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Research Article

Promoter-proximal pausing of RNA polymerase II: an opportunity to regulate gene transcription

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Pages 31-42 | Received 28 Aug 2009, Accepted 20 Nov 2009, Published online: 22 Feb 2010

References

  • Orphanides G, Reinberg D. A unified theory of gene expression. Cell 2002, 108, 439–451.
  • Papavassiliou AG. Transcription factors. N Engl J Med 1995, 332, 45–47.
  • Barnes PJ, Adcock IM. Transcription factors and asthma. Eur Respir J 1998, 12, 221–234.
  • Lewis BA, Reinberg D. The mediator coactivator complex: functional and physical roles in transcriptional regulation. J Cell Sci 2003, 116, 3667–3675.
  • Spiegelman BM, Heinrich R. Biological control through regulated transcriptional coactivators. Cell 2004, 119, 157–167.
  • Price DH. Poised polymerases: on your mark…get set…go! Mol Cell 2008, 30, 7–10.
  • Wade JT, Struhl K. The transition from transcriptional initiation to elongation. Curr Opin Genetics Dev 2008, 18, 130–136.
  • Core LJ, Lis J. Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 2008, 319, 1791–1792.
  • Uptain SM, Kane CM, Chamberlin MJ. Basic mechanisms of transcript elongation and its regulation. Annu Rev Biochem 1997, 66, 117–172.
  • Collart MA, Tourkine N, Belin D, Vassalli P, Jeanteur P, Blanchard JM. c-fos gene transcription in murine macrophages is modulated by a calcium-dependent block to elongation in intron 1. Mol Cell Biol 1991, 11, 2826–2831.
  • Krumm A, Meulia T, Groudine M. Common mechanisms for the control of eukaryotic transcriptional elongation. Bioessays 1993, 15, 659–665.
  • Werlen G, Belin D, Conne B, Roche E, Lew DP, Prentki M. Intracellular Ca2+ and the regulation of early response gene expression in HL-60 myeloid leukemia cells. J Biol Chem 1993, 268, 16596–16601.
  • Coulon V, Veyrune JL, Tourkine N, Vie A, Hipskind RA, Blanchard JM. A novel calcium signaling pathway targets the c-fos intragenic transcriptional pausing site. J Biol Chem 1999, 274, 30439–30446.
  • Ryser S, Tortola S, van Haasteren G, Muda M, Li S, Schlegel W. MAP kinase phosphatase-1 gene transcription in rat neuroendocrine cells is modulated by a calcium-sensitive block to elongation in the first exon. J Biol Chem 2001, 276, 33319–33327.
  • Spencer CA, Groudine M. Transcription elongation and eukaryotic gene regulation. Oncogene 1990, 5, 777–785.
  • Bentley DL, Groudine M. Sequence requirements for premature termination of transcription in the human c-myc gene. Cell 1988, 53, 245–256.
  • Mechti N, Piechaczyk M, Blanchard JM, Jeanteur P, Lebleu B. Sequence requirements for premature transcription arrest within the first intron of the mouse c-fos gene. Mol Cell Biol 1991, 11, 2832–2841.
  • Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322, 1845–1848.
  • Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, Flynn RA, Young RA, Sharp PA. Divergent transcription from active promoters. Science 2008, 322, 1849–1851.
  • Preker P, Nielsen J, Kammler S, Lykke-Andersen S, Christensen MS, Mapendano CK, Schierup MH, Jensen TH. RNA exosome depletion reveals transcription upstream of active human promoters. Science 2008, 322, 1851–1854.
  • He Y, Vogelstein B, Velculescu VE, Papadopoulos N, Kinzler KW. The antisense transcriptomes of human cells. Science 2008, 322, 1855–1857.
  • Buratowski S. Gene expression—where to start? Science 2008, 322, 1804–1805.
  • Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA. A high-resolution map of active promoters in the human genome. Nature 2005, 436, 876–880.
  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130, 77–88.
  • Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, Adelman K, Levine M, Young RA. RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 2007, 39, 1512–1516.
  • Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS, Grissom SF, Zeitlinger J, Adelman K. RNA polymerase is poised for activation across the genome. Nat Genet 2007, 39, 1507–1511.
  • Bentley DL, Groudine M. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature 1986, 321, 702–706.
  • Eick D, Bornkamm GW. Transcriptional arrest within the first exon is a fast control mechanism in c-myc gene expression. Nucleic Acids Res 1986, 14, 8331–8346.
  • Marzluff WF Jr. Transcription of RNA in isolated nuclei. Methods Cell Biol 1978, 19, 317–332.
  • Krumm A, Meulia T, Brunvand M, Groudine M. The block to transcriptional elongation within the human c-myc gene is determined in the promoter-proximal region. Genes Dev 1992, 6, 2201–2213.
  • Orlando V. Mapping chromosomal proteins in vivo by formaldehyde-crosslinked-chromatin immunoprecipitation. Trends Biochem Sci 2000, 25, 99–104.
  • Borowiec JA, Zhang L, Sasse-Dwight S, Gralla JD. DNA supercoiling promotes formation of a bent repression loop in lac DNA. J Mol Biol 1987, 196, 101–111.
  • Wang W, Carey M, Gralla JD. Polymerase II promoter activation: closed complex formation and ATP-driven start site opening. Science 1992, 255, 450–453.
  • Fort P, Rech J, Vie A, Piechaczyk M, Bonnieu A, Jeanteur P, Blanchard JM. Regulation of c-fos gene expression in hamster fibroblasts: initiation and elongation of transcription and mRNA degradation. Nucleic Acids Res 1987, 15, 5657–5667.
  • Sobczak J, Mechti N, Tournier MF, Blanchard JM, Duguet M. c-myc and c-fos gene regulation during mouse liver regeneration. Oncogene 1989, 4, 1503–1508.
  • Lamb NJ, Fernandez A, Tourkine N, Jeanteur P, Blanchard JM. Demonstration in living cells of an intragenic negative regulatory element within the rodent c-fos gene. Cell 1990, 61, 485–496.
  • van Haasteren G, Li S, Muda M, Susini S, Schlegel W. Calcium signaling and gene expression. J Recept Signal Transduct Res 1999, 19, 481–492.
  • van Haasteren G, Li S, Ryser S, Schlegel W. Essential contribution of intron sequences to Ca(2+)-dependent activation of c-fos transcription in pituitary cells. Neuroendocrinology 2000, 72, 368–378.
  • Susini S, Van Haasteren G, Li S, Prentki M, Schlegel W. Essentiality of intron control in the induction of c-fos by glucose and glucoincretin peptides in INS-1 beta-cells. FASEB J 2000, 14, 128–136.
  • Finkbeiner S. New roles for introns: sites of combinatorial regulation of Ca2+- and cyclic AMP-dependent gene transcription. Sci STKE 2001, 94, PE1.
  • Plet A, Eick D, Blanchard JM. Elongation and premature termination of transcripts initiated from c-fos and c-myc promoters show dissimilar patterns. Oncogene 1995, 10, 319–328.
  • Pinaud, S, Mirkovitch, J. Regulation of c-fos expression by RNA polymerase elongation competence. J Mol Biol 1998, 280, 785–798.
  • Ryser S, Fujita T, Tortola S, Piuz I, Schlegel W. The rate of c-fos transcription in vivo is continuously regulated at the level of elongation by dynamic stimulus-coupled recruitment of positive transcription elongation factor b. J Biol Chem 2007, 282, 5075–5084.
  • Fujita T, Ryser S, Piuz I, Schlegel W. Up-regulation of P-TEFb by the MEK1-extracellular signal-regulated kinase signaling pathway contributes to stimulated transcription elongation of immediate early genes in neuroendocrine cells. Mol Cell Biol 2008, 28, 1630–1643.
  • Ryser S, Tortola S, van Haasteren G, Muda M, Li S, Schlegel W. MAP kinase phosphatase-1 gene transcription in rat neuroendocrine cells is modulated by a calcium-sensitive block to elongation in the first exon. J Biol Chem 2001, 276, 33319–33327.
