WHSC1 links transcription elongation to HIRA-mediated histone H3.3 deposition

EMBO Journal

Volumn 32, Issue 17, 2013, Pages 2392-2406

  Sarai, Naoyuki ^a   Nimura, Keisuke ^b   Tamura, Tomohiko ^c   Kanno, Tomohiko ^a   Patel, Mira C ^a   Heightman, Tom D ^d   Ura, Kiyoe ^b,e   Ozato, Keiko ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

BRD4; HIRA; histone H3.3 exchange; transcription elongation; WHSC1

Indexed keywords

CHAPERONE; CYCLIN T1; FLAVOPIRIDOL; HISTONE METHYLTRANSFERASE; INTERFERON; MESSENGER RNA; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN C FOS; PROTEIN C JUN; SHORT HAIRPIN RNA; STAT1 PROTEIN; UNCLASSIFIED DRUG; WOLF HIRSCHHORN SYNDROME CANDIDATE 1;

ARTICLE; CONTROLLED STUDY; DNA BINDING; GENE EXPRESSION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; ULTRAVIOLET RADIATION;

ANIMALS; BASE SEQUENCE; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMATIN; FIBROBLASTS; HISTONE CHAPERONES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; INTERFERON-BETA; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION FACTORS; ULTRAVIOLET RAYS;

EID: 84883304136     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.176     Document Type: Article

References (72)

