Cotranscriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate

Genome Research

Volumn 24, Issue 10, 2014, Pages 1572-1583

  Fuchs, Gilad ^a   Hollander, Dror ^b   Voichek, Yoav ^a   Ast, Gil ^b   Oren, Moshe ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2B; LYSINE; MESSENGER RNA PRECURSOR; POLYPYRIMIDINE TRACT BINDING PROTEIN; RNA POLYMERASE II; SPACER DNA; HISTONE; MESSENGER RNA;

ARTICLE; CONTROLLED STUDY; EARLY RESPONSE GENE; EMBRYO; EMBRYONAL CARCINOMA STEM CELL; EXON; GENE EXPRESSION; HCT116 CELL LINE; HELA CELL LINE; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INTRON; MONOUBIQUITYLATION; NONHUMAN; PROMOTER REGION; STOP CODON; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; UBIQUITINATION; DNA SEQUENCE; GENETICS; METABOLISM; MOLECULAR GENETICS; TUMOR CELL LINE;

CELL LINE, TUMOR; EXONS; HELA CELLS; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; RNA POLYMERASE II; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION ELONGATION, GENETIC; UBIQUITINATION;

EID: 84907541195     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.176487.114     Document Type: Article

References (95)

1. Amit I, Citri A, Shay T, Lu Y, Katz M, Zhang F, Tarcic G, Siwak D, Lahad J, Jacob-Hirsch J, et al. 2007. A module of negative feedback regulators defines growth factor signaling. Nat Genet 39: 503-512.
2. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
3. Batta K, Zhang Z, Yen K, Goffman DB, Pugh BF. 2011. Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev 25: 2254-2265.
4. Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412.
5. Blahnik KR, Dou L, Echipare L, Iyengar S, O'Geen H, Sanchez E, Zhao Y, Marra MA, Hirst M, Costello JF, et al. 2011. Characterization of the contradictory chromatin signatures at the 39 exons of zinc finger genes. PLoS ONE 6: e17121.
6. Blank M, Tang Y, Yamashita M, Burkett SS, Cheng SY, Zhang YE. 2012. A tumor suppressor function of Smurf2 associated with controlling chromatin landscape and genome stability through RNF20. NatMed 18: 227-234.
7. Braunschweig U, Gueroussov S, Plocik AM, Graveley BR, Blencowe BJ. 2013. Dynamic integration of splicing within gene regulatory pathways. Cell 152: 1252-1269.
8. Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, Hunt DF, Allis CD, Strahl BD. 2002. Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418: 498.
9. Buszczak M, Paterno S, Spradling AC. 2009. Drosophila stem cells share a common requirement for the histone H2B ubiquitin protease scrawny. Science 323: 248-251.
10. Campos EI, Reinberg D. 2009. Histones: annotating chromatin. Annu Rev Genet 43: 559-599.
11. Chandrasekharan MB, Huang F, Sun ZW. 2009. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci 106: 16686-16691.
12. Chernikova SB, Dorth JA, Razorenova OV, Game JC, Brown JM. 2010. Deficiency in Bre1 impairs homologous recombination repair and cell cycle checkpoint response to radiation damage in mammalian cells. Radiat Res 174: 558-565.
13. Davie JR, Murphy LC. 1990. Level of ubiquitinated histone H2B in chromatin is coupled to ongoing transcription. Biochemistry 29: 4752-4757.
14. de Almeida SF, Grosso AR, Koch F, Fenouil R, Carvalho S, Andrade J, Levezinho H, Gut M, Eick D, Gut I, et al. 2011. Splicing enhances recruitment of methyltransferase HYPB/Setd2 and methylation of histone H3 Lys36. Nat Struct Mol Biol 18: 977-983.
15. de la Mata M, Alonso CR, Kadener S, Fededa JP, Blaustein M, Pelisch F, Cramer P, Bentley D, Kornblihtt AR. 2003. A slow RNA polymerase II affects alternative splicing in vivo. Mol Cell 12: 525-532.
16. 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.
17. The ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
18. Fierz B, Chatterjee C, McGinty RK, Bar-Dagan M, Raleigh DP, Muir TW. 2011. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 7: 113-119.
19. Fleming AB, Kao CF, Hillyer C, Pikaart M, Osley MA. 2008. H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31: 57-66.
20. Fonseca GJ, Thillainadesan G, Yousef AF, Ablack JN, Mossman KL, Torchia J, Mymryk JS. 2012. Adenovirus evasion of interferon-mediated innate immunity by direct antagonism of a cellular histone posttranslational modification. Cell Host Microbe 11: 597-606.
