CTCF regulates NELF, DSIF and P-TEFb recruitment during transcription

Transcription

Volumn 6, Issue 5, 2015, Pages 79-90

  Laitem, Clélia ^a,e   Zaborowska, Justyna ^a   Tellier, Michael ^a   Yamaguchi, Yuki ^b   Cao, Qingfu ^b   Egloff, Sylvain ^c   Handa, Hiroshi ^d   Murphy, Shona ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITÉ DE TOULOUSE   (France)

^d TOKYO MEDICAL UNIVERSITY   (Japan)

^e Immunocore Limited   (United Kingdom)

Author keywords

CTCF; elongation checkpoint; P TEFb; RNA Polymerase II pausing; snRNA gene; transcription

Indexed keywords

BIOLOGICAL FACTOR; DRB SENSITIVITY INDUCING FACTOR; ELONGATION FACTOR; MYC PROTEIN; NEGATIVE ELONGATION FACTOR; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; RECOMBINANT PROTEIN; RNA POLYMERASE II; SMALL INTERFERING RNA; SMALL NUCLEAR RNA; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CCCTC-BINDING FACTOR; MYC PROTEIN, HUMAN; NELF PROTEIN, HUMAN; NUCLEAR PROTEIN; REPRESSOR PROTEIN; SUPT5H PROTEIN, HUMAN; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR; U2 SMALL NUCLEAR RNA;

ARTICLE; CHEMICAL ANALYSIS; CHROMATIN IMMUNOPRECIPITATION; CLONING; CONTROLLED STUDY; DNA TRANSCRIPTION; GENE SILENCING; HUMAN; HUMAN CELL; NUCLEAR RUN ON ANALYSIS; PROTEIN DNA INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PULL DOWN ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBONUCLEASE PROTECTION ASSAY; RNA ANALYSIS; RNA PROCESSING; TRANSCRIPTION TERMINATION; WESTERN BLOTTING; GENETIC TRANSCRIPTION; GENETICS; HELA CELL LINE; METABOLISM; PHOSPHORYLATION;

GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTO-ONCOGENE PROTEINS C-MYC; REPRESSOR PROTEINS; RNA POLYMERASE II; RNA, SMALL NUCLEAR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84951908964     PISSN: 21541264     EISSN: 21541272     Source Type: Journal    
DOI: 10.1080/21541264.2015.1095269     Document Type: Article

References (62)

