Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment

Development

Volumn 137, Issue 15, 2010, Pages 2483-2492

  Alder, Olivia ^a   Lavial, Fabrice ^a   Helness, Anne ^a   Brookes, Emily ^a   Pinho, Sandra ^a   Chandrashekran, Anil ^a   Arnaud, Philippe ^b   Pombo, Ana ^a   O'Neill, Laura ^c   Azuara, Véronique ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^c UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

Author keywords

Bivalent chromatin; Early development; Histone methylation; Mouse; Silencing; Stem cells

Indexed keywords

HISTONE; PROTEIN RING 1 B; PROTEIN SUV 39 H 1; RNA POLYMERASE II; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLASTOCYST; CHROMATIN; CONTROLLED STUDY; DNA METHYLATION; EMBRYO; FEMALE; GENE SILENCING; IN VIVO STUDY; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; STEM CELL; TROPHOBLAST;

ANIMALS; BLASTOCYST; CELL LINEAGE; CHROMATIN; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; METHYLTRANSFERASES; MICE; MODELS, BIOLOGICAL; REPRESSOR PROTEINS; RNA INTERFERENCE; RNA POLYMERASE II; TROPHOBLASTS;

EID: 77955759070     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.048363     Document Type: Article

References (68)

1. Arney, K. L., Bao, S., Bannister, A. J., Kouzarides, T. and Surani, M. A. (2002). Histone methylation defines epigenetic asymmetry in the mouse zygote. Int. J. Dev. Biol. 46, 317-320.
2. Atsuta, T., Fujimura, S., Moriya, H., Vidal, M., Akasaka, T. and Koseki, H. (2001). Production of monoclonal antibodies against mammalian Ring1B proteins. Hybridoma 20, 43-46.
3. Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jorgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M. et al. (2006). Chromatin signatures of pluripotent cell lines. Nat. Cell Biol. 8, 532-538.
4. Bantignies, F. and Cavalli, G. (2006). Cellular memory and dynamic regulation of polycomb group proteins. Curr. Opin. Cell Biol. 18, 275-283.
5. Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007). High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837. (Pubitemid 46802390)
6. Bernstein, B. E., Mikkelsen, T. S., Xie, X., Kamal, M., Huebert, D. J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006a). A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326.
7. Bernstein, E., Duncan, E. M., Masui, O., Gil, J., Heard, E. and Allis, C. D. (2006b). Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol. Cell. Biol. 26, 2560-2569.
8. Bilodeau, S., Kagey, M. H., Frampton, G. M., Rahl, P. B. and Young, R. A. (2009). SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev. 23, 2484-2489.
9. Bird, A. (2002). DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21.
10. Boyer, L. A., Plath, K., Zeitlinger, J., Brambrink, T., Medeiros, L. A., Lee, T. I., Levine, S. S., Wernig, M., Tajonar, A., Ray, M. K. et al. (2006). Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441, 349-353.
11. Bracken, A. P., Dietrich, N., Pasini, D., Hansen, K. H. and Helin, K. (2006). Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20, 1123-1136.
12. Brookes, E. and Pombo, A. (2009). Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep. 10, 1213-1219.
13. Chamberlain, S. J., Yee, D. and Magnuson, T. (2008). Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26, 1496-1505.
14. Cloos, P. A., Christensen, J., Agger, K., Maiolica, A., Rappsilber, J., Antal, T., Hansen, K. H. and Helin, K. (2006). The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 442, 307-311.
15. Cui, K., Zang, C., Roh, T. Y., Schones, D. E., Childs, R. W., Peng, W. and Zhao, K. (2009). Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4, 80-93.
16. de Napoles, M., Mermoud, J. E., Wakao, R., Tang, Y. A., Endoh, M., Appanah, R., Nesterova, T. B., Silva, J., Otte, A. P., Vidal, M. et al. (2004). Polycomb group proteins Ring1A/B link ubiquitylation of histone H2A to heritable gene silencing and X inactivation. Dev. Cell 7, 663-676.
17. Delaval, K. and Feil, R. (2004). Epigenetic regulation of mammalian genomic imprinting. Curr. Opin. Genet. Dev. 14, 188-195. (Pubitemid 38520147)
18. Dietrich, J. E. and Hiiragi, T. (2007). Stochastic patterning in the mouse preimplantation embryo. Development 134, 4219-4231.
19. Endoh, M., Endo, T. A., Endoh, T., Fujimura, Y., Ohara, O., Toyoda, T., Otte, A. P., Okano, M., Brockdorff, N., Vidal, M. et al. (2008). Polycomb group proteins Ring1A/B are functionally linked to the core transcriptional regulatory circuitry to maintain ES cell identity. Development 135, 1513-1524. (Pubitemid 351753641)