21. Fuchs G, Oren M. 2014. Writing and reading H2B monoubiquitylation. Biochim Biophys Acta 1839: 694-701.
22. Fuchs G, Shema E, Vesterman R, Kotler E, Wolchinsky Z, Wilder S, Golomb L, Pribluda A, Zhang F, Haj-Yahya M, et al. 2012. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol Cell 46: 662-673.
23. Fuchs G, Voichek Y, Benjamin S, Gilad S, Amit I, Oren M. 2014. 4sUDRB-seq: measuring genomewide transcriptional elongation rates and initiation frequencies within cells. Genome Biol 15: R69.
24. Gelfman S, Burstein D, Penn O, Savchenko A, Amit M, Schwartz S, Pupko T, Ast G. 2012. Changes in exon-intron structure during vertebrate evolution affect the splicing pattern of exons. Genome Res 22: 35-50.
25. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, HuarteM, Zuk O, Carey BW, Cassady JP, et al. 2009. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458: 223-227.
26. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576-589.
27. Henry KW, Wyce A, LoWS, Duggan LJ, Emre NC, Kao CF, Pillus L, Shilatifard A, Osley MA, Berger SL. 2003. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGAassociated Ubp8. Genes Dev 17: 2648-2663.
28. Herissant L, Moehle EA, Bertaccini D, Van Dorsselaer A, Schaeffer-Reiss C, Guthrie C, Dargemont C. 2014. H2B ubiquitylation modulates spliceosome assembly and function in budding yeast. Biol Cell 106: 126-138.
29. Huff JT, Plocik AM, Guthrie C, Yamamoto KR. 2010. Reciprocal intronic and exonic histone modification regions in humans. Nat Struct Mol Biol 17: 1495-1499.
30. Hwang WW, Madhani HD. 2009. Nonredundant requirement for multiple histone modifications for the early anaphase release of the mitotic exit regulator Cdc14 from nucleolar chromatin. PLoS Genet 5: e1000588.
31. Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, Tong A, Boone C, Madhani HD. 2003. A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 11: 261-266.
32. Ip JY, Schmidt D, Pan Q, Ramani AK, Fraser AG, Odom DT, Blencowe BJ. 2011. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res 21: 390-401.
33. Johnsen SA. 2012. The enigmatic role of H2Bub1 in cancer. FEBS Lett 586: 1592-1601.
34. Jonkers I, Kwak H, Lis JT. 2014. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 3: e02407.
35. Jung I, Kim SK, Kim M, Han YM, Kim YS, Kim D, Lee D. 2012. H2B monoubiquitylation is a 59-enriched active transcription mark and correlates with exon-intron structure in human cells. Genome Res 22: 1026-1035.
36. Kari V, Shchebet A, Neumann H, Johnsen SA. 2011. The H2B ubiquitin ligase RNF40 cooperates with SUPT16H to induce dynamic changes in chromatin structure during DNA double-strand break repair. Cell Cycle 10: 3495-3504.
37. Karpiuk O, Najafova Z, Kramer F, Hennion M, Galonska C, Konig A, Snaidero N, Vogel T, Shchebet A, Begus-Nahrmann Y, et al. 2012. The histone H2B monoubiquitination regulatory pathway is required for differentiation of multipotent stem cells. Mol Cell 46: 705-713.
38. Ke S, Shang S, Kalachikov SM, Morozova I, Yu L, Russo JJ, Ju J, Chasin LA. 2011. Quantitative evaluation of all hexamers as exonic splicing elements. Genome Res 21: 1360-1374.
39. Kim J, Hake SB, Roeder RG. 2005. The human homolog of yeast BRE1 functions as a transcriptional coactivator through direct activator interactions. Mol Cell 20: 759-770.
40. Kim J, Guermah M, McGinty RK, Lee JS, Tang Z, Milne TA, Shilatifard A, Muir TW, Roeder RG. 2009. RAD6-mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 137: 459-471.
41. Kim S, Kim H, Fong N, Erickson B, Bentley DL. 2011. Pre-mRNA splicing is a determinant of histone H3K36 methylation. Proc Natl Acad Sci 108: 13564-13569.
42. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J. 2009. Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41: 376-381.
43. Kornblihtt AR, Schor IE, Allo M, Dujardin G, Petrillo E, Munoz MJ. 2013. Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 14: 153-165.
44. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
45. Kwak H, Fuda NJ, Core LJ, Lis JT. 2013. Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 339: 950-953.
46. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
