Prc1 and prc2 are not required for targeting of h2a.z to developmental genes in embryonic stem cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Illingworth, Robert S ^a   Botting, Catherine H ^b   Grimes, Graeme R ^a   Bickmore, Wendy A ^a   Eskeland, Ragnhild ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AZ; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 1; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN RING1B; PROTEIN SUZ12; UNCLASSIFIED DRUG; EED PROTEIN, MOUSE; HISTONE; REPRESSOR PROTEIN; RNF2 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CPG ISLAND; DEVELOPMENTAL GENE; EMBRYONIC STEM CELL; GENE LOCUS; GENE SILENCING; GENE TARGETING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TARGETING; ANIMAL; CELL LINE; CHROMATIN; GENETICS; METABOLISM; MOUSE; PROMOTER REGION;

ANIMALS; CELL LINE; CHROMATIN; CPG ISLANDS; EMBRYONIC STEM CELLS; GENES, DEVELOPMENTAL; GENETIC LOCI; HISTONES; MICE; PROMOTER REGIONS, GENETIC; REPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84859501917     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034848     Document Type: Article

References (69)

1. Talbert PB, Henikoff S, (2010) Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
2. Zlatanova J, Thakar A, (2008) H2A.Z: view from the top. Structure 16: 166-179.
3. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, et al. (2008) Nucleosome organization in the Drosophila genome. Nature 453: 358-362.
4. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones DE, et al. (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
5. Gevry N, Hardy S, Jacques PE, Laflamme L, Svotelis A, et al. (2009) Histone H2A.Z is essential for estrogen receptor signaling. Genes Dev 23: 1522-1533.
6. Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, et al. (2005) Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123: 233-248.
7. Shia WJ, Li B, Workman JL, (2006) SAS-mediated acetylation of histone H4 Lys 16 is required for H2A.Z incorporation at subtelomeric regions in Saccharomyces cerevisiae. Genes Dev 20: 2507-2512.
8. Meneghini MD, Wu M, Madhani HD, (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725-736.
9. Sarcinella E, Zuzarte PC, Lau PN, Draker R, Cheung P, (2007) Monoubiquitylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol 27: 6457-6468.
10. Rangasamy D, Berven L, Ridgway P, Tremethick DJ, (2003) Pericentric heterochromatin becomes enriched with H2A.Z during early mammalian development. Embo J 22: 1599-1607.
11. Swaminathan J, Baxter EM, Corces VG, (2005) The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev 19: 65-76.
12. Fan JY, Rangasamy D, Luger K, Tremethick DJ, (2004) H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding. Mol Cell 16: 655-661.
13. Creyghton MP, Markoulaki S, Levine SS, Hanna J, Lodato MA, et al. (2008) H2AZ Is Enriched at Polycomb Complex Target Genes in ES Cells and Is Necessary for Lineage Commitment. Cell 135: 649-661.
14. Margueron R, Reinberg D, (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
15. Simon JA, Kingston RE, (2009) Mechanisms of Polycomb gene silencing: knowns and unknowns. Nature Reviews Molecular Cell Biology pp. 1-12.
16. Gevry N, Chan HM, Laflamme L, Livingston DM, Gaudreau L, (2007) p21 transcription is regulated by differential localization of histone H2A.Z. Genes Dev 21: 1869-1881.
17. Martinato F, Cesaroni M, Amati B, Guccione E, (2008) Analysis of Myc-induced histone modifications on target chromatin. PLoS One 3: e3650.
18. Ruhl DD, Jin J, Cai Y, Swanson S, Florens L, et al. (2006) Purification of a human SRCAP complex that remodels chromatin by incorporating the histone variant H2A.Z into nucleosomes. Biochemistry 45: 5671-5677.
19. Lu PY, Levesque N, Kobor MS, (2009) NuA4 and SWR1-C: two chromatin-modifying complexes with overlapping functions and components. Biochem Cell Biol 87: 799-815.
20. Fazzio TG, Huff JT, Panning B, (2008) An RNAi screen of chromatin proteins identifies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134: 162-174.
