Brd4 and JMJD6-associated anti-pause enhancers in regulation of transcriptional pause release

Cell

Volumn 155, Issue 7, 2013, Pages 1581-1595

  Liu, Wen ^a,b   Ma, Qi ^a,c   Wong, Kaki ^a   Li, Wenbo ^a   Ohgi, Kenny ^a   Zhang, Jie ^a   Aggarwal, Aneel K ^d   Rosenfeld, Michael G ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b XIAMEN UNIVERSITY   (China)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMODOMAIN CONTAINING PROTEIN 4; CYCLIN T1; HISTONE DEMETHYLASE; JUMONJI C DOMAIN CONTAINING PROTEIN 6; METHYLTRANSFERASE; PEPTIDES AND PROTEINS; RNA POLYMERASE II; SMALL INTERFERING RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; BRD4 PROTEIN, HUMAN; JMJD6 PROTEIN, HUMAN; NUCLEAR PROTEIN; TRANSCRIPTION FACTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DEMETHYLATION; DNA FLANKING REGION; ENHANCER REGION; ENZYME ACTIVITY; GENE ACTIVATION; GENETIC CODE; GENETIC TRANSCRIPTION; HELA CELL; HISTONE METHYLATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN HOMEOSTASIS; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; CELL STRAIN HEK293; METABOLISM; HEK293 CELL LINE;

ENHANCER ELEMENTS, GENETIC; HEK293 CELLS; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; RNA, SMALL NUCLEAR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84894579192     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.10.056     Document Type: Article

References (59)

