The Mediator subunit MED23 couples H2B mono-ubiquitination to transcriptional control and cell fate determination

EMBO Journal

Volumn 34, Issue 23, 2015, Pages 2885-2902

  Yao, Xiao ^a   Tang, Zhanyun ^b   Fu, Xing ^c   Yin, Jingwen ^a   Liang, Yan ^a   Li, Chonghui ^a   Li, Huayun ^a   Tian, Qing ^a   Roeder, Robert G ^b   Wang, Gang ^a  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b ROCKEFELLER UNIVERSITY   (United States)

^c Chinese Academy of Sciences   (China)

Author keywords

H2B mono ubiquitination; Mediator MED23; myogenesis; RNF20 and RNF40; tumorigenesis

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; HISTONE H2B; MED23 PROTEIN; MEDIATOR COMPLEX; PROTEIN; RNF20 40 PROTEIN; UNCLASSIFIED DRUG; HISTONE; MED23 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; CARCINOGENESIS; CELL FATE; CELL FREE SYSTEM; CHROMATIN; COMPARATIVE STUDY; CONTROLLED STUDY; EPIGENETICS; FEMALE; GEL FILTRATION; GENE LOCUS; HELA CELL LINE; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG ADENOCARCINOMA; LUNG CARCINOGENESIS; MASS SPECTROMETRY; MICROARRAY ANALYSIS; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEFICIENCY; PROTEIN DEPLETION; PROTEIN PURIFICATION; SKELETAL MUSCLE; TANDEM MASS SPECTROMETRY; TRANSCRIPTION INITIATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; PHYSIOLOGY; UBIQUITINATION;

ANIMALS; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HISTONES; MEDIATOR COMPLEX; MICE; MODELS, BIOLOGICAL; MUSCLE DEVELOPMENT; UBIQUITINATION;

EID: 84956581461     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591279     Document Type: Article

References (64)