21. Gearhart MD, Corcoran CM, Wamstad JA, Bardwell VJ, (2006) Polycomb Group and SCF Ubiquitin Ligases Are Found in a Novel BCOR Complex That Is Recruited to BCL6 Targets. Molecular and Cellular Biology 26: 6880-6889.
22. Sanchez C, Sanchez I, Demmers JA, Rodriguez P, Strouboulis J, et al. (2007) Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor. Mol Cell Proteomics 6: 820-834.
23. 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.
24. Elderkin S, Maertens GN, Endoh M, Mallery DL, Morrice N, et al. (2007) A phosphorylated form of Mel-18 targets the Ring1B histone H2A ubiquitin ligase to chromatin. Mol Cell 28: 107-120.
25. Levine SS, Weiss A, Erdjument-Bromage H, Shao Z, Tempst P, et al. (2002) The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans. Mol Cell Biol 22: 6070-6078.
26. 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.
27. Vidal M, (2009) Role of polycomb proteins Ring1A and Ring1B in the epigenetic regulation of gene expression. Int J Dev Biol 53: 355-370.
28. Gambetta MC, Oktaba K, Muller J, (2009) Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science 325: 93-96.
29. Sinclair DA, Syrzycka M, Macauley MS, Rastgardani T, Komljenovic I, et al. (2009) Drosophila O-GlcNAc transferase (OGT) is encoded by the Polycomb group (PcG) gene, super sex combs (sxc). Proc Natl Acad Sci U S A 106: 13427-13432.
30. Wamstad JA, Corcoran CM, Keating AM, Bardwell VJ, (2008) Role of the transcriptional corepressor Bcor in embryonic stem cell differentiation and early embryonic development. PLoS One 3: e2814.
31. Ogawa H, (2002) A Complex with Chromatin Modifiers That Occupies E2F- and Myc-Responsive Genes in G0 Cells. Science 296: 1132-1136.
32. Trojer P, Cao AR, Gao Z, Li Y, Zhang J, et al. (2011) L3MBTL2 Protein Acts in Concert with PcG Protein-Mediated Monoubiquitination of H2A to Establish a Repressive Chromatin Structure. Mol Cell 42: 438-450.
33. Wynder C, Hakimi MA, Epstein JA, Shilatifard A, Shiekhattar R, (2005) Recruitment of MLL by HMG-domain protein iBRAF promotes neural differentiation. Nat Cell Biol 7: 1113-1117.
34. 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.
35. Negishi M, Saraya A, Miyagi S, Nagao K, Inagaki Y, et al. (2007) Bmi1 cooperates with Dnmt1-associated protein 1 in gene silencing. Biochemical and Biophysical Research Communications 353: 992-998.
36. Fuchs M, Gerber J, Drapkin R, Sif S, Ikura T, et al. (2001) The p400 complex is an essential E1A transformation target. Cell 106: 297-307.
37. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, et al. (2010) Polycomb complexes act redundantly to repress genomic repeats and genes. Genes & Development 24: 265-276.
38. 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.
39. Wang L, Brown JL, Cao R, Zhang Y, Kassis JA, et al. (2004) Hierarchical recruitment of polycomb group silencing complexes. Mol Cell 14: 637-646.
40. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
41. 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.
42. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, et al. (2008) Genomewide Analysis of PRC1 and PRC2 Occupancy Identifies Two Classes of Bivalent Domains. PLoS Genet 4: e1000242.
43. 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.
44. 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.
45. 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.
46. Garrick D, De Gobbi M, Samara V, Rugless M, Holland M, et al. (2008) The role of the polycomb complex in silencing-globin gene expression in nonerythroid cells. Blood 112: 3889-3899.
47. 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. The Journal of Cell Biology 178: 219-229.
48. Ollinger R, Childs AJ, Burgess HM, Speed RM, Lundegaard PR, et al. (2008) Deletion of the pluripotency-associated Tex19.1 gene causes activation of endogenous retroviruses and defective spermatogenesis in mice. PLoS Genet 4: e1000199.