1. J.E.Phillips, V.G.Corces. CTCF: master weaver of the genome. Cell 2009; 137:1194-211; PMID:19563753; http://dx.doi.org/10.1016/j.cell.2009.06.001
2. V.Torrano, I.Chernukhin, F.Docquier, V.D'Arcy, J.Leon, E.Klenova, M.D.Delgado. CTCF regulates growth and erythroid differentiation of human myeloid leukemia cells. J Biol Chem 2005; 280:28152-61; PMID:15941718; http://dx.doi.org/10.1074/jbc.M501481200
3. F.P.Fiorentino, A.Giordano. The tumor suppressor role of CTCF. J Cell Physiol 2012; 227:479-92; PMID:21465478; http://dx.doi.org/10.1002/jcp.22780
4. H.Heath, C.Ribeiro de Almeida, F.Sleutels, G.Dingjan, S.van de Nobelen, I.Jonkers, K.W.Ling, J.Gribnau, R.Renkawitz, F.Grosveld, et al. CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J 2008; 27:2839-50; PMID:18923423; http://dx.doi.org/10.1038/emboj.2008.214
5. S.Cuddapah, R.Jothi, D.E.Schones, T.Y.Roh, K.Cui, K.Zhao. Global analysis of the insulator binding protein CTCF in chromatin barrier regions reveals demarcation of active and repressive domains. Genome Res 2009; 19:24-32; PMID:19056695; http://dx.doi.org/10.1101/gr.082800.108
6. E.Splinter, H.Heath, J.Kooren, R.J.Palstra, P.Klous, F.Grosveld, N.Galjart, W.de Laat. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev 2006; 20:2349-54; PMID:16951251; http://dx.doi.org/10.1101/gad.399506
7. G.N.Filippova, S.Fagerlie, E.M.Klenova, C.Myers, Y.Dehner, G.Goodwin, P.E.Neiman, S.J.Collins, V.V.Lobanenkov. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol Cell Biol 1996; 16:2802-13; PMID:8649389
8. J.Gao, J.Wang, Y.Wang, W.Dai, L.Lu. Regulation of Pax6 by CTCF during induction of mouse ES cell differentiation. PLoS One 2011; 6:e20954; PMID:21695148; http://dx.doi.org/10.1371/journal.pone.0020954
9. M.Burcin, R.Arnold, M.Lutz, B.Kaiser, D.Runge, F.Lottspeich, G.N.Filippova, V.V.Lobanenkov, R.Renkawitz. Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol Cell Biol 1997; 17:1281-8; PMID:9032255
10. E.M.Klenova, I.V.Chernukhin, A.El-Kady, R.E.Lee, E.M.Pugacheva, D.I.Loukinov, G.H.Goodwin, D.Delgado, G.N.Filippova, J.León, et al. Functional phosphorylation sites in the C-terminal region of the multivalent multifunctional transcriptional factor CTCF. Mol Cell Biol 2001; 21:2221-34; PMID:11238955; http://dx.doi.org/10.1128/MCB.21.6.2221-2234.2001
11. R.Ohlsson, V.Lobanenkov, E.Klenova. Does CTCF mediate between nuclear organization and gene expression? Bioessays 2010; 32:37-50; PMID:20020479; http://dx.doi.org/10.1002/bies.200900118
12. I.Chernukhin, S.Shamsuddin, S.Y.Kang, R.Bergstrom, Y.W.Kwon, W.Yu, J.Whitehead, R.Mukhopadhyay, F.Docquier, D.Farrar, et al. CTCF interacts with and recruits the largest subunit of RNA polymerase II to CTCF target sites genome-wide. Mol Cell Biol 2007; 27:1631-48; PMID:17210645; http://dx.doi.org/10.1128/MCB.01993-06
13. A.El-Kady, E.Klenova. Regulation of the transcription factor, CTCF, by phosphorylation with protein kinase CK2. FEBS Lett 2005; 579:1424-34; PMID:15733852; http://dx.doi.org/10.1016/j.febslet.2005.01.044
14. T.H.Kim, Z.K.Abdullaev, A.D.Smith, K.A.Ching, D.I.Loukinov, R.D.Green, M.Q.Zhang, V.V.Lobanenkov, B.Ren. Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 2007; 128:1231-45; PMID:17382889; http://dx.doi.org/10.1016/j.cell.2006.12.048
15. X.Chen, H.Xu, P.Yuan, F.Fang, M.Huss, V.B.Vega, E.Wong, Y.L.Orlov, W.Zhang, J.Jiang, et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008; 133:1106-17; PMID:18555785; http://dx.doi.org/10.1016/j.cell.2008.04.043