47. Le Martelot G, Canella D, Symul L, Migliavacca E,Gilardi F, Liechti R, Martin O, Harshman K, Delorenzi M, Desvergne B, et al. 2012. Genome-wide RNA polymerase II profiles and RNA accumulation reveal kinetics of transcription and associated epigenetic changes during diurnal cycles. PLoS Biol 10: e1001442.
48. Lee JS, Shukla A, Schneider J, Swanson SK, Washburn MP, Florens L, Bhaumik SR, Shilatifard A. 2007. Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131: 1084-1096.
49. Llorian M, Schwartz S, Clark TA, Hollander D, Tan LY, Spellman R, Gordon A, Schweitzer AC, de la Grange P, Ast G, et al. 2010. Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat Struct Mol Biol 17: 1114-1123.
50. Long L, Thelen JP, Furgason M, Haj-YahyaM, Brik A, Cheng D, Peng J, Yao T. 2014. The U4/U6 recycling factor SART3 has histone chaperone activity and associates with USP15 to regulate H2B deubiquitination. J Biol Chem 289: 8916-8930.
51. Luco RF, Pan Q, Tominaga K, Blencowe BJ, Pereira-Smith OM, Misteli T. 2010. Regulation of alternative splicing by histone modifications. Science 327: 996-1000.
52. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T. 2011. Epigenetics in alternative pre-mRNA splicing. Cell 144: 16-26.
53. Maunakea AK, Chepelev I, Cui K, Zhao K. 2013. Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition. Cell Res 23: 1256-1269.
54. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. 2006. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10: 105-116.
55. Minsky N, Shema E, Field Y, Schuster M, Segal E, Oren M. 2008. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol 10: 483-488.
56. Miyazaki H, Higashimoto K, Yada Y, Endo TA, Sharif J, Komori T, Matsuda M, Koseki Y, Nakayama M, Soejima H, et al. 2013. Ash1l methylates lys36 of histone h3 independently of transcriptional elongation to counteract polycomb silencing. PLoS Genet 9: e1003897.
57. Moehle EA, Ryan CJ, Krogan NJ, Kress TL, Guthrie C. 2012. The yeast SR-like protein Npl3 links chromatin modification to mRNA processing. PLoS Genet 8: e1003101.
58. Moyal L, Lerenthal Y, Gana-Weisz M, Mass G, So S, Wang SY, Eppink B, Chung YM, Shalev G, Shema E, et al. 2011. Requirement of ATMdependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol Cell 41: 529-542.
59. Nakamura K, Kato A, Kobayashi J, Yanagihara H, Sakamoto S, Oliveira DV, Shimada M, Tauchi H, Suzuki H, Tashiro S, et al. 2011. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol Cell 41: 515-528.
60. Ng HH, Xu RM, Zhang Y, Struhl K. 2002. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem 277: 34655-34657.
61. Patel DJ, Wang Z. 2013. Readout of epigenetic modifications. Annu Rev Biochem 82: 81-118.
62. Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A, Reinberg D. 2006. Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703-717.
63. Pirngruber J, Shchebet A, Schreiber L, Shema E, Minsky N, Chapman RD, Eick D, Aylon Y, Oren M, Johnsen SA. 2009. CDK9 directs H2B monoubiquitination and controls replication-dependent histone mRNA 39-end processing. EMBO Rep 10: 894-900.
64. R Development Core Team. 2014 R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
65. Rhead B, Karolchik D, Kuhn RM, Hinrichs AS, Zweig AS, Fujita PA, Diekhans M, Smith KE, RosenbloomKR, Raney BJ, et al. 2010. The UCSC Genome Browser database: update 2010. Nucleic Acids Res 38: D613-D619.
66. Sadeghi L, Siggens L, Svensson JP, Ekwall K. 2014. Centromeric histone H2B monoubiquitination promotes noncoding transcription and chromatin integrity. Nat Struct Mol Biol 21: 236-243.
67. Saldanha AJ. 2004. Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
68. Sarkari F, Sanchez-Alcaraz T, Wang S, Holowaty MN, Sheng Y, Frappier L. 2009. EBNA1-mediated recruitment of a histone H2B deubiquitylating complex to the Epstein-Barr virus latent origin of DNA replication. PLoS Pathog 5: e1000624.
69. Schor IE, Rascovan N, Pelisch F, Allo M, Kornblihtt AR. 2009. Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing. Proc Natl Acad Sci 106: 4325-4330.
70. Schor IE, Fiszbein A, Petrillo E, Kornblihtt AR. 2013. Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation. EMBO J 32: 2264-2274.