20. Epsztejn-Litman, S., Feldman, N., Abu-Remaileh, M., Shufaro, Y., Gerson, A., Ueda, J., Deplus, R., Fuks, F., Shinkai, Y., Cedar, H. et al. (2008). De novo DNA methylation promoted by G9a prevents reprogramming of embryonically silenced genes. Nat. Struct. Mol. Biol. 15, 1176-1183.
21. Fang, J., Chen, T., Chadwick, B., Li, E. and Zhang, Y. (2004). Ring1b-mediated H2A ubiquitination associates with inactive X chromosomes and is involved in initiation of X inactivation. J. Biol. Chem. 279, 52812-52815.
22. Farthing, C. R., Ficz, G., Ng, R. K., Chan, C. F., Andrews, S., Dean, W., Hemberger, M. and Reik, W. (2008). Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet. 4, e1000116. (Pubitemid 351914802)
23. Fuks, F., Hurd, P. J., Deplus, R. and Kouzarides, T. (2003). The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucleic Acids Res. 31, 2305-2312.
24. Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R. and Young, R. A. (2007). A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130, 77-88.
25. Jaenisch, R. and Young, R. (2008). Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582.
26. Jedrusik, A., Parfitt, D. E., Guo, G., Skamagki, M., Grabarek, J. B., Johnson, M. H., Robson, P. and Zernicka-Goetz, M. (2008). Role of Cdx2 and cell polarity in cell allocation and specification of trophectoderm and inner cell mass in the mouse embryo. Genes Dev. 22, 2692-2706.
27. Jorgensen, H. F., Giadrossi, S., Casanova, M., Endoh, M., Koseki, H., Brockdorff, N. and Fisher, A. G. (2006). Stem cells primed for action: polycomb repressive complexes restrain the expression of lineage-specific regulators in embryonic stem cells. Cell Cycle 5, 1411-1414.
28. Ku, M., Koche, R. P., Rheinbay, E., Mendenhall, E. M., Endoh, M., Mikkelsen, T. S., Presser, A., Nusbaum, C., Xie, X., Chi, A. S. et al. (2008). Genome-wide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242.
29. Kutner, R. H., Zhang, X. Y. and Reiser, J. (2009). Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat. Protoc. 4, 495-505.
30. Lande-Diner, L. and Cedar, H. (2005). Silence of the genes-mechanisms of long-term repression. Nat. Rev. Genet. 6, 648-654.
31. Lee, T. I., Jenner, R. G., Boyer, L. A., Guenther, M. G., Levine, S. S., Kumar, R. M., Chevalier, B., Johnstone, S. E., Cole, M. F., Isono, K. et al. (2006). Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125, 301-313.
32. Leeb, M. and Wutz, A. (2007). Ring1B is crucial for the regulation of developmental control genes and PRC1 proteins but not X inactivation in embryonic cells. J. Cell Biol. 178, 219-229. (Pubitemid 47076459)
33. Loh, Y.-H., Zhang, W., Chen, X., George, J. and Ng, H.-H. (2008). Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes & Development 21, 2545-2547.
34. Mak, W., Nesterova, T. B., de Napoles, M., Appanah, R., Yamanaka, S., Otte, A. P. and Brockdorff, N. (2004). Reactivation of the paternal X chromosome in early mouse embryos. Science 303, 666-669. (Pubitemid 38141631)
35. Matoba, R., Niwa, H., Masui, S., Ohtsuka, S., Carter, M. G., Sharov, A. A. and Ko, M. S. (2006). Dissecting Oct3/4-regulated gene networks in embryonic stem cells by expression profiling. PLoS ONE 1, e26.
36. Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B. et al. (2008). Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770.
37. Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T. K., Koche, R. P. et al. (2007). Genomewide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553-560.
38. Mohn, F., Weber, M., Rebhan, M., Roloff, T. C., Richter, J., Stadler, M. B., Bibel, M. and Schubeler, D. (2008). Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766.
39. Niwa, H., Miyazaki, J. and Smith, A. G. (2000). Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24, 372-376.
40. Ohm, J. E., McGarvey, K. M., Yu, X., Cheng, L., Schuebel, K. E., Cope, L., Mohammad, H. P., Chen, W., Daniel, V. C., Yu, W. et al. (2007). A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 39, 237-242.
41. O'Neill, L. P., VerMilyea, M. D. and Turner, B. M. (2006). Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations. Nat. Genet. 38, 835-841.
42. Otte, A. P. and Kwaks, T. H. (2003). Gene repression by Polycomb group protein complexes: a distinct complex for every occasion? Curr. Opin. Genet. Dev. 13, 448-454.
43. Pan, G., Tian, S., Nie, J., Yang, C., Ruotti, V., Wei, H., Jonsdottir, G. A., Stewart, R. and Thomson, J. A. (2007). Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1, 299-312.
