RNA Polymerase II Regulates Topoisomerase 1 Activity to Favor Efficient Transcription

Cell

Volumn 165, Issue 2, 2016, Pages 357-371

  Baranello, Laura ^a   Wojtowicz, Damian ^b   Cui, Kairong ^c   Devaiah, Ballachanda N ^a   Chung, Hye Jung ^a   Chan Salis, Ka Yim ^d   Guha, Rajarshi ^b   Wilson, Kelli ^b   Zhang, Xiaohu ^b   Zhang, Hongliang ^a   Piotrowski, Jason ^a   Thomas, Craig J ^b   Singer, Dinah S ^a   Pugh, B Franklin ^d   Pommier, Yves ^a   Przytycka, Teresa M ^b   Kouzine, Fedor ^a   Lewis, Brian A ^a   Zhao, Keji ^c   Levens, David ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE; RNA POLYMERASE II; DNA; TOP1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; ENZYME ASSAY; ENZYME REGULATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION; TWO DIMENSIONAL GEL ELECTROPHORESIS; CHEMISTRY; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION SITE;

DNA; DNA TOPOISOMERASES, TYPE I; GENE KNOCKDOWN TECHNIQUES; HUMANS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 84964063194     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.02.036     Document Type: Article

References (74)

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. S. Amente, B. Gargano, G. Napolitano, L. Lania, and B. Majello Camptothecin releases P-TEFb from the inactive 7SK snRNP complex Cell Cycle 8 2009 1249 1255
3. L. Baranello, D. Levens, A. Gupta, and F. Kouzine The importance of being supercoiled: how DNA mechanics regulate dynamic processes Biochim. Biophys. Acta 1819 2012 632 638
4. L. Baranello, F. Kouzine, D. Wojtowicz, K. Cui, T.M. Przytycka, K. Zhao, and D. Levens DNA break mapping reveals topoisomerase II activity genome-wide Int. J. Mol. Sci. 15 2014 13111 13122
5. A. Barski, S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao High-resolution profiling of histone methylations in the human genome Cell 129 2007 823 837
6. C. Bowen, A. Stuart, J.H. Ju, J. Tuan, J. Blonder, T.P. Conrads, T.D. Veenstra, and E.P. Gelmann NKX3.1 homeodomain protein binds to topoisomerase I and enhances its activity Cancer Res. 67 2007 455 464
7. S.J. Brill, S. DiNardo, K. Voelkel-Meiman, and R. Sternglanz Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA Nature 326 1987 414 416
8. S.M. Carty, and A.L. Greenleaf Hyperphosphorylated C-terminal repeat domain-associating proteins in the nuclear proteome link transcription to DNA/chromatin modification and RNA processing Mol. Cell. Proteomics 1 2002 598 610
9. J.J. Champoux DNA topoisomerases: structure, function, and mechanism Annu. Rev. Biochem. 70 2001 369 413
10. I. Chepelev, G. Wei, Q. Tang, and K. Zhao Detection of single nucleotide variations in expressed exons of the human genome using RNA-Seq Nucleic Acids Res. 37 2009 e106
11. A.C. Cheung, and P. Cramer A movie of RNA polymerase II transcription Cell 149 2012 1431 1437
12. S. Chong, C. Chen, H. Ge, and X.S. Xie Mechanism of transcriptional bursting in bacteria Cell 158 2014 314 326
13. B.N. Devaiah, B.A. Lewis, N. Cherman, M.C. Hewitt, B.K. Albrecht, P.G. Robey, K. Ozato, R.J. Sims 3rd, and D.S. Singer BRD4 is an atypical kinase that phosphorylates serine2 of the RNA polymerase II carboxy-terminal domain Proc. Natl. Acad. Sci. USA 109 2012 6927 6932
14. M. Dunaway, and E.A. Ostrander Local domains of supercoiling activate a eukaryotic promoter in vivo Nature 361 1993 746 748