  • Fujita T, Ryser S, Tortola S, Piuz I, Schlegel W. Gene specific recruitment of positive and negative elongation factors during stimulated transcription of the MKP-1 gene in neuroendocrine cells. Nucleic Acids Res 2007, 35, 1007–1017.
  • Aida M, Chen Y, Nakajima K, Yamaguchi Y, Wada T, Handa H. Transcriptional pausing caused by NELF plays a dual role in regulating immediate-early expression of the junB gene. Mol Cell Biol 2006, 26, 6094–6104.
  • Ucker DS, Yamamoto KR. Early events in the stimulation of mammary tumor virus RNA synthesis by glucocorticoids. Novel assays of transcription rates. J Biol Chem 1984, 259, 7416–7420.
  • Thummel CS, Burtis KC, Hogness DS. Spatial and temporal patterns of E74 transcription during Drosophila development. Cell 1990, 61, 101–111.
  • Tennyson CN, Klamut HJ, Worton RG. The human dystrophin gene requires 16 hours to be transcribed and is cotranscriptionally spliced. Nat Genet 1995, 9, 184–190.
  • Shilatifard A. Factors regulating the transcriptional elongation activity of RNA polymerase II. FASEB J 1998, 12, 1437–1446.
  • Kerppola TK, Kane CM. RNA polymerase: regulation of transcript elongation and termination. FASEB J 1991, 5, 2833–2842.
  • Aso T, Conaway JW, Conaway RC. The RNA polymerase II elongation complex. FASEB J 1995, 9, 1419–1428.
  • Sims RJ 3rd, Belotserkovskaya R, Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev 2004, 18, 2437–2468.
  • Wada T, Takagi T, Yamaguchi Y, Ferdous A, Imai T, Hirose S, Sugimoto S, Yano K, Hartzog GA, Winston F, Buratowski S, Handa H. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev 1998, 12, 343–356.
  • Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A, Sugimoto S, Hasegawa J, Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 1999, 97, 41–51.
  • Richardson JP. Rho-dependent termination and ATPases in transcript termination. Biochim Biophys Acta 2002, 1577, 251–260.
  • Narita T, Yamaguchi Y, Yano K, Sugimoto S, Chanarat S, Wada T, Kim DK, Hasegawa J, Omori M, Inukai N, Endoh M, Yamada T, Handa H. Human transcription elongation factor NELF: identification of novel subunits and reconstitution of the functionally active complex. Mol Cell Biol 2003, 23, 1863–1873.
  • Yamaguchi Y, Inukai N, Narita T, Wada T, Handa H. 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, 2918–2927.
  • Yamaguchi Y, Wada T, Watanabe D, Takagi T, Hasegawa J, Handa H. Structure and function of the human transcription elongation factor DSIF. J Biol Chem, 1999, 274, 8085–8092.
  • Lee C, Li X, Hechmer A, Eisen M, Biggin MD, Venters BJ, Jiang C, Li J, Pugh BF, Gilmour DS. NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol Cell Biol 2008, 28, 3290–3300.
  • Hendrix DA, Hong JW, Zeitlinger J, Rokhsar DS, Levine MS. Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc Natl Acad Sci USA 2008, 105, 7762–7767.
  • Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006, 23, 297–305.
  • Zhou Q, Yik JH. The Yin and Yang of P-TEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol Mol Biol Rev 2006, 70, 646–659.
  • Wada T, Takagi T, Yamaguchi Y, Watanabe D, Handa H. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J 1998, 17, 7395–7403.
  • Ivanov D, Kwak YT, Guo J, Gaynor RB. Domains in the SPT5 protein that modulate its transcriptional regulatory properties. Mol Cell Biol 2000, 20, 2970–2983.
  • Kim JB, Sharp, PA. Positive transcription elongation factor B phosphorylates hSPT5 and RNA polymerase II carboxyl-terminal domain independently of cyclin-dependent kinase-activating kinase. J Biol Chem 2001, 276, 12317–1223.
