Requirement of TFIIH kinase subunit Mat1 for RNA Pol II C-terminal domain Ser5 phosphorylation, transcription and mRNA turnover

Nucleic Acids Research

Volumn 39, Issue 12, 2011, Pages 5025-5035

  Helenius, Katja ^a,b   Yang, Ying ^a,b   Tselykh, Timofey V ^a,b   Pessa, Heli K J ^a   Frilander, Mikko J ^a   Mäkelä, Tomi P ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 70; MESSENGER RNA; PHOSPHOTRANSFERASE; PROTEIN C FOS; RNA POLYMERASE II; SERINE; TFIIH KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAT1; UNCLASSIFIED DRUG;

ANIMAL CELL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FIBROBLAST; GENE DELETION; GENETIC ASSOCIATION; MAMMAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN METABOLISM; REVIEW; RNA SPLICING; RNA STABILITY; RNA TRANSCRIPTION; STEADY STATE;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; FIBROBLASTS; GENE DELETION; HSP70 HEAT-SHOCK PROTEINS; MICE; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-FOS; RNA CAPS; RNA POLYMERASE II; RNA SPLICING; RNA STABILITY; RNA, MESSENGER; SERINE; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 79960284319     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr107     Document Type: Review

References (66)

1. Saunders, A., Core, L.J. and Lis, J.T. (2006) Breaking barriers to transcription elongation. Nat. Rev., 7, 557-567. (Pubitemid 44325347)
2. Tirode, F., Busso, D., Coin, F. and Egly, J.M. (1999) Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol. Cell, 3, 87-95. (Pubitemid 29292480)
3. Coin, F., Oksenych, V., Mocquet, V., Groh, S., Blattner, C. and Egly, J.M. (2008) Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Mol. Cell, 31, 9-20. (Pubitemid 351916723)
4. Roy, R., Adamczewski, J.P., Seroz, T., Vermeulen, W., Tassan, J.P., Schaeffer, L., Nigg, E.A., Hoeijmakers, J.H. and Egly, J.M. (1994) The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell, 79, 1093-1101.
5. Serizawa, H., Makela, T.P., Conaway, J.W., Conaway, R.C., Weinberg, R.A. and Young, R.A. (1995) Association of Cdk-activating kinase subunits with transcription factor TFIIH. Nature, 374, 280-282.
6. Shiekhattar, R., Mermelstein, F., Fisher, R.P., Drapkin, R., Dynlacht, B., Wessling, H.C., Morgan, D.O. and Reinberg, D. (1995) Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature, 374, 283-287.
7. Adamczewski, J.P., Rossignol, M., Tassan, J.P., Nigg, E.A., Moncollin, V. and Egly, J.M. (1996) MAT1, cdk7 and cyclin H form a kinase complex which is UV light-sensitive upon association with TFIIH. EMBO J., 15, 1877-1884. (Pubitemid 26119692)
8. Rossi, D.J., Londesborough, A., Korsisaari, N., Pihlak, A., Lehtonen, E., Henkemeyer, M. and Makela, T.P. (2001) Inability to enter S phase and defective RNA polymerase II CTD phosphorylation in mice lacking Mat1. EMBO J., 20, 2844-2856. (Pubitemid 32938567)
9. Korsisaari, N., Rossi, D.J., Paetau, A., Charnay, P., Henkemeyer, M. and Makela, T.P. (2002) Conditional ablation of the Mat1 subunit of TFIIH in Schwann cells provides evidence that Mat1 is not required for general transcription. J. Cell Sci., 115, 4275-4284. (Pubitemid 35460698)
10. Helenius, K., Yang, Y., Alasaari, J. and Makela, T.P. (2009) Mat1 inhibits peroxisome proliferator-activated receptor gamma-mediated adipocyte differentiation. Mol. Cell. Biol., 29, 315-323.
11. Chang, W.H. and Kornberg, R.D. (2000) Electron crystal structure of the transcription factor and DNA repair complex, core TFIIH. Cell, 102, 609-613.
12. Egloff, S. and Murphy, S. (2008) Cracking the RNA polymerase II CTD code. Trends Genet., 24, 280-288.
13. Glover-Cutter, K., Larochelle, S., Erickson, B., Zhang, C., Shokat, K., Fisher, R.P. and Bentley, D.L. (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.
14. Donner, A.J., Ebmeier, C.C., Taatjes, D.J. and Espinosa, J.M. (2010) CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat. Struct. Mol. Biol., 17, 194-201.