1. Bartkowiak B, Liu P, Phatnani HP, Fuda NJ, Cooper JJ, Price DH, Adelman K, Lis JT, Greenleaf AL (2010) CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev 24: 2303-2316
2. Bergemann AD, Cole F, Hirschhorn K (2005) The etiology of Wolf- Hirschhorn syndrome. Trends Genet 21: 188-195
3. Carrozza MJ, Li B, Florens L, Suganuma T, Swanson SK, Lee KK, Shia WJ, Anderson S, Yates J, Washburn MP, Workman JL (2005) Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592
4. Chao SH, Fujinaga K, Marion JE, Taube R, Sausville EA, Senderowicz AM, Peterlin BM, Price DH (2000) Flavopiridol inhibits P-TEFb and blocks HIV-1 replication. J Biol Chem 275: 28345-28348
5. Chen S, Dai Y, Pei XY, Myers J, Wang L, Kramer LB, Garnett M, Schwartz DM, Su F, Simmons GL, Richey JD, Larsen DG, Dent P, Orlowski RZ, Grant S (2012) CDK inhibitors upregulate BH3-only proteins to sensitize human myeloma cells to BH3 mimetic therapies. Cancer Res 72: 4225-4237
6. Cooper SJ, Bowden GT (2007) Ultraviolet B regulation of transcription factor families: roles of nuclear factor-kappa B (NF-kappaB) and activator protein-1 (AP-1) in UVB-induced skin carcinogenesis. Curr Cancer Drug Targets 7: 325-334
7. Core LJ, Lis JT (2008) Transcription regulation through promoterproximal pausing of RNA polymerase II. Science 319: 1791-1792
8. Darnell Jr JE, Kerr IM, Stark GR (1994) Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264: 1415-1421
9. Daury L, Chailleux C, Bonvallet J, Trouche D (2006) Histone H3.3 deposition at E2F-regulated genes is linked to transcription. EMBO Rep 7: 66-71
10. Devaiah BN, Lewis BA, Cherman N, Hewitt MC, Albrecht BK, Robey PG, Ozato K, Sims 3rd RJ, Singer DS (2012) BRD4 is an atypical kinase that phosphorylates serine2 of the RNA polymerase II carboxy-terminal domain. Proc Natl Acad Sci USA 109: 6927-6932
11. Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K (2003) The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci USA 100: 8758-8763
12. Dey A, Nishiyama A, Karpova T, McNally J, Ozato K (2009) Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription. Mol Biol Cell 20: 4899-4909
13. Drane P, Ouararhni K, Depaux A, Shuaib M, Hamiche A (2010) The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. Genes Dev 24: 1253-1265
14. Du HN, Briggs SD (2010) A nucleosome surface formed by histone H4, H2A, and H3 residues is needed for proper histone H3 Lys36 methylation, histone acetylation, and repression of cryptic transcription. J Biol Chem 285: 11704-11713
15. Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27: 406-420
16. Elsaesser SJ, Goldberg AD, Allis CD (2010) New functions for an old variant: no substitute for histone H3.3. Curr Opin Genet Dev 20: 110-117
17. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, Morse EM, Keates T, Hickman TT, Felletar I, Philpott M, Munro S, McKeown MR, Wang Y, Christie AL, West N, Cameron MJ, Schwartz B, Heightman TD, La Thangue N et al (2010) Selective inhibition of BET bromodomains. Nature 468: 1067-1073
18. Goldberg AD, Banaszynski LA, Noh KM, Lewis PW, Elsaesser SJ, Stadler S, Dewell S, Law M, Guo X, Li X, Wen D, Chapgier A, DeKelver RC, Miller JC, Lee YL, Boydston EA, Holmes MC, Gregory PD, Greally JM, Rafii S et al (2010) Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140: 678-691
19. Hake SB, Allis CD (2006) Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis". Proc Natl Acad Sci USA 103: 6428-6435
20. Hake SB, Garcia BA, Duncan EM, Kauer M, Dellaire G, Shabanowitz J, Bazett-Jones DP, Allis CD, Hunt DF (2006) Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem 281: 559-568
21. Harada A, Okada S, Konno D, Odawara J, Yoshimi T, Yoshimura S, Kumamaru H, Saiwai H, Tsubota T, Kurumizaka H, Akashi K, Tachibana T, Imbalzano AN, Ohkawa Y (2012) Chd2 interacts with H3.3 to determine myogenic cell fate. EMBO J 31: 2994-3007
22. Hargreaves DC, Horng T, Medzhitov R (2009) Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138: 129-145
23. He C, Li F, Zhang J, Wu J, Shi Y (2013) The methyltransferase NSD3 has chromatin-binding motifs, PHD5-C5HCH, that are distinct from other NSD (Nuclear Receptor SET Domain) family members in their histone H3 recognition. J Biol Chem 288: 4692-4703