49. 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.
50. Chamberlain SJ, Yee D, Magnuson T, (2008) Polycomb Repressive Complex 2 Is Dispensable for Maintenance of Embryonic Stem Cell Pluripotency. Stem Cells 26: 1496-1505.
51. Pasini D, Bracken AP, Hansen JB, Capillo M, Helin K, (2007) The Polycomb Group Protein Suz12 Is Required for Embryonic Stem Cell Differentiation. Molecular and Cellular Biology 27: 3769-3779.
52. Conerly ML, Teves SS, Diolaiti D, Ulrich M, Eisenman RN, et al. (2010) Changes in H2A.Z occupancy and DNA methylation during B-cell lymphomagenesis. Genome Res 20: 1383-1390.
53. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S, (2008) Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature 456: 125-129.
54. Fouse SD, Shen Y, Pellegrini M, Cole S, Meissner A, et al. (2008) Promoter CpG methylation contributes to ES cell gene regulation in parallel with Oct4/Nanog, PcG complex, and histone H3 K4/K27 trimethylation. Cell Stem Cell 2: 160-169.
55. Mendenhall EM, Koche RP, Truong T, Zhou VW, Issac B, et al. (2010) GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 6: e1001244.
56. Lynch MD, Smith AJ, De Gobbi M, Flenley M, Hughes JR, et al. (2011) An interspecies analysis reveals a key role for unmethylated CpG dinucleotides in vertebrate Polycomb complex recruitment. Embo J 31: 317-329.
57. Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, et al. (2010) A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143: 313-324.
58. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, et al. (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6: 369-381.
59. Myers SA, Panning B, Burlingame AL, (2011) Polycomb repressive complex 2 is necessary for the normal site-specific O-GlcNAc distribution in mouse embryonic stem cells. Proc Natl Acad Sci USA.
60. Lu J, Ruhf ML, Perrimon N, Leder P, (2007) A genome-wide RNA interference screen identifies putative chromatin regulators essential for E2F repression. Proc Natl Acad Sci U S A 104: 9381-9386.
61. Ruhf ML, Braun A, Papoulas O, Tamkun JW, Randsholt N, et al. (2001) The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes. Development 128: 1429-1441.
62. Dou Y, Milne TA, Tackett AJ, Smith ER, Fukuda A, et al. (2005) Physical association and coordinate function of the H3 K4 methyltransferase MLL1 and the H4 K16 acetyltransferase MOF. Cell 121: 873-885.
63. Strubbe G, Popp C, Schmidt A, Pauli A, Ringrose L, et al. (2011) Polycomb purification by in vivo biotinylation tagging reveals cohesin and Trithorax group proteins as interaction partners. Proc Natl Acad Sci U S A 108: 5572-5577.
64. Wright KJ, Marr MT, 2nd, Tjian R, (2006) TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc Natl Acad Sci U S A 103: 12347-12352.
65. Shevchenko A, Wilm M, Vorm O, Jensen ON, Podtelejnikov AV, et al. (1996) A strategy for identifying gel-separated proteins in sequence databases by MS alone. Biochem Soc Trans 24: 893-896.
66. Eskeland R, Czermin B, Boeke J, Bonaldi T, Regula JT, et al. (2004) The N-terminus of Drosophila SU(VAR)3-9 mediates dimerization and regulates its methyltransferase activity. Biochemistry 43: 3740-3749.
67. Luger K, Rechsteiner TJ, Richmond TJ, (1999) Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol Biol 119: 1-16.
68. Vogler C, Huber C, Waldmann T, Ettig R, Braun L, et al. (2010) Histone H2A C-terminus regulates chromatin dynamics, remodeling, and histone H1 binding. PLoS Genet 6: e1001234.
69. Straub T, Grimaud C, Gilfillan GD, Mitterweger A, Becker PB, (2008) The chromosomal high-affinity binding sites for the Drosophila dosage compensation complex. PLoS Genet 4: e1000302.