Cyclin-dependent kinase 7 controls mRNA synthesis by affecting stability of preinitiation complexes, leading to altered gene expression, cell cycle progression, and survival of tumor cells

Molecular and Cellular Biology

Volumn 34, Issue 19, 2014, Pages 3675-3688

  Kelso, Timothy W R ^a   Baumgart, Karen ^a   Eickhoff, Jan ^b   Albert, Thomas ^a   Antrecht, Claudia ^a   Lemcke, Sarah ^a   Klebl, Bert ^b   Meisterernst, Michael ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b Lead Discovery Center GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE 7; LDC 3140; LDC 4297; PROTEIN P53; RNA POLYMERASE II; UNCLASSIFIED DRUG; BS 181; BS-181; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE ACTIVATING KINASE; CYCLIN-DEPENDENT KINASE-ACTIVATING KINASE; LDC3140; LDC4297; MESSENGER RNA; PROTEIN KINASE INHIBITOR; PURINE DERIVATIVE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; ROSCOVITINE; TRIAZINE DERIVATIVE;

APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; M PHASE CELL CYCLE CHECKPOINT; MESSENGER RNA SYNTHESIS; TUMOR CELL; CELL CYCLE; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; NEOPLASM; PHOSPHORYLATION; TUMOR CELL LINE;

APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HUMANS; NEOPLASMS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PURINES; PYRAZOLES; PYRIMIDINES; RNA POLYMERASE II; RNA, MESSENGER; TRIAZINES;

EID: 84906956187     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00595-14     Document Type: Article

References (51)