24. Henikoff S (2008) Nucleosome destabilization in the epigenetic regulation of gene expression. Nat Rev Genet 9: 15-26
25. Jang MK, Mochizuki K, Zhou M, Jeong HS, Brady JN, Ozato K (2005) The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell 19: 523-534
26. Janicki SM, Tsukamoto T, Salghetti SE, Tansey WP, Sachidanandam R, Prasanth KV, Ried T, Shav-Tal Y, Bertrand E, Singer RH, Spector DL (2004) From silencing to gene expression: real-time analysis in single cells. Cell 116: 683-698
27. Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome- free regions' of active promoters and other regulatory regions. Nat Genet 41: 941-945
28. Joshi AA, Struhl K (2005) Eaf3 chromodomain interaction with methylated H3-K36 links histone deacetylation to Pol II elongation. Mol Cell 20: 971-978
29. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, Collins SR, Schuldiner M, Chin K, Punna T, Thompson NJ, Boone C, Emili A, Weissman JS, Hughes TR, Strahl BD, Grunstein M, Greenblatt JF, Buratowski S, Krogan NJ (2005) Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605
30. Kim JY, Kee HJ, ChoeNW, KimSM, EomGH, Baek HJ, KookH, Seo SB (2008) Multiple-myeloma-related WHSC1/MMSET isoform RE-IIBP is a histone methyltransferase with transcriptional repression activity. Mol Cell Biol 28: 2023-2034
31. Kulaeva OI, Hsieh FK, Studitsky VM (2010) RNA polymerase complexes cooperate to relieve the nucleosomal barrier and evict histones. Proc Natl Acad Sci USA 107: 11325-11330
32. Kuo AJ, Cheung P, Chen K, Zee BM, Kioi M, Lauring J, Xi Y, Park BH, Shi X, Garcia BA, Li W, Gozani O (2011) NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming. Mol Cell 44: 609-620
33. Lachner M, Jenuwein T (2002) The many faces of histone lysine methylation. Curr Opin Cell Biol 14: 286-298
34. Lewis PW, Elsaesser SJ, Noh KM, Stadler SC, Allis CD (2010) Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication- independent chromatin assembly at telomeres. Proc Natl Acad Sci USA 107: 14075-14080
35. Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128: 707-719
36. Li B, Howe L, Anderson S, Yates 3rd JR, Workman JL (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J Biol Chem 278: 8897-8903
37. Li J, Moazed D, Gygi SP (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J Biol Chem 277: 49383-49388
38. Loyola A, Bonaldi T, Roche D, Imhof A, Almouzni G (2006) PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell 24: 309-316
39. Mapendano CK, Lykke-Andersen S, Kjems J, Bertrand E, Jensen TH (2010) Crosstalk between mRNA 3' end processing and transcription initiation. Mol Cell 40: 410-422
40. Marango J, Shimoyama M, Nishio H, Meyer JA, Min DJ, Sirulnik A, Martinez-Martinez Y, Chesi M, Bergsagel PL, Zhou MM, Waxman S, Leibovitch BA, Walsh MJ, Licht JD (2008) The MMSET protein is a histone methyltransferase with characteristics of a transcriptional corepressor. Blood 111: 3145-3154
41. Mito Y, Henikoff JG, Henikoff S (2005) Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37: 1090-1097
42. Mochizuki K, Nishiyama A, Jang MK, Dey A, Ghosh A, Tamura T, Natsume H, Yao H, Ozato K (2008) The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase. J Biol Chem 283: 9040-9048
43. Nechaev S, Adelman K (2011) Pol II waiting in the starting gates: regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809: 34-45
44. Ng RK, Gurdon JB (2008) Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nat Cell Biol 10: 102-109
45. Nicodeme E, Jeffrey KL, Schaefer U, Beinke S, Dewell S, Chung CW, Chandwani R, Marazzi I, Wilson P, Coste H, White J, Kirilovsky J, Rice CM, Lora JM, Prinjha RK, Lee K, Tarakhovsky A (2010) Suppression of inflammation by a synthetic histone mimic. Nature 468: 1119-1123
46. Nimura K, Ura K, Shiratori H, Ikawa M, Okabe M, Schwartz RJ, Kaneda Y (2009) A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome. Nature 460: 287-291
47. Patel MC, Debrosse M, Smith M, Dey A, Huynh W, Sarai N, Heightman TD, Tamura T, Ozato K (2013) BRD4 coordinates recruitment of pause release factor P-TEFb and the pausing complex NELF/DSIF to regulate transcription elongation of interferon- stimulated genes. Mol Cell Biol 33: 2497-2507
48. Pei H, Zhang L, Luo K, Qin Y, Chesi M, Fei F, Bergsagel PL, Wang L, You Z, Lou Z (2011) MMSETregulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470: 124-128
49. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA (2010) c-Myc regulates transcriptional pause release. Cell 141: 432-445
50. Rahman S, Sowa ME, Ottinger M, Smith JA, Shi Y, Harper JW, Howley PM (2011) The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3. Mol Cell Biol 31: 2641-2652
51. Ray-Gallet D, Woolfe A, Vassias I, Pellentz C, Lacoste N, Puri A, Schultz DC, Pchelintsev NA, Adams PD, Jansen LE, Almouzni G (2011) Dynamics of histone h3 deposition in vivo reveal a nucleosome gap-filling mechanism for h3.3 to maintain chromatin integrity. Mol Cell 44: 928-941
52. Roeder RG (2005) Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett 579: 909-915
53. Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S, Suzuki E, Tanabe M, Zhao Y, Kimura S, Fujiyama S, Ueda T, Umetsu D, Ito T, Takeyama K, Kato S (2010) A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Genes Dev 24: 159-170
54. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19: 804-814
55. Schwartzentruber J, Korshunov A, Liu XY, Jones DT, Pfaff E, Jacob K, Sturm D, Fontebasso AM, Quang DA, Tonjes M, Hovestadt V, Albrecht S, Kool M, Nantel A, Konermann C, Lindroth A, Jager N, Rausch T, Ryzhova M, Korbel JO et al (2012) Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482: 226-231
56. Stec I, Wright TJ, van Ommen GJ, de Boer PA, van Haeringen A, Moorman AF, Altherr MR, den Dunnen JT (1998) WHSC1, a 90 kb SET domain-containing gene, expressed in early development and homologous to a Drosophila dysmorphy gene maps in the Wolf-Hirschhorn syndrome critical region and is fused to IgH in t(4;14) multiple myeloma. Hum Mol Genet 7: 1071-1082
57. Strahl BD, Grant PA, Briggs SD, Sun ZW, Bone JR, Caldwell JA, Mollah S, Cook RG, Shabanowitz J, Hunt DF, Allis CD (2002) Set2 is a nucleosomal histone H3-selective methyltransferase that mediates transcriptional repression. Mol Cell Biol 22: 1298-1306
58. Suganuma T, Workman JL (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499
59. Sutcliffe EL, Parish IA, He YQ, Juelich T, Tierney ML, Rangasamy D, Milburn PJ, Parish CR, Tremethick DJ, Rao S (2009) Dynamic histone variant exchange accompanies gene induction in T cells. Mol Cell Biol 29: 1972-1986
60. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61
61. Talbert PB, Henikoff S (2010) Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275
62. Tamura T, Smith M, Kanno T, Dasenbrock H, Nishiyama A, Ozato K (2009) Inducible deposition of the histone variant H3.3 in interferon- stimulated genes. J Biol Chem 284: 12217-12225
63. Tanaka Y, Katagiri Z, Kawahashi K, Kioussis D, Kitajima S (2007) Trithorax-group protein ASH1 methylates histone H3 lysine 36. Gene 397: 161-168
64. Taverna SD, Ilin S, Rogers RS, Tanny JC, Lavender H, Li H, Baker L, Boyle J, Blair LP, Chait BT, Patel DJ, Aitchison JD, Tackett AJ, Allis CD (2006) Yng1 PHD finger binding to H3 trimethylated at K4 promotes NuA3 HATactivity at K14 of H3 and transcription at a subset of targeted ORFs. Mol Cell 24: 785-796
65. Venkatesh S, Smolle M, Li H, Gogol MM, Saint M, Kumar S, Natarajan K, Workman JL (2012) Set2 methylation of histone H3 lysine 36 suppresses histone exchange on transcribed genes. Nature 489: 452-455
66. Vezzoli A, Bonadies N, Allen MD, Freund SM, Santiveri CM, Kvinlaug BT, Huntly BJ, Gottgens B, Bycroft M (2010) Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat Struct Mol Biol 17: 617-619
67. Wagner EJ, Carpenter PB (2012) Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13: 115-126
68. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903
69. Wirbelauer C, Bell O, Schubeler D (2005) Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter- proximal bias. Genes Dev 19: 1761-1766
70. Wu G, Broniscer A, McEachron TA, Lu C, Paugh BS, Becksfort J, Qu C, Ding L, Huether R, Parker M, Zhang J, Gajjar A, Dyer MA, Mullighan CG, Gilbertson RJ, Mardis ER, Wilson RK, Downing JR, Ellison DW, Baker SJ (2012) Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet 44: 251-253
71. Yang Z, Yik JH, Chen R, He N, Jang MK, Ozato K, Zhou Q (2005) Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 19: 535-545
72. Yudkovsky N, Ranish JA, Hahn S (2000) A transcription reinitiation intermediate that is stabilized by activator. Nature 408: 225-229