THZ1 Reveals Roles for Cdk7 in Co-transcriptional Capping and Pausing

Molecular Cell

Volumn 59, Issue 4, 2015, Pages 576-587

  Nilson, Kyle A ^a   Guo, Jiannan ^a   Turek, Michael E ^a   Brogie, John E ^a   Delaney, Elizabeth ^b   Luse, Donal S ^b   Price, David H ^a  

^a UNIVERSITY OF IOWA   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 7; FLAVOPIRIDOL; PROTEIN SERINE THREONINE KINASE INHIBITOR; THZ1; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE; CYCLIN-DEPENDENT KINASE-ACTIVATING KINASE; NELF PROTEIN, HUMAN; NUCLEAR PROTEIN; PHENYLENEDIAMINE DERIVATIVE; PYRIMIDINE DERIVATIVE; RNA POLYMERASE II; SUPT5H PROTEIN, HUMAN; THZ1 COMPOUND; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; RNA CAPPING; TRANSCRIPTION INITIATION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; KINETICS; METABOLISM; PHOSPHORYLATION; PROMOTER REGION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; RNA PROCESSING;

ANTINEOPLASTIC AGENTS; CYCLIN-DEPENDENT KINASES; HELA CELLS; HUMANS; KINETICS; NUCLEAR PROTEINS; PHENYLENEDIAMINES; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PYRIMIDINES; RNA POLYMERASE II; RNA PROCESSING, POST-TRANSCRIPTIONAL; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84939530621     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.06.032     Document Type: Article

References (57)