16. D.Schmidt, P.C.Schwalie, C.S.Ross-Innes, A.Hurtado, G.D.Brown, J.S.Carroll, P.Flicek, D.T.Odom. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 2010; 20:578-88; PMID:20219941; http://dx.doi.org/10.1101/gr.100479.109
17. L.J.Core, J.J.Waterfall, J.T.Lis. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008; 322:1845-8; PMID:19056941; http://dx.doi.org/10.1126/science.1162228
18. I.M.Min, J.J.Waterfall, L.J.Core, R.J.Munroe, J.Schimenti, J.T.Lis. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev 2011; 25:742-54; PMID:21460038; http://dx.doi.org/10.1101/gad.2005511
19. N.Hah, C.G.Danko, L.Core, J.J.Waterfall, A.Siepel, J.T.Lis, W.L.Kraus. A rapid, extensive, and transient transcriptional response to estrogen signaling in breast cancer cells. Cell 2011; 145:622-34; PMID:21549415; http://dx.doi.org/10.1016/j.cell.2011.03.042
20. S.H.Paredes, M.F.Melgar, P.Sethupathy. Promoter proximal CTCF binding is associated with an increase in the transcriptional pausing index. Bioinformatics 2013;1485-7; PMID:23047559
21. S.Shukla, E.Kavak, M.Gregory, M.Imashimizu, B.Shutinoski, M.Kashlev, P.Oberdoerffer, R.Sandberg, S.Oberdoerffer. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 2011; 479(7371):74-9; PMID: 21964334
22. Y.Wada, Y.Ohta, M.Xu, S.Tsutsumi, T.Minami, K.Inoue, D.Komura, J.Kitakami, N.Oshida, A.Papantonis, et al. A wave of nascent transcription on activated human genes. Proc Natl Acad Sci U S A 2009; 106:18357-61; PMID:19826084; http://dx.doi.org/10.1073/pnas.0902573106
23. H.Kang, P.M.Lieberman. Mechanism of glycyrrhizic acid inhibition of Kaposi's sarcoma-associated herpesvirus: disruption of CTCF-cohesin-mediated RNA polymerase II pausing and sister chromatid cohesion. J Virol 2011; 85:11159-69; PMID:21880767; http://dx.doi.org/10.1128/JVI.00720-11
24. S.Egloff, H.Al-Rawaf, D.O'Reilly, S.Murphy. Chromatin structure is implicated in “late” elongation checkpoints on the U2 snRNA and beta-actin genes. Mol Cell Biol 2009; 29:4002-13; PMID:19451231; http://dx.doi.org/10.1128/MCB.00189-09
25. K.Adelman, J.T.Lis. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet 2012; 13:720-31; PMID:22986266; http://dx.doi.org/10.1038/nrg3293
26. C.Laitem, J.Zaborowska, N.F.Isa, J.Kufs, M.Dienstbier, S.Murphy. CDK9 inhibitors define elongation checkpoints at both ends of RNA polymerase II-transcribed genes. Nat Struct Mol Biol 2015; 22:396-403; PMID:25849141
27. T.Narita, Y.Yamaguchi, K.Yano, S.Sugimoto, S.Chanarat, T.Wada, D.K.Kim, J.Hasegawa, M.Omori, N.Inukai, et al. Human transcription elongation factor NELF: identification of novel subunits and reconstitution of the functionally active complex. Mol Cell Biol 2003; 23:1863-73; PMID:12612062; http://dx.doi.org/10.1128/MCB.23.6.1863-1873.2003
28. Y.Yamaguchi, N.Inukai, T.Narita, T.Wada, H.Handa. Evidence that negative elongation factor represses transcription elongation through binding to a DRB sensitivity-inducing factor/RNA polymerase II complex and RNA. Mol Cell Biol 2002; 22:2918-27; PMID:11940650; http://dx.doi.org/10.1128/MCB.22.9.2918-2927.2002
29. T.Wada, T.Takagi, Y.Yamaguchi, A.Ferdous, T.Imai, S.Hirose, S.Sugimoto, K.Yano, G.A.Hartzog, F.Winston, et al. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev 1998; 12:343-56; PMID:9450929; http://dx.doi.org/10.1101/gad.12.3.343
30. D.K.Kim, N.Inukai, T.Yamada, A.Furuya, H.Sato, Y.Yamaguchi, T.Wada, H.Handa. Structure-function analysis of human Spt4: evidence that hSpt4 and hSpt5 exert their roles in transcriptional elongation as parts of the DSIF complex. Genes Cells 2003; 8:371-8; PMID:12653964; http://dx.doi.org/10.1046/j.1365-2443.2003.00638.x
