Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice

Developmental Biology

Volumn 278, Issue 2, 2005, Pages 440-458

  Seki, Yoshiyuki ^a,b,c,d   Hayashi, Katsuhiko ^a,c   Itoh, Kunihiko ^e   Mizugaki, Michinao ^f   Saitou, Mitinori ^c,d,g   Matsui, Yasuhisa ^a,b,c,h  

^a RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d RIKEN KOBE INSTITUTE   (Japan)

^e AKITA UNIVERSITY HOSPITAL   (Japan)

^f TOHOKU PHARMACEUTICAL UNIVERSITY   (Japan)

^g KYOTO UNIVERSITY   (Japan)

^h TOHOKU UNIVERSITY   (Japan)

Author keywords

DNA methylation; Epigenetics; Germ cells; Histone modification; Reprogramming; Transcriptional repression

Indexed keywords

ANIMAL CELL; ARTICLE; CELL MIGRATION; CENTROMERE; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GAMETE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOME; GERM CELL; GONAD; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 12944308793     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.11.025     Document Type: Article

References (53)

1. R. Anderson, T.K. Copeland, H. Scholer, J. Heasman, and C. Wylie The onset of germ cell migration in the mouse embryo Mech. Dev. 91 2000 61 68
2. K.L. Arney, S. Bao, A.J. Bannister, T. Kouzarides, and M.A. Surani Histone methylation defines epigenetic asymmetry in the mouse zygote Int. J. Dev. Biol. 46 2002 317 320
3. C. Batchelder, M.A. Dunn, B. Choy, Y. Suh, C. Cassie, E.Y. Shim, T.H. Shin, C. Mello, G. Seydoux, and T.K. Blackwell Transcriptional repression by the Caenorhabditis elegans germ-line protein PIE-1 Genes Dev. 13 1999 202 212
4. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21
5. S. Erhardt, I.H. Su, R. Schneider, S. Barton, A.J. Bannister, L. Perez-Burgos, T. Jenuwein, T. Kouzarides, A. Tarakhovsky, and M.A. Surani Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development Development 130 2003 4235 4248
6. N. Fujita, S. Watanabe, T. Ichimura, S. Tsuruzoe, Y. Shinkai, M. Tachibana, T. Chiba, and M. Nakao Methyl-CpG binding domain 1 (MBD1) interacts with the Suv39h1-HP1 heterochromatic complex for DNA methylation-based transcriptional repression J. Biol. Chem. 278 2003 24132 24138 (Electronic publication 2003 Apr. 23)
7. N. Geijsen, M. Horoschak, K. Kim, J. Gribnau, K. Eggan, and G.Q. Daley Derivation of embryonic germ cells and male gametes from embryonic stem cells Nature 427 2004 148 154
8. M. Ginsburg, M.H. Snow, and A. McLaren Primordial germ cells in the mouse embryo during gastrulation Development 110 1990 521 528
9. P. Hajkova, S. Erhardt, N. Lane, T. Haaf, O. El-Maarri, W. Reik, J. Walter, and M.A. Surani Epigenetic reprogramming in mouse primordial germ cells Mech. Dev. 117 2002 15 23
10. T. Hashimshony, J. Zhang, I. Keshet, M. Bustin, and H. Cedar The role of DNA methylation in setting up chromatin structure during development Nat. Genet. 34 2003 187 192
11. R. Holdeman, S. Nehrt, and S. Strome MES-2, a maternal protein essential for viability of the germline in Caenorhabditis elegans, is homologous to a Drosophila Polycomb group protein Development 125 1998 2457 2467
12. K. Hubner, G. Fuhrmann, L.K. Christenson, J. Kehler, R. Reinbold, R. De La Fuente, J. Wood, I.J. Strauss, M. Boiani, and H.R. Scholer Derivation of oocytes from mouse embryonic stem cells Science 1 2003 1
13. J.P. Jackson, A.M. Lindroth, X. Cao, and S.E. Jacobsen Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase Nature 416 2002 556 560
14. S.A. Jacobs, and S. Khorasanizadeh Structure of HP1 chromodomain bound to a lysine 9-methylated histone H3 tail Science 295 2002 2080 2083
15. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080
16. M. Lachner, D. O'Carroll, S. Rea, K. Mechtler, and T. Jenuwein Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins Nature 410 2001 116 120
17. M. Lachner, R.J. O'Sullivan, and T. Jenuwein An epigenetic road map for histone lysine methylation J. Cell Sci. 116 2003 2117 2124
18. N. Lane, W. Dean, S. Erhardt, P. Hajkova, A. Surani, J. Walter, and W. Reik Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse Genesis 35 2003 88 93
19. K.A. Lawson, and W.J. Hage Clonal analysis of the origin of primordial germ cells in the mouse Ciba Found. Symp. 182 1994 68 84 (Discussion 84-91)
20. K.A. Lawson, N.R. Dunn, B.A. Roelen, L.M. Zeinstra, A.M. Davis, C.V. Wright, J.P. Korving, and B.L. Hogan Bmp4 is required for the generation of primordial germ cells in the mouse embryo Genes Dev. 13 1999 424 436
21. B. Lehnertz, Y. Ueda, A.A. Derijck, U. Braunschweig, L. Perez-Burgos, S. Kubicek, T. Chen, E. Li, T. Jenuwein, and A.H. Peters Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin Curr. Biol. 13 2003 1192 1200
22. E. Li Chromatin modification and epigenetic reprogramming in mammalian development Nat. Rev., Genet. 3 2002 662 673
23. E. Li, T.H. Bestor, and R. Jaenisch Targeted mutation of the DNA methyltransferase gene results in embryonic lethality Cell 69 1992 915 926
24. H. Liu, J.M. Kim, and F. Aoki Regulation of histone H3 lysine 9 methylation in oocytes and early pre-implantation embryos Development 131 2004 2269 2280 (Electronic publication 2004 Apr. 21)
25. W. Mayer, A. Niveleau, J. Walter, R. Fundele, and T. Haaf Demethylation of the zygotic paternal genome Nature 403 2000 501 502
26. K.A. Molyneaux, J. Stallock, K. Schaible, and C. Wylie Time-lapse analysis of living mouse germ cell migration Dev. Biol. 240 2001 488 498
27. D. O'Carroll, S. Erhardt, M. Pagani, S.C. Barton, M.A. Surani, and T. Jenuwein The polycomb-group gene Ezh2 is required for early mouse development Mol. Cell. Biol. 21 2001 4330 4336
28. M. Okano, D.W. Bell, D.A. Haber, and E. Li DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development Cell 99 1999 247 257
29. J. Oswald, S. Engemann, N. Lane, W. Mayer, A. Olek, R. Fundele, W. Dean, W. Reik, and J. Walter Active demethylation of the paternal genome in the mouse zygote Curr. Biol. 10 2000 475 478
30. M. Pesce, and M. De Felici Purification of mouse primordial germ cells by MiniMACS magnetic separation system Dev. Biol. 170 1995 722 725
31. A.H. Peters, D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, C. Schofer, K. Weipoltshammer, M. Pagani, M. Lachner, A. Kohlmaier, S. Opravil, M. Doyle, M. Sibilia, and T. Jenuwein Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability Cell 107 2001 323 337
32. A.H. Peters, S. Kubicek, K. Mechtler, R.J. O'Sullivan, A.A. Derijck, L. Perez-Burgos, A. Kohlmaier, S. Opravil, M. Tachibana, Y. Shinkai, J.H. Martens, and T. Jenuwein Partitioning and plasticity of repressive histone methylation states in mammalian chromatin Mol. Cell 12 2003 1577 1589
33. K. Plath, J. Fang, S.K. Mlynarczyk-Evans, R. Cao, K.A. Worringer, H. Wang, C.C. de la Cruz, A.P. Otte, B. Panning, and Y. Zhang Role of histone H3 lysine 27 methylation in X inactivation Science 300 2003 131 135
34. N. Rougier, D. Bourc'his, D.M. Gomes, A. Niveleau, M. Plachot, A. Paldi, and E. Viegas-Pequignot Chromosome methylation patterns during mammalian preimplantation development Genes Dev. 12 1998 2108 2113