15. M. Durand-Dubief, J. Persson, U. Norman, E. Hartsuiker, and K. Ekwall Topoisomerase I regulates open chromatin and controls gene expression in vivo EMBO J. 29 2010 2126 2134
16. W.S. Dynan, J.J. Jendrisak, D.A. Hager, and R.R. Burgess Purification and characterization of wheat germ DNA topoisomerase I (nicking-closing enzyme) J. Biol. Chem. 256 1981 5860 5865
17. S. Egloff, M. Dienstbier, and S. Murphy Updating the RNA polymerase CTD code: adding gene-specific layers Trends Genet. 28 2012 333 341
18. D. Eick, and M. Geyer The RNA polymerase II carboxy-terminal domain (CTD) code Chem. Rev. 113 2013 8456 8490
19. A. Fedier, R.A. Steiner, V.A. Schwarz, L. Lenherr, U. Haller, and D. Fink The effect of loss of Brca1 on the sensitivity to anticancer agents in p53-deficient cells Int. J. Oncol. 22 2003 1169 1173
20. P. Filippakopoulos, J. Qi, S. Picaud, Y. Shen, W.B. Smith, O. Fedorov, E.M. Morse, T. Keates, T.T. Hickman, I. Felletar, and et al. Selective inhibition of BET bromodomains Nature 468 2010 1067 1073
21. M.R. Gartenberg, and J.C. Wang Positive supercoiling of DNA greatly diminishes mRNA synthesis in yeast Proc. Natl. Acad. Sci. USA 89 1992 11461 11465
22. D.A. Gilchrist, G. Dos Santos, D.C. Fargo, B. Xie, Y. Gao, L. Li, and K. Adelman Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation Cell 143 2010 540 551
23. S. Grünberg, L. Warfield, and S. Hahn Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening Nat. Struct. Mol. Biol. 19 2012 788 796
24. 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
25. R.S. Joshi, B. Piña, and J. Roca Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes EMBO J. 29 2010 740 748
26. T. Kanno, Y. Kanno, G. LeRoy, E. Campos, H.W. Sun, S.R. Brooks, G. Vahedi, T.D. Heightman, B.A. Garcia, D. Reinberg, and et al. BRD4 assists elongation of both coding and enhancer RNAs by interacting with acetylated histones Nat. Struct. Mol. Biol. 21 2014 1047 1057
27. A. Khobta, F. Ferri, L. Lotito, A. Montecucco, R. Rossi, and G. Capranico Early effects of topoisomerase I inhibition on RNA polymerase II along transcribed genes in human cells J. Mol. Biol. 357 2006 127 138
28. W.Y. Kim, and M.E. Dahmus Purification of RNA polymerase IIO from calf thymus J. Biol. Chem. 263 1988 18880 18885
29. I.F. King, C.N. Yandava, A.M. Mabb, J.S. Hsiao, H.S. Huang, B.L. Pearson, J.M. Calabrese, J. Starmer, J.S. Parker, T. Magnuson, and et al. Topoisomerases facilitate transcription of long genes linked to autism Nature 501 2013 58 62
30. D.A. Koster, K. Palle, E.S. Bot, M.A. Bjornsti, and N.H. Dekker Antitumour drugs impede DNA uncoiling by topoisomerase I Nature 448 2007 213 217
31. F. Kouzine, S. Sanford, Z. Elisha-Feil, and D. Levens The functional response of upstream DNA to dynamic supercoiling in vivo Nat. Struct. Mol. Biol. 15 2008 146 154
32. F. Kouzine, A. Gupta, L. Baranello, D. Wojtowicz, K. Ben-Aissa, J. Liu, T.M. Przytycka, and D. Levens Transcription-dependent dynamic supercoiling is a short-range genomic force Nat. Struct. Mol. Biol. 20 2013 396 403
33. M. Kretzschmar, M. Meisterernst, and R.G. Roeder Identification of human DNA topoisomerase I as a cofactor for activator-dependent transcription by RNA polymerase II Proc. Natl. Acad. Sci. USA 90 1993 11508 11512
34. H. Kwak, and J.T. Lis Control of transcriptional elongation Annu. Rev. Genet. 47 2013 483 508
