Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity

PLoS Genetics

Volumn 8, Issue 7, 2012, Pages

  Endoh, Mitsuhiro ^a,b   Endo, Takaho A ^c   Endoh, Tamie ^a   Isono, Kyo ichi ^a   Sharif, Jafar ^a   Ohara, Osamu ^a   Toyoda, Tetsuro ^c   Ito, Takashi ^d   Eskeland, Ragnhild ^e   Bickmore, Wendy A ^e   Vidal, Miguel ^a,f   Bernstein, Bradley E ^g,h,i   Koseki, Haruhiko ^a,b  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c RIKEN   (Japan)

^d NAGASAKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

ⁱ BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; HISTONE H2AK119U1; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1; PROTEIN RING1A; PROTEIN RING1B; RING FINGER PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL DIFFERENTIATION; CELL IDENTITY; CELLULAR PARAMETERS; CHROMATIN; CHROMATIN COMPACTION; COMPLEX FORMATION; DEVELOPMENTAL GENE; EMBRYONIC STEM CELL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; GENE REPRESSION; GENE SILENCING; GENETIC ASSOCIATION; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINE; CHROMATIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYCOMB REPRESSIVE COMPLEX 1; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84864585700     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002774     Document Type: Article

References (40)

1. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
2. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
3. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
4. Kim J, Chu J, Shen X, Wang J, Orkin SH, (2008) An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061.
5. Endoh M, Endo TA, Endoh T, Fujimura Y, Ohara O, 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.
6. van der Stoop P, Boutsma EA, Hulsman D, Noback S, Heimerikx M, et al. (2008) Ubiquitin E3 ligase Ring1b/Rnf2 of polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells. PLoS ONE 3: e2235 doi:10.1371/journal.pone.0002235.
7. Dahle O, Kumar A, Kuehn MR Nodal signaling recruits the histone demethylase Jmjd3 to counteract polycomb-mediated repression at target genes. Sci Signal 3: ra48.
8. Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K, (2007) The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol Cell Biol 27: 3769-3779.
9. Leeb M, 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.
10. Shao Z, Raible F, Mollaaghababa R, Guyon JR, Wu CT, et al. (1999) Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98: 37-46.
11. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
12. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
13. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043.
14. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D, (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
15. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, et al. (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881.
16. Bernstein E, Duncan EM, Masui O, Gil J, Heard E, et al. (2006) Mouse polycomb proteins bind differentially to methylated histone H3 and RNA and are enriched in facultative heterochromatin. Mol Cell Biol 26: 2560-2569.
17. Buchwald G, van der Stoop P, Weichenrieder O, Perrakis A, van Lohuizen M, et al. (2006) Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. Embo J 25: 2465-2474.
18. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, et al. (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature 431: 873-878.
19. Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, et al. (2007) Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 9: 1428-1435.
20. de Napoles M, Mermoud JE, Wakao R, Tang YA, Endoh 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.
21. Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, et al. (1999) Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 207: 322-333.
22. Kallin EM, Cao R, Jothi R, Xia K, Cui K, et al. (2009) Genome-wide uH2A localization analysis highlights Bmi1-dependent deposition of the mark at repressed genes. PLoS Genet 5: e1000506 doi:10.1371/journal.pgen.1000506.
23. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S, et al. (2010) Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 38: 452-464.
24. Francis NJ, Kingston RE, Woodcock CL, (2004) Chromatin compaction by a polycomb group protein complex. Science 306: 1574-1577.
25. Cao R, Tsukada Y, Zhang Y, (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol Cell 20: 845-854.
26. Fujimura Y, Isono K, Vidal M, Endoh M, Kajita H, et al. (2006) Distinct roles of Polycomb group gene products in transcriptionally repressed and active domains of Hoxb8. Development 133: 2371-2381.
27. Richly H, Rocha-Viegas L, Ribeiro JD, Demajo S, Gundem G, et al. (2010) Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 468: 1124-1128.
28. Nakagawa T, Kajitani T, Togo S, Masuko N, Ohdan H, et al. (2008) Deubiquitylation of histone H2A activates transcriptional initiation via trans-histone cross-talk with H3K4 di- and trimethylation. Genes Dev 22: 37-49.
29. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, et al. (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123: 917-929.
30. Singh AM, Hamazaki T, Hankowski KE, Terada N, (2007) A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25: 2534-2542.
31. Ben-Saadon R, Zaaroor D, Ziv T, Ciechanover A, (2006) The polycomb protein Ring1B generates self atypical mixed ubiquitin chains required for its in vitro histone H2A ligase activity. Mol Cell 24: 701-711.
32. Ying QL, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-523.
33. Joo HY, Zhai L, Yang C, Nie S, Erdjument-Bromage H, et al. (2007) Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449: 1068-1072.
34. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538.
35. Atsuta T, Fujimura S, Moriya H, Vidal M, Akasaka T, et al. (2001) Production of monoclonal antibodies against mammalian Ring1B proteins. Hybridoma 20: 43-46.
36. Schoorlemmer J, Marcos-Gutierrez C, Were F, Martinez R, Garcia E, et al. (1997) Ring1A is a transcriptional repressor that interacts with the Polycomb-M33 protein and is expressed at rhombomere boundaries in the mouse hindbrain. EMBO J 16: 5930-5942.
37. Miyagishima H, Isono K, Fujimura Y, Iyo M, Takihara Y, et al. (2003) Dissociation of mammalian Polycomb-group proteins, Ring1B and Rae28/Ph1, from the chromatin correlates with configuration changes of the chromatin in mitotic and meiotic prophase. Histochem Cell Biol 120: 111-119.
38. Orlando V, Strutt H, Paro R, (1997) Analysis of chromatin structure by in vivo formaldehyde cross-linking. Methods 11: 205-214.
39. van Bakel H, van Werven FJ, Radonjic M, Brok MO, van Leenen D, et al. (2008) Improved genome-wide localization by ChIP-chip using double-round T7 RNA polymerase-based amplification. Nucleic Acids Res 36: e21.
40. Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, et al. (2002) Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res 276: 10-23.