1. K. Adelman, and J.T. Lis Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans Nat. Rev. Genet. 13 2012 720 731
2. P. Anand, J.D. Brown, C.Y. Lin, J. Qi, R. Zhang, P.C. Artero, M.A. Alaiti, J. Bullard, K. Alazem, and K.B. Margulies et al. BET bromodomains mediate transcriptional pause release in heart failure Cell 154 2013 569 582
3. J. Böse, A.D. Gruber, L. Helming, S. Schiebe, I. Wegener, M. Hafner, M. Beales, F. Köntgen, and A. Lengeling The phosphatidylserine receptor has essential functions during embryogenesis but not in apoptotic cell removal J. Biol. 3 2004 15
4. B. Chang, Y. Chen, Y. Zhao, and R.K. Bruick JMJD6 is a histone arginine demethylase Science 318 2007 444 447
5. P. Cui, B. Qin, N. Liu, G. Pan, and D. Pei Nuclear localization of the phosphatidylserine receptor protein via multiple nuclear localization signals Exp. Cell Res. 293 2004 154 163
6. J.E. Delmore, G.C. Issa, M.E. Lemieux, P.B. Rahl, J. Shi, H.M. Jacobs, E. Kastritis, T. Gilpatrick, R.M. Paranal, and J. Qi et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc Cell 146 2011 904 917
7. A. Dey, A. Nishiyama, T. Karpova, J. McNally, and K. Ozato Brd4 marks select genes on mitotic chromatin and directs postmitotic transcription Mol. Biol. Cell 20 2009 4899 4909
8. V.A. Fadok, D.L. Bratton, D.M. Rose, A. Pearson, R.A. Ezekewitz, and P.M. Henson A receptor for phosphatidylserine-specific clearance of apoptotic cells Nature 405 2000 85 90
9. P. Filippakopoulos, J. Qi, S. Picaud, Y. Shen, W.B. Smith, O. Fedorov, E.M. Morse, T. Keates, T.T. Hickman, and I. Felletar et al. Selective inhibition of BET bromodomains Nature 468 2010 1067 1073
10. A. Gyuris, D.J. Donovan, K.A. Seymour, L.A. Lovasco, N.R. Smilowitz, A.L. Halperin, J.E. Klysik, and R.N. Freiman The chromatin-targeting protein Brd2 is required for neural tube closure and embryogenesis Biochim. Biophys. Acta 1789 2009 413 421
11. N. Hah, S. Murakami, A. Nagari, C.G. Danko, and W.L. Kraus Enhancer transcripts mark active estrogen receptor binding sites Genome Res. 23 2013 1210 1223
12. D.C. Hargreaves, T. Horng, and R. Medzhitov Control of inducible gene expression by signal-dependent transcriptional elongation Cell 138 2009 129 145
13. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, and C.W. Ching et al. Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
14. X. Hong, J. Zang, J. White, C. Wang, C.H. Pan, R. Zhao, R.C. Murphy, S. Dai, P. Henson, and J.W. Kappler et al. Interaction of JMJD6 with single-stranded RNA Proc. Natl. Acad. Sci. USA 107 2010 14568 14572
15. D. Houzelstein, S.L. Bullock, D.E. Lynch, E.F. Grigorieva, V.A. Wilson, and R.S. Beddington Growth and early postimplantation defects in mice deficient for the bromodomain-containing protein Brd4 Mol. Cell. Biol. 22 2002 3794 3802
16. M.K. Jang, K. Mochizuki, M. Zhou, H.S. Jeong, J.N. Brady, and K. Ozato The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription Mol. Cell 19 2005 523 534
17. C. Jeronimo, D. Forget, A. Bouchard, Q. Li, G. Chua, C. Poitras, C. Thérien, D. Bergeron, S. Bourassa, and J. Greenblatt et al. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme Mol. Cell 27 2007 262 274
18. M.H. Kagey, J.J. Newman, S. Bilodeau, Y. Zhan, D.A. Orlando, N.L. van Berkum, C.C. Ebmeier, J. Goossens, P.B. Rahl, and S.S. Levine et al. Mediator and cohesin connect gene expression and chromatin architecture Nature 467 2010 430 435
19. J.B. Kim, and P.A. Sharp Positive transcription elongation factor B phosphorylates hSPT5 and RNA polymerase II carboxyl-terminal domain independently of cyclin-dependent kinase-activating kinase J. Biol. Chem. 276 2001 12317 12323
20. B.J. Krueger, K. Varzavand, J.J. Cooper, and D.H. Price The mechanism of release of P-TEFb and HEXIM1 from the 7SK snRNP by viral and cellular activators includes a conformational change in 7SK PLoS ONE 5 2010 e12335
21. Y. Kunisaki, S. Masuko, M. Noda, A. Inayoshi, T. Sanui, M. Harada, T. Sasazuki, and Y. Fukui Defective fetal liver erythropoiesis and T lymphopoiesis in mice lacking the phosphatidylserine receptor Blood 103 2004 3362 3364
22. M. Lachner, R.J. O'Sullivan, and T. Jenuwein An epigenetic road map for histone lysine methylation J. Cell Sci. 116 2003 2117 2124
23. M.T. Lam, H. Cho, H.P. Lesch, D. Gosselin, S. Heinz, Y. Tanaka-Oishi, C. Benner, M.U. Kaikkonen, A.S. Kim, and M. Kosaka et al. Rev-Erbs repress macrophage gene expression by inhibiting enhancer-directed transcription Nature 498 2013 511 515
24. M.O. Li, M.R. Sarkisian, W.Z. Mehal, P. Rakic, and R.A. Flavell Phosphatidylserine receptor is required for clearance of apoptotic cells Science 302 2003 1560 1563
25. X. Li, X. Hu, B. Patel, Z. Zhou, S. Liang, R. Ybarra, Y. Qiu, G. Felsenfeld, J. Bungert, and S. Huang H4R3 methylation facilitates beta-globin transcription by regulating histone acetyltransferase binding and H3 acetylation Blood 115 2010 2028 2037
26. W. Li, D. Notani, Q. Ma, B. Tanasa, E. Nunez, A.Y. Chen, D. Merkurjev, J. Zhang, K. Ohgi, and X. Song et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation Nature 498 2013 516 520
27. J. Lovén, H.A. Hoke, C.Y. Lin, A. Lau, D.A. Orlando, C.R. Vakoc, J.E. Bradner, T.I. Lee, and R.A. Young Selective inhibition of tumor oncogenes by disruption of super-enhancers Cell 153 2013 320 334
28. N.F. Marshall, J. Peng, Z. Xie, and D.H. Price Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase J. Biol. Chem. 271 1996 27176 27183