15. Perales, R. and Bentley, D. (2009) "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell, 36, 178-191.
16. Pei, Y., Schwer, B. and Shuman, S. (2003) Interactions between fission yeast Cdk9, its cyclin partner Pch1, and mRNA capping enzyme Pct1 suggest an elongation checkpoint for mRNA quality control. J. Biol. Chem., 278, 7180-7188. (Pubitemid 36800717)
17. Guiguen, A., Soutourina, J., Dewez, M., Tafforeau, L., Dieu, M., Raes, M., Vandenhaute, J., Werner, M. and Hermand, D. (2007) Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J., 26, 1552-1559. (Pubitemid 46480946)
18. Qiu, H., Hu, C. and Hinnebusch, A.G. (2009) Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell, 33, 752-762.
19. Viladevall, L., St Amour, C.V., Rosebrock, A., Schneider, S., Zhang, C., Allen, J.J., Shokat, K.M., Schwer, B., Leatherwood, J.K. and Fisher, R.P. (2009) TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol. Cell, 33, 738-751.
20. Ng, H.H., Robert, F., Young, R.A. and Struhl, K. (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell, 11, 709-719. (Pubitemid 36385124)
21. Xiao, T., Kao, C.F., Krogan, N.J., Sun, Z.W., Greenblatt, J.F., Osley, M.A. and Strahl, B.D. (2005) Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell. Biol., 25, 637-651. (Pubitemid 40096585)
22. Qiu, H., Hu, C., Wong, C.M. and Hinnebusch, A.G. (2006) The Spt4p subunit of yeast DSIF stimulates association of the Paf1 complex with elongating RNA polymerase II. Mol. Cell. Biol., 26, 3135-3148.
23. Govind, C.K., Qiu, H., Ginsburg, D.S., Ruan, C., Hofmeyer, K., Hu, C., Swaminathan, V., Workman, J.L., Li, B. and Hinnebusch, A.G. (2010) Phosphorylated Pol II CTD recruits multiple HDACs, including Rpd3C(S), for methylation-dependent deacetylation of ORF nucleosomes. Mol. Cell, 39, 234-246.
24. Lee, J.H. and Skalnik, D.G. (2008) Wdr82 is a C-terminal domain-binding protein that recruits the Setd1A Histone H3-Lys4 methyltransferase complex to transcription start sites of transcribed human genes. Mol. Cell. Biol., 28, 609-618.
25. Garber, M.E., Mayall, T.P., Suess, E.M., Meisenhelder, J., Thompson, N.E. and Jones, K.A. (2000) CDK9 autophosphorylation regulates high-affinity binding of the human immunodeficiency virus type 1 tat-P-TEFb complex to TAR RNA. Mol. Cell. Biol., 20, 6958-6969.
26. Gomes, N.P., Bjerke, G., Llorente, B., Szostek, S.A., Emerson, B.M. and Espinosa, J.M. (2006) Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev., 20, 601-612. (Pubitemid 43345325)
27. Rickert, P., Corden, J.L. and Lees, E. (1999) Cyclin C/CDK8 and cyclin H/CDK7/p36 are biochemically distinct CTD kinases. Oncogene, 18, 1093-1102. (Pubitemid 29086287)
28. Mäkelä , T.P., Parvin, J.D., Kim, J., Huber, L.J., Sharp, P.A. and Weinberg, R.A. (1995) A kinase-deficient transcription factor IIH is functional in basal and activated transcription. Proc. Natl Acad. Sci. USA, 92, 5174-5178.
29. Akoulitchev, S., Mäkelä , T.P., Weinberg, R.A. and Reinberg, D. (1995) Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature, 377, 557-560.
30. Holstege, F.C., Jennings, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S. and Young, R.A. (1998) Dissecting the regulatory circuitry of a eukaryotic genome. Cell, 95, 717-728. (Pubitemid 28544132)
31. Komarnitsky, P., Cho, E.J. and Buratowski, S. (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev., 14, 2452-2460.
32. Schroeder, S.C., Schwer, B., Shuman, S. and Bentley, D. (2000) Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev., 14, 2435-2440.
33. Kim, M., Suh, H., Cho, E.J. and Buratowski, S. (2009) Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem., 284, 26421-26426.
