis 26: 116-117.
40. Maksakova IA, Romanish MT, Gagnier L, Dunn CA, Van De Lagemaat LN, Mager DL. 2006. Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2: e2.
41. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, Tachibana M, Lorincz MC, Shinkai Y. 2010. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
42. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim T-K, Koche RP, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
43. Miura F, Enomoto Y, Dairiki R, Ito T. 2012. Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 40: e136.
44. Mouse Genome Sequencing Consortium. 2002. Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
45. Nagy A. 2003. Manipulating the mouse embryo. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Nellåker C, Keane TM, Yalcin B, Wong K, Agam A, Belgard TG, Flint J, Adams DJ, Frankel WN, Ponting CP. 2012. The genomic landscape shaped by selection on transposable elements across 18 mouse strains. Genome Biol 13: R45.
47. Ng J-H, Kumar V, Muratani M, Kraus P, Yeo J-C, Yaw L-P, Xue K, Lufkin T, Prabhakar S, Ng H-H. 2013. In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev Cell 24: 324-333.
48. Oda M, Oxley D, Dean W, Reik W. 2013. Regulation of lineage specific DNA hypomethylation in mouse trophectoderm. PLoS ONE 8: e68846.
49. Pauler FM, Sloane MA, Huang R, Regha K, Koerner MV, Tamir I, Sommer A, Aszodi A, Jenuwein T, Barlow DP. 2009. H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res 19: 221-233.
50. Pezic D, Manakov SA, Sachidanandam R, Aravin AA. 2014. piRNA pathway targets active LINE1 elements to establish the repressive H3K9me3 mark in germ cells. Genes Dev 28: 1410-1428.
51. Rangan P, Malone CD, Navarro C, Newbold SP, Hayes PS, Sachidanandam R, Hannon GJ, Lehmann R. 2011. piRNA production requires heterochromatin formation in Drosophila. Curr Biol 21: 1373-1379.
52. Reuss FU, Frankel WN, Moriwaki K, Shiroishi T, Coffin JM. 1996. Genetics of intracisternal-A-particle-related envelopeencoding proviral elements in mice. J Virol 70: 6450-6454.
53. Rothbart SB, Krajewski K, Nady N, Tempel W, Xue S, Badeaux AI, Barsyte-Lovejoy D, Martinez JY, Bedford MT, Fuchs SM, et al. 2012. Association of UHRF1 with methylated H3K9 directs the maintenance of DNA methylation. Nat Struct Mol Biol 19: 1155-1160.
54. Rothbart SB, Dickson BM, Ong MS, Krajewski K, Houliston S, Kireev DB, Arrowsmith CH, Strahl BD. 2013. Multivalent histone engagement by the linked tandem Tudor and PHD domains of UHRF1 is required for the epigenetic inheritance of DNA methylation. Genes Dev 27: 1288-1298.
55. Rowe HM, Jakobsson J, Mesnard D, Rougemont J, Reynard S, Aktas T, Maillard PV, Layard-Liesching H, Verp S, Marquis J, et al. 2010. KAP1 controls endogenous retroviruses in embryonic stem cells. Nature 463: 237-240.
56. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W. 2012. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48: 849-862.
57. Seki Y, Yamaji M, Yabuta Y, Sano M, Shigeta M, Matsui Y, Saga Y, Tachibana M, Shinkai Y, Saitou M. 2007. Cellular dynamics associated with the genome-wide epigenetic reprogramming in migrating primordial germ cells in mice. Development 134: 2627-2638.
58. Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T, Kono T, Sasaki H. 2013. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet 9: e1003439.
59. 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.
60. Tan S-L, Nishi M, Ohtsuka T, Matsui T, Takemoto K, Kamio-Miura A, Aburatani H, Shinkai Y, Kageyama R. 2012. Essential roles of the histone methyltransferase ESET in the epigenetic control of neural progenitor cells during development. Development 139: 3806-3816.
61. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotech 29: 52-54.
62. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, et al. 2010. Quantitative interaction proteomics and genomewide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
63. Walsh CP, Chaillet JR, Bestor TH. 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20: 116-117.
64. Weber P, Cammas F, Gerard C, Metzger D, Chambon P, Losson R, Mark M. 2002. Germ cell expression of the transcriptional co-repressor TIF1b is required for the maintenance of spermatogenesis in the mouse. Development 129: 2329-2337.
65. Wolf D, Goff SP. 2008. Host restriction factors blocking retroviral replication. Annu Rev Genet 42: 143-163.
66. Zhang Y, Yang X, Gui B, Xie G, Zhang D, Shang Y, Liang J. 2011. Corepressor protein CDYL functions as a molecular bridge between polycomb repressor complex 2 and repressive chromatin mark trimethylated histone lysine 27. J Biol Chem 286: 42414-42425.