35. G.S. Laco, and Y. Pommier Role of a tryptophan anchor in human topoisomerase I structure, function and inhibition Biochem. J. 411 2008 523 530
36. J.P. Laine, P.L. Opresko, F.E. Indig, J.A. Harrigan, C. von Kobbe, and V.A. Bohr Werner protein stimulates topoisomerase I DNA relaxation activity Cancer Res. 63 2003 7136 7146
37. C.J. Li, L. Averboukh, and A.B. Pardee beta-Lapachone, a novel DNA topoisomerase I inhibitor with a mode of action different from camptothecin J. Biol. Chem. 268 1993 22463 22468
38. L.F. Liu, and J.C. Wang Supercoiling of the DNA template during transcription Proc. Natl. Acad. Sci. USA 84 1987 7024 7027
39. J. Liu, F. Kouzine, Z. Nie, H.J. Chung, Z. Elisha-Feil, A. Weber, K. Zhao, and D. Levens The FUSE/FBP/FIR/TFIIH system is a molecular machine programming a pulse of c-myc expression EMBO J. 25 2006 2119 2130
40. W. Liu, Q. Ma, K. Wong, W. Li, K. Ohgi, J. Zhang, A.K. Aggarwal, and M.G. Rosenfeld Brd4 and JMJD6-associated anti-pause enhancers in regulation of transcriptional pause release Cell 155 2013 1581 1595
41. 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
42. J. Ma, L. Bai, and M.D. Wang Transcription under torsion Science 340 2013 1580 1583
43. E. Maldonado, R. Drapkin, and D. Reinberg Purification of human RNA polymerase II and general transcription factors Methods Enzymol. 274 1996 72 100
44. T. Maruyama, A. Farina, A. Dey, J. Cheong, V.P. Bermudez, T. Tamura, S. Sciortino, J. Shuman, J. Hurwitz, and K. Ozato A Mammalian bromodomain protein, brd4, interacts with replication factor C and inhibits progression to S phase Mol. Cell. Biol. 22 2002 6509 6520
45. A. Merino, K.R. Madden, W.S. Lane, J.J. Champoux, and D. Reinberg DNA topoisomerase I is involved in both repression and activation of transcription Nature 365 1993 227 232
46. Z.H. Miao, A. Player, U. Shankavaram, Y.H. Wang, D.B. Zimonjic, P.L. Lorenzi, Z.Y. Liao, H. Liu, T. Shimura, H.L. Zhang, and et al. Nonclassic functions of human topoisomerase I: genome-wide and pharmacologic analyses Cancer Res. 67 2007 8752 8761
47. C. Naughton, N. Avlonitis, S. Corless, J.G. Prendergast, I.K. Mati, P.P. Eijk, S.L. Cockroft, M. Bradley, B. Ylstra, and N. Gilbert Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures Nat. Struct. Mol. Biol. 20 2013 387 395
48. Z. Nie, G. Hu, G. Wei, K. Cui, A. Yamane, W. Resch, R. Wang, D.R. Green, L. Tessarollo, R. Casellas, and et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells Cell 151 2012 68 79
49. J.D. Parvin, and P.A. Sharp DNA topology and a minimal set of basal factors for transcription by RNA polymerase II Cell 73 1993 533 540
50. M.C. Patel, M. Debrosse, M. Smith, A. Dey, W. Huynh, N. Sarai, T.D. Heightman, T. Tamura, and K. Ozato 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 2013 2497 2507
51. J.M. Pedersen, J. Fredsoe, M. Roedgaard, L. Andreasen, K. Mundbjerg, M. Kruhøffer, M. Brinch, M.H. Schierup, L. Bjergbaek, and A.H. Andersen DNA Topoisomerases maintain promoters in a state competent for transcriptional activation in Saccharomyces cerevisiae PLoS Genet. 8 2012 e1003128
52. B.M. Peterlin, and D.H. Price Controlling the elongation phase of transcription with P-TEFb Mol. Cell 23 2006 297 305
53. Y. Pommier Topoisomerase I inhibitors: camptothecins and beyond Nat. Rev. Cancer 6 2006 789 802
54. Y. Pommier DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition Chem. Rev. 109 2009 2894 2902