  • Bourgeois CF, Kim YK, Churcher MJ, West MJ, Karn J. Spt5 cooperates with human immunodeficiency virus type 1 Tat by preventing premature RNA release at terminator sequences. Mol Cell Biol 2002, 22, 1079–1093.
  • Yamada T, Yamaguchi Y, Inukai N, Okamoto S, Mura T, Handa H. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 2006, 20, 227–237.
  • Cheng B, Price DH. Properties of RNA polymerase II elongation complexes before and after the P-TEFb-mediated transition into productive elongation. J Biol Chem 2007, 282, 21901–21912.
  • Fujinaga K, Irwin D, Huang Y, Taube R, Kurosu T, Peterlin BM. Dynamics of human immunodeficiency virus transcription: P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol Cell Biol 2004, 24, 787–795.
  • Hirose Y, Manley JL. RNA polymerase II and the integration of nuclear events. Genes Dev 2000, 14, 1415–1429.
  • Ni Z, Schwartz BE, Werner J, Suarez JR, Lis JT. Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol Cell 2004, 13, 55–65.
  • Ni Z, Saunders A, Fuda NJ, Yao J, Suarez JR, Webb WW, Lis JT. P-TEFb is critical for the maturation of RNA polymerase II into productive elongation in vivo. Mol Cell Biol 2008, 28, 1161–1170.
  • Andrulis ED, Guzman E, Doring P, Werner J, Lis JT. High-resolution localization of Drosophila Spt5 and Spt6 at heat shock genes in vivo: roles in promoter proximal pausing and transcription elongation. Genes Dev 2000, 14, 2635–2649.
  • Boehm AK, Saunders A, Werner J, Lis JT. Transcription factor and polymerase recruitment, modification, and movement on dhsp70 in vivo in the minutes following heat shock. Mol Cell Biol 2003, 23, 7628–7637.
  • Wu CH, Yamaguchi Y, Benjamin LR, Horvat-Gordon M, Washinsky J, Enerly E, Larsson J, Lambertsson A, Handa H, Gilmour D. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. Genes Dev 2003, 17, 1402–1414.
  • Lindstrom DL, Hartzog GA. Genetic interactions of Spt4-Spt5 and TFIIS with the RNA polymerase II CTD and CTD modifying enzymes in Saccharomyces cerevisiae. Genetics 2001, 159, 487–497.
  • Lindstrom DL, Squazzo SL, Muster N, Burckin TA, Wachter KC, Emigh CA, McCleery JA, Yates JR 3rd, Hartzog GA. Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol Cell Biol 2003, 23, 1368–1378.
  • Wada T, Orphanides G, Hasegawa J, Kim DK, Shima D, Yamaguchi Y, Fukuda A, Hisatake K, Oh S, Reinberg D, Handa H. FACT relieves DSIF/NELF-mediated inhibition of transcriptional elongation and reveals functional differences between P-TEFb and TFIIH. Mol Cell 2000, 5, 1067–1072.
  • Compagnone-Post PA, Osley MA. Mutations in the SPT4, SPT5, and SPT6 genes alter transcription of a subset of histone genes in Saccharomyces cerevisiae. Genetics 1996, 143, 1543–1554.
  • Kaplan CD, Morris JR, Wu C, Winston F. Spt5 and spt6 are associated with active transcription and have characteristics of general elongation factors in D. melanogaster. Genes Dev 2000, 14, 2623–2634.
  • Saunders A, Werner J, Andrulis ED, Nakayama T, Hirose S, Reinberg D, Lis JT. Tracking FACT and the RNA polymerase II elongation complex through chromatin in vivo. Science 2003, 301, 1094–1096.
  • Belotserkovskaya R, Reinberg D. Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev 2004, 14, 139–146.
  • Wind M, Reines D. Transcription elongation factor SII. Bioessays 2000, 22, 327–336.