1. Balamotis MA, Pennella MA, Stevens JL, Wasylyk B, Belmont AS, Berk AJ, (2009) Complexity in transcription control at the activation domain-mediator interface. Sci Signal 2: ra20
2. Berger SL, (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12: 142-148
3. Dhawan R, Luo H, Foerster AM, Abuqamar S, Du HN, Briggs SD, Mittelsten Scheid O, Mengiste T, (2009) HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. Plant Cell 21: 1000-1019
4. Ding N, Zhou H, Esteve PO, Chin HG, Kim S, Xu X, Joseph SM, Friez MJ, Schwartz CE, Pradhan S, Boyer TG, (2008) Mediator links epigenetic silencing of neuronal gene expression with x-linked mental retardation. Mol Cell 31: 347-359
5. Donner AJ, Ebmeier CC, Taatjes DJ, Espinosa JM, (2010) CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17: 194-201
6. Dover J, Schneider J, Tawiah-Boateng MA, Wood A, Dean K, Johnston M, Shilatifard A, (2002) Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 277: 28368-28371
7. 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
8. 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
9. Fukasawa R, Tsutsui T, Hirose Y, Tanaka A, Ohkuma Y, (2012) Mediator CDK subunits are platforms for interactions with various chromatin regulatory complexes. J Biochem 152: 241-249
10. Galbraith M, Allen M, Bensard C, Wang X, Schwinn M, Qin B, Long H, Daniels D, Hahn W, Dowell R, Espinosa J, (2013) HIF1A employs CDK8-mediator to stimulate RNAPII elongation in response to hypoxia. Cell 153: 1327-1339
11. Hahn MA, Dickson KA, Jackson S, Clarkson A, Gill AJ, Marsh DJ, (2012) The tumor suppressor CDC73 interacts with the ring finger proteins RNF20 and RNF40 and is required for the maintenance of histone 2B monoubiquitination. Hum Mol Genet 21: 559-568
12. Huang Y, Li W, Yao X, Lin QJ, Yin JW, Liang Y, Heiner M, Tian B, Hui J, Wang G, (2012) Mediator complex regulates alternative mRNA processing via the MED23 subunit. Mol Cell 45: 459-469
13. 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
14. Jaaskelainen T, Makkonen H, Visakorpi T, Kim J, Roeder RG, Palvimo JJ, (2012) Histone H2B ubiquitin ligases RNF20 and RNF40 in androgen signaling and prostate cancer cell growth. Mol Cell Endocrinol 350: 87-98
15. Jenuwein T, Allis CD, (2001) Translating the histone code. Science 293: 1074-1080
16. Jung I, Kim S-K, Kim M, Han Y-M, Kim Y, Kim D, Lee D, (2012) H2B monoubiquitylation is a 5′-enriched active transcription mark and correlates with exon-intron structure in human cells. Genome Res 22: 1026-1035
17. Kagey MH, Newman JJ, Bilodeau S, Zhan Y, Orlando DA, van Berkum NL, Ebmeier CC, Goossens J, Rahl PB, Levine SS, Taatjes DJ, Dekker J, Young RA, (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435
18. 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
19. 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
20. Kim J, Kim JA, McGinty RK, Nguyen UT, Muir TW, Allis CD, Roeder RG, (2013) The n-SET domain of Set1 regulates H2B ubiquitylation-dependent H3K4 methylation. Mol Cell 49: 1121-1133
21. Koutelou E, Hirsch CL, Dent SY, (2010) Multiple faces of the SAGA complex. Curr Opin Cell Biol 22: 374-382
22. Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA, Shiekhattar R, (2013) Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 494: 497-501
23. Langmead B, Salzberg S, (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359
24. Lee JS, Garrett AS, Yen K, Takahashi YH, Hu D, Jackson J, Seidel C, Pugh BF, Shilatifard A, (2012) Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev 26: 914-919
25. Lee TI, Young RA, (2013) Transcriptional regulation and its misregulation in disease. Cell 152: 1237-1251
26. Li B, Carey M, Workman JL, (2007) The role of chromatin during transcription. Cell 128: 707-719
27. Lovén J, Hoke H, Lin C, Lau A, Orlando D, Vakoc C, Bradner J, Lee T, Young R, (2013) Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153: 320-334
28. Malik S, Roeder RG, (2003) Isolation and functional characterization of the TRAP/mediator complex. Methods Enzymol 364: 257-284
29. Malik S, Roeder RG, (2010) The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11: 761-772
30. Mukundan B, Ansari A, (2011) Novel role for mediator complex subunit Srb5/Med18 in termination of transcription. J Biol Chem 286: 37053-37057
31. 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
32. Prenzel T, Begus-Nahrmann Y, Kramer F, Hennion M, Hsu C, Gorsler T, Hintermair C, Eick D, Kremmer E, Simons M, Beissbarth T, Johnsen SA, (2011) Estrogen-dependent gene transcription in human breast cancer cells relies upon proteasome-dependent monoubiquitination of histone H2B. Cancer Res 71: 5739-5753
33. Samara NL, Wolberger C, (2011) A new chapter in the transcription SAGA. Curr Opin Struct Biol 21: 767-774
34. Shema E, Tirosh I, Aylon Y, Huang J, Ye C, Moskovits N, Raver-Shapira N, Minsky N, Pirngruber J, Tarcic G, Hublarova P, Moyal L, Gana-Weisz M, Shiloh Y, Yarden Y, Johnsen SA, Vojtesek B, Berger SL, Oren M, (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