44. Peters, A. H., O'Carroll, D., Scherthan, H., Mechtler, K., Sauer, S., Schofer, C., Weipoltshammer, K., Pagani, M., Lachner, M., Kohlmaier, A. et al. (2001). Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107, 323-337.
45. Pietersen, A. M. and van Lohuizen, M. (2008). Stem cell regulation by polycomb repressors: postponing commitment. Curr. Opin. Cell Biol. 20, 201-207.
46. Probst, A. V., Santos, F., Reik, W., Almouzni, G. and Dean, W. (2007). Structural differences in centromeric heterochromatin are spatially reconciled on fertilisation in the mouse zygote. Chromosoma 116, 403-415. (Pubitemid 46995578)
47. Puschendorf, M., Terranova, R., Boutsma, E., Mao, X., Isono, K., Brykczynska, U., Kolb, C., Otte, A. P., Koseki, H., Orkin, S. H. et al. (2008). PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat. Genet. 40, 411-420.
48. Reik, W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432. (Pubitemid 46816749)
49. Ringrose, L. and Paro, R. (2007). Polycomb/Trithorax response elements and epigenetic memory of cell identity. Development 134, 223-232. (Pubitemid 46252409)
50. Roh, T. Y., Cuddapah, S., Cui, K. and Zhao, K. (2006). The genomic landscape of histone modifications in human T cells. Proc. Natl. Acad. Sci. USA 103, 15782-15787. (Pubitemid 44657544)
51. Rossant, J. and Tam, P. P. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
52. Santos, F., Peters, A. H., Otte, A. P., Reik, W. and Dean, W. (2005). Dynamic chromatin modifications characterise the first cell cycle in mouse embryos. Dev. Biol. 280, 225-236. (Pubitemid 40342755)
53. Sanz, L. A., Chamberlain, S., Sabourin, J. C., Henckel, A., Magnuson, T., Hugnot, J. P., Feil, R. and Arnaud, P. (2008). A mono-allelic bivalent chromatin domain controls tissue-specific imprinting at Grb10. EMBO J. 27, 2523-2532.
54. Schuettengruber, B. and Cavalli, G. (2009). Recruitment of polycomb group complexes and their role in the dynamic regulation of cell fate choice. Development 136, 3531-3542.
55. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B. and Cavalli, G. (2007). Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745. (Pubitemid 46273581)
56. Schwartz, Y. B. and Pirrotta, V. (2007). Polycomb silencing mechanisms and the management of genomic programmes. Nat. Rev. Genet. 8, 9-22.
57. Simon, J. A. and Kingston, R. E. (2009). Mechanisms of polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697-708.
58. Solter, D. and Knowles, B. B. (1975). Immunosurgery of mouse blastocyst. Proc. Natl. Acad. Sci. USA 72, 5099-5102.
59. Stock, J. K., Giadrossi, S., Casanova, M., Brookes, E., Vidal, M., Koseki, H., Brockdorff, N., Fisher, A. G. and Pombo, A. (2007). Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 9, 1428-1435. (Pubitemid 350201756)
60. van der Stoop, P., Boutsma, E. A., Hulsman, D., Noback, S., Heimerikx, M., Kerkhoven, R. M., Voncken, J. W., Wessels, L. F. and van Lohuizen, M. (2008). Ubiquitin E3 ligase Ring1b/Rnf2 of polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells. PLoS ONE 3, e2235.
61. VerMilyea, M. D., O'Neill, L. P. and Turner, B. M. (2009). Transcription-independent heritability of induced histone modifications in the mouse preimplantation embryo. PLoS ONE 4, e6086.
62. Voncken, J. W., Roelen, B. A., Roefs, M., de Vries, S., Verhoeven, E., Marino, S., Deschamps, J. and van Lohuizen, M. (2003). Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition. Proc. Natl. Acad. Sci. USA 100, 2468-2473.
63. Wang, J., Zhang, M., Zhang, Y., Kou, Z., Han, Z., Chen, D. Y., Sun, Q. Y. and Gao, S. (2009). The histone demethylase JMJD2C is stage-specifically expressed in preimplantation mouse embryos and is required for embryonic development. Biol. Reprod. 82, 101-111.
64. Weber, M. and Schubeler, D. (2007). Genomic patterns of DNA methylation: targets and function of an epigenetic mark. Curr. Opin. Cell Biol. 19, 273-280.
65. Wei, G., Wei, L., Zhu, J., Zang, C., Hu-Li, J., Yao, Z., Cui, K., Kanno, Y., Roh, T. Y., Watford, W. T. et al. (2009). Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155-167.
66. Wissmann, M., Yin, N., Muller, J. M., Greschik, H., Fodor, B. D., Jenuwein, T., Vogler, C., Schneider, R., Gunther, T., Buettner, R. et al. (2007). Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell Biol. 9, 347-353.
67. Yuan, P., Han, J., Guo, G., Orlov, Y. L., Huss, M., Loh, Y. H., Yaw, L. P., Robson, P., Lim, B. and Ng, H. H. (2009). Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev. 23, 2507-2520.
68. Zhao, X. D., Han, X., Chew, J. L., Liu, J., Chiu, K. P., Choo, A., Orlov, Y. L., Sung, W. K., Shahab, A., Kuznetsov, V. A. 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.