1. Malumbres M, Barbacid M. 2005. Mammalian cyclin-dependent kinases. Trends Biochem. Sci. 30:630-641. http://dx.doi.org/10.1016/j.tibs.2005.09.005.
2. Akoulitchev S, Ma¨kela¨ TP, Weinberg RA, Reinberg D. 1995. Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature 377:557-560. http://dx.doi.org/10.1038/377557a0.
3. Cismowski MJ, Laff GM, Solomon MJ, Reed SI. 1995. KIN28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity. Mol. Cell. Biol. 15:2983-2992.
4. Valay JG, Simon M, Dubois MF, Bensaude O, Facca C, Faye G. 1995. The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J. Mol. Biol. 249:535-544. http://dx.doi.org/10.1006/jmbi.1995.0316.
5. Liu Y, Kung C, Fishburn J, Ansari AZ, Shokat KM, Hahn S. 2004. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol. Cell. Biol. 24:1721-1735. http://dx.doi.org/10.1128/MCB.24.4.1721-1735.2004.
6. Wohlbold L, Larochelle S, Liao JC-F, Livshits G, Singer J, Shokat KM, Fisher RP. 2006. The cyclin-dependent kinase (CDK) family member PNQALRE/CCRK supports cell proliferation but has no intrinsic CDKactivating kinase (CAK) activity. Cell Cycle 5:546-554. http://dx.doi.org/10.4161/cc.5.5.2541.
7. Ganuza M, Sa´iz-Ladera C, Cañamero M, Go´mez G, Schneider R, Blasco MA, Pisano D, Paramio JM, Santamari´a D, Barbacid M. 2012. Genetic inactivation of Cdk7 leads to cell cycle arrest and induces premature aging due to adult stem cell exhaustion. EMBO J. 31:2498-2510. http://dx.doi.org/10.1038/emboj.2012.94.
8. Schachter MM, Merrick KA, Larochelle S, Hirschi A, Zhang C, Shokat KM, Rubin SM, Fisher RP. 2013. A Cdk7-Cdk4 T-loop phosphorylation cascade promotesG1 progression. Mol. Cell 50:250-260. http://dx.doi.org/10.1016/j.molcel.2013.04.003.
9. Roeder RG. 2005. Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett. 579:909-915. http://dx.doi.org/10.1016/j.febslet.2004.12.007.
10. Roy R, Adamczewski JP, Seroz T, Vermeulen W, Tassan JP, Schaeffer L, Nigg EA, Hoeijmakers JH, Egly JM. 1994. The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell 79:1093- 1101. http://dx.doi.org/10.1016/0092-8674(94)90039-6.
11. Trigon S, Serizawa H, Conaway JW, Conaway RC, Jackson SP, Morange M. 1998. Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases. J. Biol. Chem. 273:6769-6775. http://dx.doi.org/10.1074/jbc.273.12.6769.
12. Pinhero R, Liaw P, Bertens K, Yankulov K. 2004. Three cyclindependent kinases preferentially phosphorylate different parts of the Cterminal domain of the large subunit of RNA polymerase II. Eur. J. Biochem. 271:1004-1014. http://dx.doi.org/10.1111/j.1432-1033.2004.04002.x.
13. Akhtar MS, Heidemann M, Tietjen JR, Zhang DW, Chapman RD, Eick D, Ansari AZ. 2009. TFIIH kinase places bivalent marks on the carboxyterminal domain of RNA polymerase II. Mol. Cell 34:387-393. http://dx.doi.org/10.1016/j.molcel.2009.04.016.
14. Glover-Cutter K, Larochelle S, Erickson B, Zhang C, Shokat K, Fisher RP, Bentley DL. 2009. TFIIH-associated Cdk7 kinase functions in phosphorylation of C-terminal domain Ser7 residues, promoter-proximal pausing, and termination by RNA polymerase II. Mol. Cell. Biol. 29:5455- 5464. http://dx.doi.org/10.1128/MCB.00637-09.
15. Kim M, Suh H, Cho E-J, Buratowski S. 2009. Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem. 284: 26421-26426. http://dx.doi.org/10.1074/jbc.M109.028993.
16. Boeing S, Rigault C, Heidemann M, Eick D, Meisterernst M. 2010. RNA polymerase II C-terminal heptarepeat domain Ser-7 phosphorylation is established in a mediator-dependent fashion. J. Biol. Chem. 285:188-196. http://dx.doi.org/10.1074/jbc.M109.046565.
17. Shiekhattar R, Mermelstein F, Fisher RP, Drapkin R, Dynlacht B, Wessling HC, Morgan DO, Reinberg D. 1995. Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374:283-287. http://dx.doi.org/10.1038/374283a0.
18. Li B, Carey M, Workman JL. 2007. The role of chromatin during transcription. Cell 128:707-719. http://dx.doi.org/10.1016/j.cell.2007.01.015.
19. Phatnani HP, Greenleaf AL. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:2922-2936. http://dx.doi.org/10.1101/gad.1477006.
20. Wong KH, Jin Y, Struhl K. 2014. TFIIH phosphorylation of the Pol II CTDstimulates mediator dissociation from the preinitiation complex and promoter escape. Mol. Cell 54:601-612. http://dx.doi.org/10.1016/j.molcel.2014.03.024.
21. Larochelle S, Amat R, Glover-Cutter K, Sanso´ M, Zhang C, Allen JJ, Shokat KM, Bentley DL, Fisher RP. 2012. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat. Struct. Mol. Biol. 19:1108-1116. http://dx.doi.org/10.1038/nsmb.2399.
22. Helenius K, Yang Y, Tselykh TV, Pessa HKJ, Frilander MJ, Ma¨kela¨ TP. 2011. Requirement of TFIIH kinase subunit Mat1 for RNA Pol II C-terminal domain Ser5 phosphorylation, transcription and mRNA turnover. Nucleic Acids Res. 39:5025-5035. http://dx.doi.org/10.1093/nar/gkr107.
23. Albert TK, Rigault C, Eickhoff J, Baumgart K, Antrecht C, Klebl B, Mittler G, Meisterernst M. 2014. Characterisation of molecular and cellular CDK9 functions using a novel specific inhibitor. Br. J. Pharmacol. 171:55-68. http://dx.doi.org/10.1111/bph.12408.
24. Dignam JD, Lebovitz RM, Roeder RG. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489. http://dx.doi.org/10.1093/nar/11.5.1475.
25. Uhlmann T, Boeing S, Lehmbacher M, Meisterernst M. 2007. The VP16 activation domain establishes an active mediator lacking CDK8 in vivo. J. Biol. Chem. 282:2163-2173. http://dx.doi.org/10.1074/jbc.M608451200.