31. C.H.Wu, Y.Yamaguchi, L.R.Benjamin, M.Horvat-Gordon, J.Washinsky, E.Enerly, J.Larsson, A.Lambertsson, H.Handa, D.Gilmour. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev 2003; 17:1402-14; PMID:12782658; http://dx.doi.org/10.1101/gad.1091403
32. Y.Yamaguchi, T.Takagi, T.Wada, K.Yano, A.Furuya, S.Sugimoto, J.Hasegawa, H.Handa. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 1999; 97:41-51; PMID:10199401; http://dx.doi.org/10.1016/S0092-8674(00)80713-8
33. Y.Yamaguchi, H.Shibata, H.Handa. Transcription elongation factors DSIF and NELF: Promoter-proximal pausing and beyond. Biochim Biophys Acta 2013; 1829:98-104; PMID:23202475; http://dx.doi.org/10.1016/j.bbagrm.2012.11.007
34. T.Yamada, Y.Yamaguchi, N.Inukai, S.Okamoto, T.Mura, H.Handa. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 2006; 21:227-37; PMID:16427012; http://dx.doi.org/10.1016/j.molcel.2005.11.024
35. N.F.Marshall, D.H.Price. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J Biol Chem 1995; 270:12335-8; PMID:7759473; http://dx.doi.org/10.1074/jbc.270.21.12335
36. T.Wada, T.Takagi, Y.Yamaguchi, D.Watanabe, H.Handa. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J 1998; 17:7395-403; PMID:9857195; http://dx.doi.org/10.1093/emboj/17.24.7395
37. N.F.Marshall, J.Peng, Z.Xie, D.H.Price. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem 1996; 271:27176-83; PMID:8900211; http://dx.doi.org/10.1074/jbc.271.43.27176
38. J.E.Medlin, P.Uguen, A.Taylor, D.L.Bentley, S.Murphy. The C-terminal domain of pol II and a DRB-sensitive kinase are required for 3′ processing of U2 snRNA. EMBO J 2003; 22:925-34; PMID:12574128; http://dx.doi.org/10.1093/emboj/cdg077
39. J.Medlin, A.Scurry, A.Taylor, F.Zhang, B.M.Peterlin, S.Murphy. P-TEFb is not an essential elongation factor for the intronless human U2 snRNA and histone H2b genes. EMBO J 2005; 24:4154-65; PMID:16308568; http://dx.doi.org/10.1038/sj.emboj.7600876
40. J.D.Dignam, R.M.Lebovitz, R.G.Roeder. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983; 11:1475-89; PMID:6828386; http://dx.doi.org/10.1093/nar/11.5.1475
41. H.O'Geen, C.M.Nicolet, K.Blahnik, R.Green, P.J.Farnham. Comparison of sample preparation methods for ChIP-chip assays. Biotechniques 2006; 41:577-80; PMID:17140114; http://dx.doi.org/10.2144/000112268
42. J.Yamamoto, Y.Hagiwara, K.Chiba, T.Isobe, T.Narita, H.Handa, Y.Yamaguchi. DSIF and NELF interact with Integrator to specify the correct post-transcriptional fate of snRNA genes. Nat Commun 2014; 5:4263; PMID:24968874
43. B.Stadelmayer, G.Micas, A.Gamot, P.Martin, N.Malirat, S.Koval, R.Raffel, B.Sobhian, D.Severac, S.Rialle, et al. Integrator complex regulates NELF-mediated RNA polymerase II pause/release and processivity at coding genes. Nat Commun 2014; 5:5531; PMID:25410209; http://dx.doi.org/10.1038/ncomms6531
44. E.P.Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57-74; PMID:22955616; http://dx.doi.org/10.1038/nature11247
45. B.Langmead, S.L.Salzberg. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357-9; PMID:22388286; http://dx.doi.org/10.1038/nmeth.1923
46. Y.Zhang, T.Liu, C.A.Meyer, J.Eeckhoute, D.S.Johnson, B.E.Bernstein, C.Nusbaum, R.M.Myers, M.Brown, W.Li, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008; 9:R137; PMID:18798982; http://dx.doi.org/10.1186/gb-2008-9-9-r137
47. S.Heinz, C.Benner, N.Spann, E.Bertolino, Y.C.Lin, P.Laslo, J.X.Cheng, C.Murre, H.Singh, C.K.Glass. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010; 38:576-89; PMID:20513432; http://dx.doi.org/10.1016/j.molcel.2010.05.004