  • Palangat M, Renner DB, Price DH, Landick R. A negative elongation factor for human RNA polymerase II inhibits the anti-arrest transcript-cleavage factor TFIIS. Proc Natl Acad Sci USA 2005, 102, 15036–15041.
  • Adelman K, Marr MT, Werner J, Saunders A, Ni Z, Andrulis ED, Lis JT. Efficient release from promoter-proximal stall sites requires transcript cleavage factor TFIIS. Mol Cell 2005, 17, 103–112.
  • Renner DB, Yamaguchi Y, Wada T, Handa H, Price DH. A highly purified RNA polymerase II elongation control system. J Biol Chem 2001, 276, 42601–42609.
  • Zorio DA, Bentley DL. The link between mRNA processing and transcription: communication works both ways. Exp Cell Res 2004, 296, 91–97.
  • Mandal SS, Chu C, Wada T, Handa H, Shatkin AJ, Reinberg D. Functional interactions of RNA-capping enzyme with factors that positively and negatively regulate promoter escape by RNA polymerase II. Proc Natl Acad Sci USA 2004, 101, 7572–7577.
  • Pei Y, Shuman S. Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J Biol Chem 2002, 277, 19639–19648.
  • Wen Y, Shatkin AJ. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev 1999, 13, 1774–1779.
  • Squazzo SL, Costa PJ, Lindstrom DL, Kumer KE, Simic R, Jennings JL, Link AJ, Arndt KM, Hartzog GA. The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J 2002, 21, 1764–1774.
  • Hampsey M, Reinberg D. Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 2003, 113, 429–432.
  • Costa PJ, Arndt KM. Synthetic lethal interactions suggest a role for the Saccharomyces cerevisiae Rtf1 protein in transcription elongation. Genetics 2000, 156, 535–547.
  • Qiu H, Hu C, Wong CM, Hinnebusch AG. The Spt4p subunit of yeast DSIF stimulates association of the Paf1 complex with elongating RNA polymerase II. Mol Cell Biol 2006, 26, 3135–3148.
  • Ng HH, Robert F, Young RA, Struhl K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 2003, 11, 709–719.
  • Dmitriev RI, Korneenko TV, Bessonov AA, Shakhparonov MI, Modyanov NN, Pestov NB. Characterization of hampin/MSL1 as a node in the nuclear interactome. Biochem Biophys Res Commun 2007, 355, 1051–1057.
  • Thomas T, Voss AK. The diverse biological roles of MYST histone acetyltransferase family proteins. Cell Cycle 2007, 6, 696–704.
  • Gilchrist DA, Nechaev S, Lee C, Ghosh SK, Collins JB, Li L, Gilmour DS, Adelman K. NELF-mediated stalling of Pol II can enhance gene expression by blocking promoter-proximal nucleosome assembly. Genes Dev 2008, 22, 1921–1933.
  • Core LJ, Lis JT. Paused pol II captures enhancer activity and acts as a potent insulator. Genes Dev 2009, 23, 1606–1612.
  • Merika M, Thanos D. Enhanceosomes. Curr Opin Genet Dev 2001, 11, 205–208.
  • Maisonnasse-Charital Y, van Haasteren G, Massihaa A, Schlegel W, Fujita T. A functional NF-κB enhancer element in the first intron contributes to the control of c-fos transcription. Gene 2009, 430, 116–122.
  • Cui Y, Denis CL. In vivo evidence that defects in the transcriptional elongation factors RPB2, TFIIS, and SPT5 enhance upstream poly(A) site utilization. Mol Cell Biol 2003, 23, 7887–7901.
  • Narita T, Yung TM, Yamamoto J, Tsuboi Y, Tanabe H, Tanaka K, Yamaguchi Y, Handa H. NELF interacts with CBC and participates in 3’ end processing of replication-dependent histone mRNAs. Mol Cell 2007, 26, 349–365.
  • Guo S, Yamaguchi Y, Schilbach S, Wada T, Lee J, Goddard A, French D, Handa H, Rosenthal A. A regulator of transcriptional elongation controls vertebrate neuronal development. Nature 2000, 408, 366–369.