35. M. Saitou, S.C. Barton, and M.A. Surani A molecular programme for the specification of germ cell fate in mice Nature 418 2002 293 300
36. M. Saitou, B. Payer, U.C. Lange, S. Erhardt, S.C. Barton, and M.A. Surani Specification of germ cell fate in mice Philos. Trans. R. Soc. Lond., B Biol. Sci. 358 2003 1363 1370
37. Y. Sakai, I. Suetake, K. Itoh, M. Mizugaki, S. Tajima, and S. Yamashina Expression of DNA methyltransferase (Dnmt1) in testicular germ cells during development of mouse embryo Cell Struct. Funct. 26 2001 685 691
38. J. Sanford, L. Forrester, V. Chapman, A. Chandley, and N. Hastie Methylation patterns of repetitive DNA sequences in germ cells of Mus musculus Nucleic Acids Res. 12 1984 2823 2836
39. S. Sato, T. Yoshimizu, E. Sato, and Y. Matsui Erasure of methylation imprinting of Igf2r during mouse primordial germ-cell development Mol. Reprod. Dev. 65 2003 41 50
40. C.E. Schaner, G. Deshpande, P.D. Schedl, and W.G. Kelly A conserved chromatin architecture marks and maintains the restricted germ cell lineage in worms and flies Dev. Cell 5 2003 747 757
41. G. Seydoux, and M.A. Dunn Transcriptionally repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of Caenorhabditis elegans and Drosophila melanogaster Development 124 1997 2191 2201
42. G. Seydoux, and S. Strome Launching the germline in Caenorhabditis elegans: regulation of gene expression in early germ cells Development 126 1999 3275 3283
43. J. Silva, W. Mak, I. Zvetkova, R. Appanah, T.B. Nesterova, Z. Webster, A.H. Peters, T. Jenuwein, A.P. Otte, and N. Brockdorff Establishment of histone h3 methylation on the inactive X chromosome requires transient recruitment of Eed-Enx1 polycomb group complexes Dev. Cell 4 2003 481 495
44. W.J. Soppe, Z. Jasencakova, A. Houben, T. Kakutani, A. Meister, M.S. Huang, S.E. Jacobsen, I. Schubert, and P.F. Fransz DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis EMBO J. 21 2002 6549 6559
45. M.A. Surani Reprogramming of genome function through epigenetic inheritance Nature 414 2001 122 128
46. M. Tachibana, K. Sugimoto, M. Nozaki, J. Ueda, T. Ohta, M. Ohki, M. Fukuda, N. Takeda, H. Niida, H. Kato, and Y. Shinkai G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis Genes Dev. 16 2002 1779 1791
47. P.P. Tam, and M.H. Snow Proliferation and migration of primordial germ cells during compensatory growth in mouse embryos J. Embryol. Exp. Morphol. 64 1981 133 147
48. P.P. Tam, S.X. Zhou, and S.S. Tan X-chromosome activity of the mouse primordial germ cells revealed by the expression of an X-linked lacZ transgene Development 120 1994 2925 2932
49. H. Tamaru, and E.U. Selker A histone H3 methyltransferase controls DNA methylation in Neurospora crassa Nature 414 2001 277 283
50. Y. Toyooka, N. Tsunekawa, R. Akasu, and T. Noce Embryonic stem cells can form germ cells in vitro Proc. Natl. Acad. Sci. U. S. A. 100 2003 11457 11462 (Electronic publication 2003 Sep 22)
51. D. Watanabe, I. Suetake, T. Tada, and S. Tajima Stage- and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis Mech. Dev. 118 2002 187 190
52. J.A. Yoder, C.P. Walsh, and T.H. Bestor Cytosine methylation and the ecology of intragenomic parasites Trends Genet. 13 1997 335 340
53. T. Yoshimizu, N. Sugiyama, M. De Felice, Y.I. Yeom, K. Ohbo, K. Masuko, M. Obinata, K. Abe, H.R. Scholer, and Y. Matsui Germline-specific expression of the Oct-4/green fluorescent protein (GFP) transgene in mice Dev. Growth Differ. 41 1999 675 684