48. P.Machanick, T.L.Bailey. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 2011; 27:1696-7; PMID:21486936; http://dx.doi.org/10.1093/bioinformatics/btr189
49. D.A.Wolf, L.J.Strobl, A.Pullner, D.Eick. Variable pause positions of RNA polymerase II lie proximal to the c-myc promoter irrespective of transcriptional activity. Nucleic Acids Res 1995; 23:3373-9; PMID:7567445; http://dx.doi.org/10.1093/nar/23.17.3373
50. A.Krumm, T.Meulia, M.Brunvand, M.Groudine. The block to transcriptional elongation within the human c-myc gene is determined in the promoter-proximal region. Genes Dev 1992; 6:2201-13; PMID:1427080; http://dx.doi.org/10.1101/gad.6.11.2201
51. S.Egloff, S.A.Szczepaniak, M.Dienstbier, A.Taylor, S.Knight, S.Murphy. The integrator complex recognizes a new double mark on the RNA polymerase II carboxyl-terminal domain. J Biol Chem 2010; 285:20564-9; PMID:20457598; http://dx.doi.org/10.1074/jbc.M110.132530
52. S.Egloff, D.O'Reilly, R.D.Chapman, A.Taylor, K.Tanzhaus, L.Pitts, D.Eick, S.Murphy. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 2007; 318:1777-9; PMID:18079403; http://dx.doi.org/10.1126/science.1145989
53. T.Xiao, J.Wallace, G.Felsenfeld. Specific sites in the C terminus of CTCF interact with the SA2 subunit of the cohesin complex and are required for cohesin-dependent insulation activity. Mol Cell Biol 2011; 31:2174-83; PMID:21444719; http://dx.doi.org/10.1128/MCB.05093-11
54. J.Sun, R.Li. Human negative elongation factor activates transcription and regulates alternative transcription initiation. J Biol Chem 2010; 285:6443-52; PMID:20028984; http://dx.doi.org/10.1074/jbc.M109.084285
55. P.B.Rahl, C.Y.Lin, A.C.Seila, R.A.Flynn, S.McCuine, C.B.Burge, P.A.Sharp, R.A.Young. c-Myc regulates transcriptional pause release. Cell 2010; 141:432-45; PMID:20434984; http://dx.doi.org/10.1016/j.cell.2010.03.030
56. Y.Yamaguchi, T.Wada, D.Watanabe, T.Takagi, J.Hasegawa, H.Handa. Structure and function of the human transcription elongation factor DSIF. J Biol Chem 1999; 274:8085-92; PMID:10075709; http://dx.doi.org/10.1074/jbc.274.12.8085
57. D.B.Renner, Y.Yamaguchi, T.Wada, H.Handa, D.H.Price. A highly purified RNA polymerase II elongation control system. J Biol Chem 2001; 276:42601-9; PMID:11553615; http://dx.doi.org/10.1074/jbc.M104967200
58. Z.Yang, J.H.Yik, R.Chen, N.He, M.K.Jang, K.Ozato, Q.Zhou. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 2005; 19:535-45; PMID:16109377; http://dx.doi.org/10.1016/j.molcel.2005.06.029
59. M.Barboric, R.M.Nissen, S.Kanazawa, N.Jabrane-Ferrat, B.M.Peterlin. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol Cell 2001; 8:327-37; PMID:11545735; http://dx.doi.org/10.1016/S1097-2765(01)00314-8
60. H.Takahashi, T.J.Parmely, S.Sato, C.Tomomori-Sato, C.A.Banks, S.E.Kong, H.Szutorisz, S.K.Swanson, S.Martin-Brown, M.P.Washburn, et al. Human mediator subunit MED26 functions as a docking site for transcription elongation factors. Cell 2011; 146:92-104; PMID:21729782; http://dx.doi.org/10.1016/j.cell.2011.06.005
61. C.T.Ong, V.G.Corces. CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet 2014; 15:234-46; PMID:24614316; http://dx.doi.org/10.1038/nrg3663
62. D.O'Reilly, O.V.Kuznetsova, C.Laitem, J.Zaborowska, M.Dienstbier, S.Murphy. Human snRNA genes use polyadenylation factors to promote efficient transcription termination. Nucleic Acids Res 2014; 42:264-75; PMID:24097444; http://dx.doi.org/10.1093/nar/gkt892