  • Krishnan K, Salomonis N, Guo S. Identification of Spt5 target genes in zebrafish development reveals its dual activity in vivo. PLoS One 2008, 3, e3621.
  • Cooper KL, Armstrong J, Moens CB. Zebrafish foggy/spt 5 is required for migration of facial branchiomotor neurons but not for their survival. Dev Dyn 2005, 234, 651–658.
  • Savage JJ, Yaden BC, Kiratipranon P, Rhodes SJ. Transcriptional control during mammalian anterior pituitary development. Gene 2003, 319, 1–19.
  • Ooi GT, Tawadros N, Escalona RM. Pituitary cell lines and their endocrine applications. Mol Cell Endocrinol 2004, 228, 1–21.
  • Keegan BR, Feldman JL, Lee DH, Koos DS, Ho RK, Stainier DY, Yelon D. The elongation factors Pandora/Spt6 and Foggy/Spt5 promote transcription in the zebrafish embryo. Development 2002, 129, 1623–1632.
  • Aiyar SE, Blair AL, Hopkinson DA, Bekiranov S, Li R. Regulation of clustered gene expression by cofactor of BRCA1 (COBRA1) in breast cancer cells. Oncogene 2007, 26, 2543–2553.
  • Bergemann AD, Cole F, Hirschhorn K. The etiology of Wolf-Hirschhorn syndrome. Trends Genet 2005, 21, 188–195.
  • Wright TJ, Costa JL, Naranjo C, Francis-West P, Altherr MR. Comparative analysis of a novel gene from the Wolf-Hirschhorn/Pitt-Rogers-Danks syndrome critical region. Genomics 1999, 59, 203–212.
  • Carè A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini P, Gu Y, Dalton ND, Elia L, Latronico MV, Høydal M, Autore C, Russo MA, Dorn GW, Ellingsen O, Ruiz-Lozano P, Peterson KL, Croce CM, Peschle C, Condorelli G. MicroRNA-133 controls cardiac hypertrophy. Nat Med 2007, 13, 613–618.
  • Dey A, Chao SH, Lane DP. HEXIM1 and the control of transcription elongation. Cell Cycle 2007, 6, 1856–1863.
  • Sano M, Abdellatif M, Oh H, Xie M, Bagella L, Giordano A, Michael LH, DeMayo FJ, Schneider MD. Activation and function of cyclin T-Cdk9 (positive transcription elongation factor-b) in cardiac muscle-cell hypertrophy. Nat Med 2002, 8, 1310–1317.
  • Sano M, Schneider MD. Cyclins that don’t cycle—cyclin T/cyclin-dependent kinase-9 determines cardiac muscle cell size. Cell Cycle 2003, 2, 99–104.
  • Sano M, Wang SC, Shirai M, Scaglia F, Xie M, Sakai S, Tanaka T, Kulkarni PA, Barger PM, Youker KA, Taffet GE, Hamamori Y, Michael LH, Craigen WJ, Schneider MD. Activation of cardiac Cdk9 represses PGC-1 and confers a predisposition to heart failure. EMBO J 2004, 23, 3559–3569.
  • Sano M, Schneider MD. Cyclin-dependent kinase-9: an RNAPII kinase at the nexus of cardiac growth and death cascades. Circ Res 2004, 95, 867–876.
  • Michels AA, Bensaude O. RNA-driven cyclin-dependent kinase regulation: when CDK9/cyclin T subunits of P-TEFb meet their ribonucleoprotein partners., Biotechnol J 2008, 3, 1022–1033.
  • Fujita T, Piuz I, Schlegel W. The transcription elongation factors NELF, DSIF and P-TEFb control constitutive transcription in a gene-specific manner. FEBS Lett 2009, 583, 2893–2898.
  • Fujita T, Piuz I, Schlegel W. Negative elongation factor NELF controls transcription of immediate early genes in a stimulus-specific manner. Exp Cell Res 2009, 315, 274–284.

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