34. Faye, G., Simon, M., Valay, J.G., Fesquet, D. and Facca, C. (1997) Rig2, a RING finger protein that interacts with the Kin28/Ccl1 CTD kinase in yeast. Mol. Gen. Genet., 255, 460-466. (Pubitemid 27390143)
35. Jona, G., Livi, L.L. and Gileadi, O. (2002) Mutations in the RING domain of TFB3, a subunit of yeast transcription factor IIH, reveal a role in cell cycle progression. J. Biol. Chem., 277, 39409-39416. (Pubitemid 35190915)
36. Kanin, E.I., Kipp, R.T., Kung, C., Slattery, M., Viale, A., Hahn, S., Shokat, K.M. and Ansari, A.Z. (2007) Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl Acad. Sci. USA, 104, 5812-5817. (Pubitemid 47175616)
37. Hong, S.W., Hong, S.M., Yoo, J.W., Lee, Y.C., Kim, S., Lis, J.T. and Lee, D.K. (2009) 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, 106, 14276-14280.
38. Lee, K.M., Miklos, I., Du, H., Watt, S., Szilagyi, Z., Saiz, J.E., Madabhushi, R., Penkett, C.J., Sipiczki, M., Bahler, J. et al. (2005) Impairment of the TFIIH-associated CDK-activating kinase selectively affects cell cycle-regulated gene expression in fission yeast. Mol. Biol. Cell, 16, 2734-2745. (Pubitemid 40741220)
39. Wallenfang, M.R. and Seydoux, G. (2002) cdk-7 is required for mRNA transcription and cell cycle progression in Caenorhabditis elegans embryos. Proc. Natl Acad. Sci. USA, 99, 5527-5532. (Pubitemid 34411582)
40. Larochelle, S., Pandur, J., Fisher, R.P., Salz, H.K. and Suter, B. (1998) Cdk7 is essential for mitosis and for in vivo Cdk-activating kinase activity. Genes Dev., 12, 370-381. (Pubitemid 28084265)
41. Leclerc, V., Raisin, S. and Leopold, P. (2000) Dominant-negative mutants reveal a role for the Cdk7 kinase at the mid-blastula transition in Drosophila embryos. EMBO J., 19, 1567-1575. (Pubitemid 30182164)
42. Schwartz, B.E., Larochelle, S., Suter, B. and Lis, J.T. (2003) Cdk7 is required for full activation of Drosophila heat shock genes and RNA polymerase II phosphorylation in vivo. Mol. Cell. Biol., 23, 6876-6886. (Pubitemid 37214657)
43. Sano, M., Izumi, Y., Helenius, K., Asakura, M., Rossi, D.J., Xie, M., Taffet, G., Hu, L., Pautler, R.G., Wilson, C.R. et al. (2007) Menage-à-trois 1 is critical for the transcriptional function of PPARγ coactivator 1. Cell Metab., 5, 129-142. (Pubitemid 46172920)
44. Larochelle, S., Merrick, K., Terret, M., Wohbold, L., Barboza, N.M., Zhang, C., Shokat, K.M., Jallepalli, P.V. and Fisher, R.P. (2007) Requirements for Cdk7 in the Assembly of Cdk1/Cyclin B and Activation of Cdk2 Revealed by Chemical Genetics in Human Cells. Mol. Cell, 25, 839-850. (Pubitemid 46442792)
45. Pessa, H.K., Ruokolainen, A. and Frilander, M.J. (2006) The abundance of the spliceosomal snRNPs is not limiting the splicing of U12-type introns. RNA, 12, 1883-1892. (Pubitemid 44484261)
46. Boisvert, F.M., Hendzel, M.J. and Bazett-Jones, D.P. (2000) Promyelocytic leukemia (PML) nuclear bodies are protein structures that do not accumulate RNA. J. Cell Biol., 148, 283-292. (Pubitemid 30078240)
47. Dolken, L., Ruzsics, Z., Radle, B., Friedel, C.C., Zimmer, R., Mages, J., Hoffmann, R., Dickinson, P., Forster, T., Ghazal, P. et al. (2008) High-resolution gene expression profiling for simultaneous kinetic parameter analysis of RNA synthesis and decay. RNA, 14, 1959-1972.
48. Jao, C.Y. and Salic, A. (2008) Exploring RNA transcription and turnover in vivo by using click chemistry. Proc. Natl Acad. Sci. USA, 105, 15779-15784.
49. Friedel, C.C., Dolken, L., Ruzsics, Z., Koszinowski, U.H. and Zimmer, R. (2009) Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res., 37, e115.