35. Shema E, Kim J, Roeder RG, Oren M, (2011) RNF20 inhibits TFIIS-facilitated transcriptional elongation to suppress pro-oncogenic gene expression. Mol Cell 42: 477-488
36. Shi J, Liu H, Yao F, Zhong C, Zhao H, (2014) Upregulation of mediator MED23 in non-small-cell lung cancer promotes the growth, migration, and metastasis of cancer cells. Tumour Biol 35: 12005-12013
37. Shilatifard A, (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75: 243-269
38. Strahl BD, Allis CD, (2000) The language of covalent histone modifications. Nature 403: 41-45
39. Suganuma T, Workman JL, (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499
40. Taatjes DJ, (2010) The human Mediator complex: a versatile, genome-wide regulator of transcription. Trends Biochem Sci 35: 315-322
41. Takahashi H, Parmely T, Sato S, Tomomori-Sato C, Banks C, Kong S, Szutorisz H, Swanson S, Martin-Brown S, Washburn M, Florens L, Seidel C, Lin C, Smith E, Shilatifard A, Conaway R, Conaway J, (2011) Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 146: 92-104
42. Tang Z, Chen WY, Shimada M, Nguyen UT, Kim J, Sun XJ, Sengoku T, McGinty RK, Fernandez JP, Muir TW, Roeder RG, (2013) SET1 and p300 act synergistically, through coupled histone modifications, in transcriptional activation by p53. Cell 154: 297-310
43. Tanny JC, Erdjument-Bromage H, Tempst P, Allis CD, (2007) Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev 21: 835-847
44. Turner BM, (2002) Cellular memory and the histone code. Cell 111: 285-291
45. Urasaki Y, Heath L, Xu CW, (2012) Coupling of glucose deprivation with impaired histone H2B monoubiquitination in tumors. PLoS ONE 7: e36775
46. Wang G, Cantin GT, Stevens JL, Berk AJ, (2001) Characterization of mediator complexes from HeLa cell nuclear extract. Mol Cell Biol 21: 4604-4613
47. Wang G, Balamotis MA, Stevens JL, Yamaguchi Y, Handa H, Berk AJ, (2005) Mediator requirement for both recruitment and postrecruitment steps in transcription initiation. Mol Cell 17: 683-694
48. Wang W, Huang L, Huang Y, Yin JW, Berk AJ, Friedman JM, Wang G, (2009) Mediator MED23 links insulin signaling to the adipogenesis transcription cascade. Dev Cell 16: 764-771
49. Wang E, Kawaoka S, Yu M, Shi J, Ni T, Yang W, Zhu J, Roeder RG, Vakoc CR, (2013a) Histone H2B ubiquitin ligase RNF20 is required for MLL-rearranged leukemia. Proc Natl Acad Sci USA 110: 3901-3906
50. Wang W, Yao X, Huang Y, Hu X, Liu R, Hou D, Chen R, Wang G, (2013b) Mediator MED23 regulates basal transcription in vivo via an interaction with P-TEFb. Transcription 4: 39-51
51. Weake VM, Workman JL, (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29: 653-663
52. Weake VM, Workman JL, (2012) SAGA function in tissue-specific gene expression. Trends Cell Biol 22: 177-184
53. Whyte W, Orlando D, Hnisz D, Abraham B, Lin C, Kagey M, Rahl P, Lee T, Young R, (2013) Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153: 307-319
54. Wu L, Lee SY, Zhou B, Nguyen UT, Muir TW, Tan S, Dou Y, (2013) ASH2L regulates ubiquitylation signaling to MLL: trans-regulation of H3 K4 methylation in higher eukaryotes. Mol Cell 49: 1108-1120
55. Wu L, Li L, Zhou B, Qin Z, Dou Y, (2014) H2B ubiquitylation promotes RNA Pol II processivity via PAF1 and pTEFb. Mol Cell 54: 920-931
56. Wyce A, Xiao T, Whelan KA, Kosman C, Walter W, Eick D, Hughes TR, Krogan NJ, Strahl BD, Berger SL, (2007) H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol Cell 27: 275-288
57. Yang X, Zhao M, Xia M, Liu Y, Yan J, Ji H, Wang G, (2012) Selective requirement for Mediator MED23 in Ras-active lung cancer. Proc Natl Acad Sci USA 109: E2813-E2822
58. Yin JW, Liang Y, Park JY, Chen D, Yao X, Xiao Q, Liu Z, Jiang B, Fu Y, Bao M, Huang Y, Liu Y, Yan J, Zhu MS, Yang Z, Gao P, Tian B, Li D, Wang G, (2012) Mediator MED23 plays opposing roles in directing smooth muscle cell and adipocyte differentiation. Genes Dev 26: 2192-2205
59. Yin JW, Wang G, (2014) The Mediator complex: a master coordinator of transcription and cell lineage development. Development 141: 977-987
60. Yuan W, Xie J, Long C, Erdjument-Bromage H, Ding X, Zheng Y, Tempst P, Chen S, Zhu B, Reinberg D, (2009) Heterogeneous nuclear ribonucleoprotein L Is a subunit of human KMT3a/Set2 complex required for H3 Lys-36 trimethylation activity in vivo. J Biol Chem 284: 15701-15707
61. Zhang XY, Varthi M, Sykes SM, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne AW, Berger SL, McMahon SB, (2008a) The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell 29: 102-111
62. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS, (2008b) Model-based analysis of ChIP-Seq (MACS). Genome Biol 9: R137
63. Zhang Z, Jones A, Joo HY, Zhou D, Cao Y, Chen S, Erdjument-Bromage H, Renfrow M, He H, Tempst P, Townes TM, Giles KE, Ma L, Wang H, (2013) USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing. Genes Dev 27: 1581-1595
64. 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