55. J. Puc, P. Kozbial, W. Li, Y. Tan, Z. Liu, T. Suter, K.A. Ohgi, J. Zhang, A.K. Aggarwal, and M.G. Rosenfeld Ligand-dependent enhancer activation regulated by topoisomerase-I activity Cell 160 2015 367 380
56. Y. Ramanathan, S.M. Rajpara, S.M. Reza, E. Lees, S. Shuman, M.B. Mathews, and T. Pe'ery Three RNA polymerase II carboxyl-terminal domain kinases display distinct substrate preferences J. Biol. Chem. 276 2001 10913 10920
57. M.R. Redinbo, L. Stewart, P. Kuhn, J.J. Champoux, and W.G. Hol Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA Science 279 1998 1504 1513
58. J. Roca Transcriptional inhibition by DNA torsional stress Transcription 2 2011 82 85
59. S. Sainsbury, J. Niesser, and P. Cramer Structure and function of the initially transcribing RNA polymerase II-TFIIB complex Nature 493 2013 437 440
60. B.M. Shykind, J. Kim, L. Stewart, J.J. Champoux, and P.A. Sharp Topoisomerase I enhances TFIID-TFIIA complex assembly during activation of transcription Genes Dev. 11 1997 397 407
61. D.T. Simmons, R. Roy, L. Chen, D. Gai, and P.W. Trowbridge The activity of topoisomerase I is modulated by large T antigen during unwinding of the SV40 origin J. Biol. Chem. 273 1998 20390 20396
62. O. Sordet, S. Larochelle, E. Nicolas, E.V. Stevens, C. Zhang, K.M. Shokat, R.P. Fisher, and Y. Pommier Hyperphosphorylation of RNA polymerase II in response to topoisomerase I cleavage complexes and its association with transcription- and BRCA1-dependent degradation of topoisomerase I J. Mol. Biol. 381 2008 540 549
63. L. Spangler, X. Wang, J.W. Conaway, R.C. Conaway, and A. Dvir TFIIH action in transcription initiation and promoter escape requires distinct regions of downstream promoter DNA Proc. Natl. Acad. Sci. USA 98 2001 5544 5549
64. L. Stewart, M.R. Redinbo, X. Qiu, W.G. Hol, and J.J. Champoux A model for the mechanism of human topoisomerase I Science 279 1998 1534 1541
65. D. Strumberg, A.A. Pilon, M. Smith, R. Hickey, L. Malkas, and Y. Pommier Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff Mol. Cell. Biol. 20 2000 3977 3987
66. S.S. Teves, and S. Henikoff Transcription-generated torsional stress destabilizes nucleosomes Nat. Struct. Mol. Biol. 21 2014 88 94
67. F. Tirode, D. Busso, F. Coin, and J.M. Egly Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7 Mol. Cell 3 1999 87 95
68. T. Uemura, and M. Yanagida Isolation of type I and II DNA topoisomerase mutants from fission yeast: single and double mutants show different phenotypes in cell growth and chromatin organization EMBO J. 3 1984 1737 1744
69. M.D. Wang, M.J. Schnitzer, H. Yin, R. Landick, J. Gelles, and S.M. Block Force and velocity measured for single molecules of RNA polymerase Science 282 1998 902 907
70. S.Y. Wu, and C.M. Chiang The double bromodomain-containing chromatin adaptor Brd4 and transcriptional regulation J. Biol. Chem. 282 2007 13141 13145
71. J. Wu, H.P. Phatnani, T.S. Hsieh, and A.L. Greenleaf The phosphoCTD-interacting domain of Topoisomerase I Biochem. Biophys. Res. Commun. 397 2010 117 119
72. 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
73. A.M. Zhelkovsky, and C.L. Moore Overexpression of human DNA topoisomerase I in insect cells using a baculovirus vector Protein Expr. Purif. 5 1994 364 370
74. K.L. Zobeck, M.S. Buckley, W.R. Zipfel, and J.T. Lis Recruitment timing and dynamics of transcription factors at the Hsp70 loci in living cells Mol. Cell 40 2010 965 975