1. Adamson T.E., Shore S.M., Price D.H. Analysis of RNA polymerase II elongation in vitro. Methods Enzymol. 2003, 371:264-275.
2. Akoulitchev S., Mäkelä T.P., Weinberg R.A., Reinberg D. Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature 1995, 377:557-560.
3. Arner E., Daub C.O., Vitting-Seerup K., Andersson R., Lilje B., Drabløs F., Lennartsson A., Rönnerblad M., Hrydziuszko O., Vitezic M., et al. Gene regulation. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science 2015, 347:1010-1014. FANTOM Consortium.
4. Bartkowiak B., Liu P., Phatnani H.P., Fuda N.J., Cooper J.J., Price D.H., Adelman K., Lis J.T., Greenleaf A.L. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 2010, 24:2303-2316.
5. Bataille A.R., Jeronimo C., Jacques P.E., Laramée L., Fortin M.E., Forest A., Bergeron M., Hanes S.D., Robert F. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol. Cell 2012, 45:158-170.
6. Bentley D.L. Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 2014, 15:163-175.
7. Bowman E.A., Kelly W.G. RNA polymerase II transcription elongation and Pol II CTD Ser2 phosphorylation: A tail of two kinases. Nucleus 2014, 5:224-236.
8. Cheng B., Price D.H. 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.
9. Cheng B., Price D.H. Analysis of factor interactions with RNA polymerase II elongation complexes using a new electrophoretic mobility shift assay. Nucleic Acids Res. 2008, 36:e135.
10. Cheng B., Price D.H. Isolation and functional analysis of RNA polymerase II elongation complexes. Methods 2009, 48:346-352.
11. Cheng B., Li T., Rahl P.B., Adamson T.E., Loudas N.B., Guo J., Varzavand K., Cooper J.J., Hu X., Gnatt A., et al. Functional association of Gdown1 with RNA polymerase II poised on human genes. Mol. Cell 2012, 45:38-50.
12. Chipumuro E., Marco E., Christensen C.L., Kwiatkowski N., Zhang T., Hatheway C.M., Abraham B.J., Sharma B., Yeung C., Altabef A., et al. CDK7 inhibition suppresses super-enhancer-linked oncogenic transcription in MYCN-driven cancer. Cell 2014, 159:1126-1139.
13. Chiu Y.L., Ho C.K., Saha N., Schwer B., Shuman S., Rana T.M. Tat stimulates cotranscriptional capping of HIV mRNA. Mol. Cell 2002, 10:585-597.
14. Cho E.J., Takagi T., Moore C.R., Buratowski S. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 1997, 11:3319-3326.
15. Christensen C.L., Kwiatkowski N., Abraham B.J., Carretero J., Al-Shahrour F., Zhang T., Chipumuro E., Herter-Sprie G.S., Akbay E.A., Altabef A., et al. Targeting transcriptional addictions in small cell lung cancer with a covalent CDK7 inhibitor. Cancer Cell 2014, 26:909-922.
16. Coppola J.A., Field A.S., Luse D.S. Promoter-proximal pausing by RNA polymerase II in vitro: transcripts shorter than 20 nucleotides are not capped. Proc. Natl. Acad. Sci. USA 1983, 80:1251-1255.
17. Core L.J., Martins A.L., Danko C.G., Waters C.T., Siepel A., Lis J.T. Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat. Genet. 2014, 46:1311-1320.
18. Doamekpor S.K., Sanchez A.M., Schwer B., Shuman S., Lima C.D. How an mRNA capping enzyme reads distinct RNA polymerase II and Spt5 CTD phosphorylation codes. Genes Dev. 2014, 28:1323-1336.
19. Doamekpor S.K., Schwer B., Sanchez A.M., Shuman S., Lima C.D. Fission yeast RNA triphosphatase reads an Spt5 CTD code. RNA 2015, 21:113-123.
20. Egly J.M., Coin F. A history of TFIIH: two decades of molecular biology on a pivotal transcription/repair factor. DNA Repair (Amst.) 2011, 10:714-721.
21. Fisher R.P. The CDK Network: Linking Cycles of Cell Division and Gene Expression. Genes Cancer 2012, 3:731-738.
22. Ghosh A., Shuman S., Lima C.D. Structural insights to how mammalian capping enzyme reads the CTD code. Mol. Cell 2011, 43:299-310.
23. Glover-Cutter K., Larochelle S., Erickson B., Zhang C., Shokat K., Fisher R.P., Bentley D.L. 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. 2009, 29:5455-5464.
24. Grohmann D., Nagy J., Chakraborty A., Klose D., Fielden D., Ebright R.H., Michaelis J., Werner F. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 2011, 43:263-274.
25. Guo J., Price D.H. RNA polymerase II transcription elongation control. Chem. Rev. 2013, 113:8583-8603.
26. Heidemann M., Hintermair C., Voß K., Eick D. Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. Biochim. Biophys. Acta 2013, 1829:55-62.
27. Ho C.K., Shuman S. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 1999, 3:405-411.
28. Hong S.W., Hong S.M., Yoo J.W., Lee Y.C., Kim S., Lis J.T., Lee D.K. Phosphorylation of the RNA polymerase II C-terminal domain by TFIIH kinase is not essential for transcription of Saccharomyces cerevisiae genome. Proc. Natl. Acad. Sci. USA 2009, 106:14276-14280.
29. Hsu P.L., Yang F., Smith-Kinnaman W., Yang W., Song J.E., Mosley A.L., Varani G. Rtr1 is a dual specificity phosphatase that dephosphorylates Tyr1 and Ser5 on the RNA polymerase II CTD. J. Mol. Biol. 2014, 426:2970-2981.