71. Schwartz S, Meshorer E, Ast G. 2009. Chromatin organization marks exonintron structure. Nat Struct Mol Biol 16: 990-995.
72. Sen R, Bhaumik SR. 2013. Transcriptional stimulatory and repressive functions of histone H2B ubiquitin ligase. Transcription 4: 221-226.
73. Shema E, Tirosh I, Aylon Y, Huang J, Ye C, Moskovits N, Raver-Shapira N, Minsky N, Pirngruber J, Tarcic G, et al. 2008. The histone H2B-specific ubiquitin ligase RNF20/hBRE1 acts as a putative tumor suppressor through selective regulation of gene expression. Genes Dev 22: 2664-2676.
74. Shema-Yaacoby E, Nikolov M, Haj-Yahya M, Siman P, Allemand E, Yamaguchi Y, Muchardt C, Urlaub H, Brik A, Oren M, et al. 2013. Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription. Cell Reports 4: 601-608.
75. Singh J, Padgett RA. 2009. Rates of in situ transcription and splicing in large human genes. Nat Struct Mol Biol 16: 1128-1133.
76. Spies N, Nielsen CB, Padgett RA, Burge CB. 2009. Biased chromatin signatures around polyadenylation sites and exons. Mol Cell 36: 245-254.
77. Sun ZW, Allis CD. 2002. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
78. Tilgner H, Nikolaou C, Althammer S, Sammeth M, Beato M, Valcarcel J, Guigo R. 2009. Nucleosome positioning as a determinant of exon recognition. Nat Struct Mol Biol 16: 996-1001.
79. Trujillo KM, Osley MA. 2012. A role for H2B ubiquitylation in DNA replication. Mol Cell 48: 734-746.
80. Veloso A, Kirkconnell KS, Magnuson B, Biewen B, Paulsen MT, Wilson TE, Ljungman M. 2014. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications. Genome Res 24: 896-905.
81. 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.
82. Vitaliano-Prunier A, Babour A, Herissant L, Apponi L, Margaritis T, Holstege FC, Corbett AH, Gwizdek C, Dargemont C. 2012. H2B ubiquitylation controls the formation of export-competent mRNP. Mol Cell 45: 132-139.
83. Wada Y, Ohta Y, Xu M, Tsutsumi S, Minami T, Inoue K, Komura D, Kitakami J, Oshida N, Papantonis A, et al. 2009. A wave of nascent transcription on activated human genes. Proc Natl Acad Sci 106: 18357-18361.
84. Walter D, Matter A, Fahrenkrog B. 2010. Bre1p-mediated histone H2B ubiquitylation regulates apoptosis in Saccharomyces cerevisiae. J Cell Sci 123: 1931-1939.
85. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, et al. 2008. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40: 897-903.
86. Weake VM, Workman JL. 2008. Histone ubiquitination: triggering gene activity. Mol Cell 29: 653-663.
87. Weinberger L, Voichek Y, Tirosh I, Hornung G, Amit I, Barkai N. 2012. Expression noise and acetylation profiles distinguish HDAC functions. Mol Cell 47: 193-202.
88. Weiner A, Chen HV, Liu CL, Rahat A, Klien A, Soares L, Gudipati M, Pfeffner J, Regev A, Buratowski S, et al. 2012. Systematic dissection of roles for chromatin regulators in a yeast stress response. PLoS Biol 10: e1001369.
89. Wood A, Krogan NJ, Dover J, Schneider J, Heidt J, Boateng MA, Dean K, Golshani A, Zhang Y, Greenblatt JF, et al. 2003. Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell 11: 267-274.
90. Wright DE,Wang CY, Kao CF. 2011. Flickin' the ubiquitin switch: the role of H2B ubiquitylation in development. Epigenetics 6: 1165-1175.
91. Wu L, Zee BM, Wang Y, Garcia BA, Dou Y. 2011. The RING finger protein MSL2 in the MOF complex is an E3 ubiquitin ligase for H2B K34 and is involved in crosstalk with H3 K4 and K79 methylation. Mol Cell 43: 132-144.
92. Yu P, Xiao S, Xin X, Song CX, HuangW, McDee D, Tanaka T,Wang T, He C, Zhong S. 2013. Spatiotemporal clustering of the epigenome reveals rules of dynamic gene regulation. Genome Res 23: 352-364.
93. Zhang Z, Jones A, Joo HY, Zhou D, Cao Y, Chen S, Erdjument-Bromage H, Renfrow M, He H, Tempst P, et al. 2013. USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing. Genes Dev 27: 1581-1595.
94. ZhouVW, Goren A, Bernstein BE. 2011. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12: 7-18.
95. Zhu B, Zheng Y, Pham AD, Mandal SS, Erdjument-Bromage H, Tempst P, Reinberg D. 2005. Monoubiquitination of human histone H2B: the factors involved and their roles in HOX gene regulation. Mol Cell 20: 601-611.