50. Guzder, S.N., Qiu, H., Sommers, C.H., Sung, P., Prakash, L. and Prakash, S. (1994) DNA repair gene RAD3 of S. cerevisiae is essential for transcription by RNA polymerase II. Nature, 367, 91-94. (Pubitemid 24038539)
51. Lee, D. and Lis, J.T. (1998) Transcriptional activation independent of TFIIH kinase and the RNA polymerase II mediator in vivo. Nature, 393, 389-392. (Pubitemid 28269715)
52. Ho, C.K. and Shuman, S. (1999) Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell, 3, 405-411. (Pubitemid 29290681)
53. McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., Siderovski, D., Hessel, A., Foster, S., Shuman, S. and Bentley, D.L. (1997) 50-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev., 11, 3306-3318. (Pubitemid 28023955)
54. Akhtar, M.S., Heidemann, M., Tietjen, J.R., Zhang, D.W., Chapman, R.D., Eick, D. and Ansari, A.Z. (2009) TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell, 34, 387-393.
55. Egloff, S., O'Reilly, D., Chapman, R.D., Taylor, A., Tanzhaus, K., Pitts, L., Eick, D. and Murphy, S. (2007) Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science, 318, 1777-1779. (Pubitemid 350274388)
56. Larochelle, S., Batliner, J., Gamble, M.J., Barboza, N.M., Kraybill, B.C., Blethrow, J.D., Shokat, K.M. and Fisher, R.P. (2006) Dichotomous but stringent substrate selection by the dual-function Cdk7 complex revealed by chemical genetics. Nat. Struct. Mol. Biol., 13, 55-62. (Pubitemid 43049403)
57. Milne, T.A., Dou, Y., Martin, M.E., Brock, H.W., Roeder, R.G. and Hess, J.L. (2005) MLL associates specifically with a subset of transcriptionally active target genes. Proc. Natl Acad. Sci. USA, 102, 14765-14770. (Pubitemid 41457130)
58. Wang, P., Lin, C., Smith, E.R., Guo, H., Sanderson, B.W., Wu, M., Gogol, M., Alexander, T., Seidel, C., Wiedemann, L.M. et al. (2009) Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol., 29, 6074-6085.
59. Molina-Navarro, M.M., Castells-Roca, L., Belli, G., Garcia-Martinez, J., Marin-Navarro, J., Moreno, J., Perez-Ortin, J.E. and Herrero, E. (2008) Comprehensive transcriptional analysis of the oxidative response in yeast. J. Biol. Chem., 283, 17908-17918.
60. Rodriguez-Gabriel, M.A., Watt, S., Bahler, J. and Russell, P. (2006) Upf1, an RNA helicase required for nonsense-mediated mRNA decay, modulates the transcriptional response to oxidative stress in fission yeast. Mol. Cell. Biol., 26, 6347-6356. (Pubitemid 44277876)
61. Bond, A.T., Mangus, D.A., He, F. and Jacobson, A. (2001) Absence of Dbp2p alters both nonsense-mediated mRNA decay and rRNA processing. Mol. Cell. Biol., 21, 7366-7379. (Pubitemid 32953489)
62. Fan, J., Yang, X., Wang, W., Wood, W.H. III, Becker, K.G. and Gorospe, M. (2002) Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc. Natl Acad. Sci. USA, 99, 10611-10616.
63. Kawai, T., Fan, J., Mazan-Mamczarz, K. and Gorospe, M. (2004) Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol., 24, 6773-6787. (Pubitemid 38944356)
64. Jensen, T.H., Patricio, K., McCarthy, T. and Rosbash, M. (2001) A block to mRNA nuclear export in S. cerevisiae leads to hyperadenylation of transcripts that accumulate at the site of transcription. Mol. Cell, 7, 887-898. (Pubitemid 32436448)
65. Custodio, N., Vivo, M., Antoniou, M. and Carmo-Fonseca, M. (2007) Splicing-and cleavage-independent requirement of RNA polymerase II CTD for mRNA release from the transcription site. J. Cell Biol., 179, 199-207. (Pubitemid 350004884)
66. Meininghaus, M., Chapman, R.D., Horndasch, M. and Eick, D. (2000) Conditional expression of RNA polymerase II in mammalian cells. Deletion of the carboxy-terminal domain of the large subunit affects early steps in transcription. J. Biol. Chem., 275, 24375-24382. (Pubitemid 30626527)