29. I.M. Min, J.J. Waterfall, L.J. Core, R.J. Munroe, J. Schimenti, and J.T. Lis Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells Genes Dev. 25 2011 742 754
30. K. Mochizuki, A. Nishiyama, M.K. Jang, A. Dey, A. Ghosh, T. Tamura, H. Natsume, H. Yao, and K. Ozato The bromodomain protein Brd4 stimulates G1 gene transcription and promotes progression to S phase J. Biol. Chem. 283 2008 9040 9048
31. G. Natoli, and J.C. Andrau Noncoding transcription at enhancers: general principles and functional models Annu. Rev. Genet. 46 2012 1 19
32. V.T. Nguyen, T. Kiss, A.A. Michels, and O. Bensaude 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes Nature 414 2001 322 325
33. E. Nicodeme, K.L. Jeffrey, U. Schaefer, S. Beinke, S. Dewell, C.W. Chung, R. Chandwani, I. Marazzi, P. Wilson, and H. Coste et al. Suppression of inflammation by a synthetic histone mimic Nature 468 2010 1119 1123
34. P.B. Rahl, C.Y. Lin, A.C. Seila, R.A. Flynn, S. McCuine, C.B. Burge, P.A. Sharp, and R.A. Young c-Myc regulates transcriptional pause release Cell 141 2010 432 445
35. S. Rahman, M.E. Sowa, M. Ottinger, J.A. Smith, Y. Shi, J.W. Harper, and P.M. Howley The Brd4 extraterminal domain confers transcription activation independent of pTEFb by recruiting multiple proteins, including NSD3 Mol. Cell. Biol. 31 2011 2641 2652
36. B. Ren Transcription: Enhancers make non-coding RNA Nature 465 2010 173 174
37. N.B. Reppas, J.T. Wade, G.M. Church, and K. Struhl The transition between transcriptional initiation and elongation in E. coli is highly variable and often rate limiting Mol. Cell 24 2006 747 757
38. A.J. Ruthenburg, H. Li, D.J. Patel, and C.D. Allis Multivalent engagement of chromatin modifications by linked binding modules Nat. Rev. Mol. Cell Biol. 8 2007 983 994
39. G.P. Shumyatsky, S.V. Tillib, and D.A. Kramerov B2 RNA and 7SK RNA, RNA polymerase III transcripts, have a cap-like structure at their 5′ end Nucleic Acids Res. 18 1990 6347 6351
40. N. Tibrewal, T. Liu, H. Li, and R.B. Birge Characterization of the biochemical and biophysical properties of the phosphatidylserine receptor (PS-R) gene product Mol. Cell. Biochem. 304 2007 119 125
41. T. Wada, T. Takagi, Y. Yamaguchi, D. Watanabe, and H. Handa Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro EMBO J. 17 1998 7395 7403
42. C.J. Webby, A. Wolf, N. Gromak, M. Dreger, H. Kramer, B. Kessler, M.L. Nielsen, C. Schmitz, D.S. Butler, and J.R. Yates 3rd et al. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing Science 325 2009 90 93
43. S.Y. Wu, T. Zhou, and C.M. Chiang Human mediator enhances activator-facilitated recruitment of RNA polymerase II and promoter recognition by TATA-binding protein (TBP) independently of TBP-associated factors Mol. Cell. Biol. 23 2003 6229 6242
44. J. Wysocka, C.D. Allis, and S. Coonrod Histone arginine methylation and its dynamic regulation Front. Biosci. 11 2006 344 355
45. X. Xu, S. Hoang, M.W. Mayo, and S. Bekiranov Application of machine learning methods to histone methylation ChIP-Seq data reveals H4R3me2 globally represses gene expression BMC Bioinformatics 11 2010 396
46. T. Yamada, Y. Yamaguchi, N. Inukai, S. Okamoto, T. Mura, and H. Handa P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation Mol. Cell 21 2006 227 237
47. Z. Yang, Q. Zhu, K. Luo, and Q. Zhou The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription Nature 414 2001 317 322
48. Z. Yang, J.H. Yik, R. Chen, N. He, M.K. Jang, K. Ozato, and Q. Zhou Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4 Mol. Cell 19 2005 535 545
49. Z. Yang, N. He, and Q. Zhou Brd4 recruits P-TEFb to chromosomes at late mitosis to promote G1 gene expression and cell cycle progression Mol. Cell. Biol. 28 2008 967 976
50. Y. Yang, Y. Lu, A. Espejo, J. Wu, W. Xu, S. Liang, and M.T. Bedford TDRD3 is an effector molecule for arginine-methylated histone marks Mol. Cell 40 2010 1016 1023
51. L. Yang, C. Lin, W. Liu, J. Zhang, K.A. Ohgi, J.D. Grinstein, P.C. Dorrestein, and M.G. Rosenfeld ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs Cell 147 2011 773 788
52. J. Zeitlinger, A. Stark, M. Kellis, J.W. Hong, S. Nechaev, K. Adelman, M. Levine, and R.A. Young RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo Nat. Genet. 39 2007 1512 1516
53. J. Zuber, J. Shi, E. Wang, A.R. Rappaport, H. Herrmann, E.A. Sison, D. Magoon, J. Qi, K. Blatt, and M. Wunderlich et al. RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia Nature 478 2011 524 528
54. C. Chu, J. Quinn, and H.Y. Chang Chromatin isolation by RNA purification (ChIRP) J. Vis. Exp. 2012 10.3791/3912 Published online March 25, 2012
55. L.J. Core, J.J. Waterfall, and J.T. Lis Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters Science 322 2008 1845 1848
56. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
57. W. Liu, B. Tanasa, O.V. Tyurina, T.Y. Zhou, R. Gassmann, W.T. Liu, K.A. Ohgi, C. Benner, I. Garcia-Bassets, and A.K. Aggarwal et al. PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression Nature 466 2010 508 512
58. M.C. Tsai, O. Manor, Y. Wan, N. Mosammaparast, J.K. Wang, F. Lan, Y. Shi, E. Segal, and H.Y. Chang Long noncoding RNA as modular scaffold of histone modification complexes Science 329 2010 689 693
59. D. Wang, I. Garcia-Bassets, C. Benner, W. Li, X. Su, Y. Zhou, J. Qiu, W. Liu, M.U. Kaikkonen, and K.A. Ohgi et al. Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA Nature 474 2011 390 394