26. Vojnic E, Mourão A, Seizl M, Simon B, Wenzeck L, Larivie`re L, Baumli S, Baumgart K, Meisterernst M, Sattler M, Cramer P. 2011. Structure and VP16 binding of the Mediator Med25 activator interaction domain. Nat. Struct. Mol. Biol. 18:404-409. http://dx.doi.org/10.1038/nsmb.1997.
27. Albert TK, Grote K, Boeing S, Meisterernst M. 2010. Basal core promoters control the equilibrium between negative cofactor 2 and preinitiation complexes in human cells. Genome Biol. 11:R33. http://dx.doi.org/10.1186/gb-2010-11-3-r33.
28. Ali S, Heathcote DA, Kroll SHB, Jogalekar AS, Scheiper B, Patel H, Brackow J, Siwicka A, Fuchter MJ, Periyasamy M, Tolhurst RS, Kanneganti SK, Snyder JP, Liotta DC, Aboagye EO, Barrett AGM, Coombes RC. 2009. The development of a selective cyclin-dependent kinase inhibitor that shows antitumor activity. Cancer Res. 69:6208-6215. http://dx.doi.org/10.1158/0008-5472.CAN-09-0301.
29. Jazbutyte V, Thum T. 2010. MicroRNA-21: from cancer to cardiovascu-lar disease. Curr. Drug Targets 11:926-935. http://dx.doi.org/10.2174/138945010791591403.
30. Takamizawa J, Konishi H, Yanagisawa K, Tomida S, Osada H, Endoh H, Harano T, Yatabe Y, Nagino M, Nimura Y, Mitsudomi T, Takahashi T. 2004. Reduced expression of the let-7 microRNAs in human lung cancers in association with shortened postoperative survival. Cancer Res. 64: 3753-3756. http://dx.doi.org/10.1158/0008-5472.CAN-04-0637.
31. Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM. 2004. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc. Natl. Acad. Sci. U. S. A. 101:2999-3004. http://dx.doi.org/10.1073/pnas.0307323101.
32. Neff AT, Lee JY, Wilusz J, Tian B, Wilusz CJ. 2012. Global analysis reveals multiple pathways for unique regulation of mRNA decay in induced pluripotent stem cells. Genome Res. 22:1457-1467. http://dx.doi.org/10.1101/gr.134312.111.
33. Patel MC, Debrosse M, Smith M, Dey A, Huynh W, Sarai N, Heightman TD, Tamura T, Ozato K. 2013. 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. 33:2497-2507. http://dx.doi.org/10.1128/MCB.01180-12.
34. Singh J, Padgett RA. 2009. Rates of in situ transcription and splicing in large human genes. Nat. Struct. Mol. Biol. 16:1128-1133. http://dx.doi.org/10.1038/nsmb.1666.
35. Gebara MM, Sayre MH, Corden JL. 1997. Phosphorylation of the carboxy- terminal repeat domain in RNA polymerase II by cyclin-dependent kinases is sufficient to inhibit transcription. J. Cell Biochem. 64:390-402. http://dx.doi.org/10.1002/(SICI)1097-4644(19970301)64:3390::AID-J CB63.0.CO;2-Q.
36. Rickert P, Corden JL, Lees E. 1999. Cyclin C/CDK8 and cyclin H/CDK7/ p36 are biochemically distinct CTD kinases. Oncogene 18:1093-1102. http://dx.doi.org/10.1038/sj.onc.1202399.
37. Czudnochowski N, Bo¨sken CA, Geyer M. 2012. Serine-7 but not serine-5 phosphorylation primesRNApolymerase IICTDfor P-TEFb recognition. Nat. Commun. 3:842. http://dx.doi.org/10.1038/ncomms1846.
38. Derheimer FA, O'Hagan HM, Krueger HM, Hanasoge S, Paulsen MT, Ljungman M. 2007. RPA and ATR link transcriptional stress to p53. Proc. Natl. Acad. Sci. U. S. A. 104:12778-12783. http://dx.doi.org/10.1073/pnas.0705317104.
39. Arima Y, Nitta M, Kuninaka S, Zhang D, Fujiwara T, Taya Y, Nakao M, Saya H. 2005. Transcriptional blockade induces p53-dependent apoptosis associated with translocation of p53 to mitochondria. J. Biol. Chem. 280: 19166-19176. http://dx.doi.org/10.1074/jbc.M410691200.
40. Blaydes JP, Hupp TR. 1998. DNA damage triggers DRB-resistant phosphorylation of human p53 at the CK2 site. Oncogene 17:1045-1052. http://dx.doi.org/10.1038/sj.onc.1202014.
41. Ljungman M, Zhang F, Chen F, Rainbow AJ, McKay BC. 1999. Inhibition of RNA polymerase II as a trigger for the p53 response. Oncogene 18:583-592. http://dx.doi.org/10.1038/sj.onc.1202356.
42. Ko LJ, Shieh SY, Chen X, Jayaraman L, Tamai K, Taya Y, Prives C, Pan ZQ. 1997. p53 is phosphorylated by CDK7-cyclin H in a p36MAT1- dependent manner. Mol. Cell. Biol. 17:7220-7229.
43. Lu H, Fisher RP, Bailey P, Levine AJ. 1997. The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol. Cell. Biol. 17:5923- 5934.
44. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, Golub TR, Lander ES, Young RA. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728. http://dx.doi.org/10.1016/S0092-8674(00)81641-4.
45. Ohkuma Y, Roeder RG. 1994. Regulation of TFIIH ATPase and kinase activities by TFIIE during active initiation complex formation. Nature 368:160-163. http://dx.doi.org/10.1038/368160a0.
46. Zawel L, Kumar KP, Reinberg D. 1995. Recycling of the general transcription factors during RNA polymerase II transcription. Genes Dev. 9:1479-1490. http://dx.doi.org/10.1101/gad.9.12.1479.
47. Peterlin BM, Price DH. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297-305. http://dx.doi.org/10.1016/j.molcel.2006.06.014.
48. Wada T, Takagi T, Yamaguchi Y, Watanabe D, Handa H. 1998. Evidence that P-TEFb alleviates the negative effect of DSIF on RNA polymerase II-dependent transcription in vitro. EMBO J. 17:7395-7403. http://dx.doi.org/10.1093/emboj/17.24.7395.
49. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. C-Myc regulates transcriptional pause release. Cell 141: 432-445. http://dx.doi.org/10.1016/j.cell.2010.03.030.
50. Lis JT, Mason P, Peng J, Price DH, Werner J. 2000. P-TEFb kinase recruitment and function at heat shock loci. Genes Dev. 14:792-803.
51. Olive V, Jiang I, He L. 2010. Mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int. J. Biochem. Cell Biol. 42:1348-1354. http://dx.doi.org/10.1016/j.biocel.2010.03.004.