30. Jeronimo C., Robert F. Kin28 regulates the transient association of Mediator with core promoters. Nat. Struct. Mol. Biol. 2014, 21:449-455.
31. Kamenski T., Heilmeier S., Meinhart A., Cramer P. Structure and mechanism of RNA polymerase II CTD phosphatases. Mol. Cell 2004, 15:399-407.
32. Kanin E.I., Kipp R.T., Kung C., Slattery M., Viale A., Hahn S., Shokat K.M., Ansari A.Z. Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. USA 2007, 104:5812-5817.
33. Kelso T.W., Baumgart K., Eickhoff J., Albert T., Antrecht C., Lemcke S., Klebl B., Meisterernst M. 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. Mol. Cell. Biol. 2014, 34:3675-3688.
34. Kwiatkowski N., Zhang T., Rahl P.B., Abraham B.J., Reddy J., Ficarro S.B., Dastur A., Amzallag A., Ramaswamy S., Tesar B., et al. Targeting transcription regulation in cancer with a covalent CDK7 inhibitor. Nature 2014, 511:616-620.
35. Larochelle S., Amat R., Glover-Cutter K., Sansó M., Zhang C., Allen J.J., Shokat K.M., Bentley D.L., Fisher R.P. Cyclin-dependent kinase control of the initiation-to-elongation switch of RNA polymerase II. Nat. Struct. Mol. Biol. 2012, 19:1108-1115.
36. Liu P., Xiang Y., Fujinaga K., Bartholomeeusen K., Nilson K.A., Price D.H., Peterlin B.M. Release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein (snRNP) activates hexamethylene bisacetamide-inducible protein (HEXIM1) transcription. J. Biol. Chem. 2014, 289:9918-9925.
37. Mandal S.S., Chu C., Wada T., Handa H., Shatkin A.J., 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.
38. Marshall N.F., Peng J., Xie Z., Price D.H. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J. Biol. Chem. 1996, 271:27176-27183.
39. Martinez-Rucobo F.W., Sainsbury S., Cheung A.C., Cramer P. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 2011, 30:1302-1310.
40. Martinez-Rucobo F.W., Kohler R., van de Waterbeemd M., Heck A.J., Hemann M., Herzog F., Stark H., Cramer P. Molecular Basis of Transcription-Coupled Pre-mRNA Capping. Mol. Cell 2015, 58:1079-1089.
41. McCracken S., Fong N., Rosonina E., Yankulov K., Brothers G., Siderovski D., Hessel A., Foster S., Shuman S., Bentley D.L. 5'-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 1997, 11:3306-3318.
42. Moteki S., Price D. Functional coupling of capping and transcription of mRNA. Mol. Cell 2002, 10:599-609.
43. Pei Y., Shuman S. Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J. Biol. Chem. 2002, 277:19639-19648.
44. Plaschka C., Larivière L., Wenzeck L., Seizl M., Hemann M., Tegunov D., Petrotchenko E.V., Borchers C.H., Baumeister W., Herzog F., et al. Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 2015, 518:376-380.
45. Poss Z.C., Ebmeier C.C., Taatjes D.J. The Mediator complex and transcription regulation. Crit. Rev. Biochem. Mol. Biol. 2013, 48:575-608.
46. Rahl P.B., Lin C.Y., Seila A.C., Flynn R.A., McCuine S., Burge C.B., Sharp P.A., Young R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
47. Rasmussen E.B., Lis J.T. In vivo transcriptional pausing and cap formation on three Drosophila heat shock genes. Proc. Natl. Acad. Sci. USA 1993, 90:7923-7927.
48. Renner D.B., Yamaguchi Y., Wada T., Handa H., Price D.H. A highly purified RNA polymerase II elongation control system. J. Biol. Chem. 2001, 276:42601-42609.
49. Schneider S., Pei Y., Shuman S., Schwer B. Separable functions of the fission yeast Spt5 carboxyl-terminal domain (CTD) in capping enzyme binding and transcription elongation overlap with those of the RNA polymerase II CTD. Mol. Cell. Biol. 2010, 30:2353-2364.
50. Schwartz B.E., Larochelle S., Suter B., Lis J.T. Cdk7 is required for full activation of Drosophila heat shock genes and RNA polymerase II phosphorylation in vivo. Mol. Cell. Biol. 2003, 23:6876-6886.
51. Schwer B., Shuman S. Deciphering the RNA polymerase II CTD code in fission yeast. Mol. Cell 2011, 43:311-318.
52. Tirode F., Busso D., Coin F., Egly J.M. Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol. Cell 1999, 3:87-95.
53. Wen Y., Shatkin A.J. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 1999, 13:1774-1779.
54. Wong K.H., Jin Y., Struhl K. TFIIH phosphorylation of the Pol II CTD stimulates mediator dissociation from the preinitiation complex and promoter escape. Mol. Cell 2014, 54:601-612.
55. Xiang K., Nagaike T., Xiang S., Kilic T., Beh M.M., Manley J.L., Tong L. Crystal structure of the human symplekin-Ssu72-CTD phosphopeptide complex. Nature 2010, 467:729-733.
56. Yamaguchi Y., Shibata H., Handa H. Transcription elongation factors DSIF and NELF: promoter-proximal pausing and beyond. Biochim. Biophys. Acta 2013, 1829:98-104.
57. Yue Z., Maldonado E., Pillutla R., Cho H., Reinberg D., Shatkin A.J. Mammalian capping enzyme complements mutant Saccharomyces cerevisiae lacking mRNA guanylyltransferase and selectively binds the elongating form of RNA polymerase II. Proc. Natl. Acad. Sci. USA 1997, 94:12898-12903.