Chemical-genomic dissection of the CTD code

Nature Structural and Molecular Biology

Volumn 17, Issue 9, 2010, Pages 1154-1161

  Tietjen, Joshua R ^a   Zhang, David W ^a   Rodríguez Molina, Juan B ^a   White, Brent E ^a   Akhtar, Md Sohail ^a   Heidemann, Martin ^b   Li, Xin ^a,c   Chapman, Rob D ^b   Shokat, Kevan ^d   Keles, Sündüz ^c   Eick, Dirk ^b   Ansari, Aseem Z ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Munich Center for Integrated Protein Science   (Germany)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUR1 ENZYME; PHOSPHOTRANSFERASE; RNA POLYMERASE II; UNCLASSIFIED DRUG; PROTEIN SERINE THREONINE KINASE; UNTRANSLATED RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; GENETIC ANALYSIS; GENOME; HUMAN; PRIORITY JOURNAL; ENZYME SPECIFICITY; GENETIC TRANSCRIPTION; METABOLISM; MULTIGENE FAMILY; OPEN READING FRAME; PHOSPHORYLATION;

GENOME; MULTIGENE FAMILY; OPEN READING FRAMES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA POLYMERASE II; RNA, UNTRANSLATED; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 77956344274     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1900     Document Type: Article

References (64)

1. Phatnani, H.P. & Greenleaf, A.L. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20, 2922-2936 (2006).
2. Buratowski, S. The CTD code. Nat. Struct. Biol. 10, 679-680 (2003).
3. Corden, J.L. Transcription: seven ups the code. Science 318, 1735-1736 (2007).
4. Perales, R. & Bentley, D. "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36, 178-191 (2009).
5. Lee, T.I. & Young, R. Transcription of eukaryotic protein-coding genes. Annu. Rev. Genet. 34, 77-137 (2000).
6. Myers, L.C. & Kornberg, R.D. Mediator of transcriptional regulation. Annu. Rev. Biochem. 69, 729-749 (2000).
7. Sims, R.J. III, Belotserkovskaya, R. & Reinberg, D. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18, 2437-2468 (2004).
8. Liu, Y. et al. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol. Cell. Biol. 24, 1721-1735 (2004).
9. Ansari, A.Z., Ogirala, A. & Ptashne, M. Transcriptional activating regions target attached substrates to a cyclin-dependent kinase. Proc. Natl. Acad. Sci. USA 102, 2346-2349 (2005).
10. Riedl, T. & Egly, J.M. Phosphorylation in transcription: the CTD and more. Gene Expr. 9, 3-13 (2000).
11. Max, T., Sogaard, M. & Svejstrup, J. Hyperphosphorylation of the C-terminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J. Biol. Chem. 282, 14113-14120 (2007).
12. Schroeder, S.C., Schwer, B., Shuman, S. & Bentley, D. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14, 2435-2440 (2000).
13. Komarnitsky, P., Cho, E.J. & Buratowski, S. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460 (2000).
14. Ng, H.H., Robert, F., Young, R.A. & Struhl, K. 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 (2003).
15. Krogan, N.J. et al. Methylation of Histone H3 by Set2 in Saccharomyces cerevisiae Is linked to transcriptional elongation by RNA polymerase II. Mol. Cell. Biol. 23, 4207-4218 (2003).
16. Carrozza, M.J. et al. Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123, 581-592 (2005).
17. Mosley, A.L. et al. Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation. Mol. Cell 34, 168-178 (2009).
18. Brès, V., Yoh, S. & Jones, K. The multi-tasking P-TEFb complex. Curr. Opin. Cell Biol. 20, 334-340 (2008).
19. Buratowski, S. Progression through the RNA polymerase II CTD cycle. Mol. Cell 36, 541-546 (2009).
20. Kornblihtt, A.R., De La Mata, M., Fededa, J., Munoz, M. & Nogues, G. Multiple links between transcription and splicing. RNA 10, 1489-1498 (2004).
21. Wood, A. & Shilatifard, A. Bur1/Bur2 and the Ctk complex in yeast: the split personality of mammalian P-TEFb. Cell Cycle 5, 1066-1068 (2006).
22. Liu, Y. et al. Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol. Cell. Biol. 29, 4852-4863 (2009).
23. Zhou, K., Kuo, W., Fillingham, J. & Greenblatt, J. Control of transcriptional elongation and cotranscriptional histone modifcation by the yeast BUR kinase substrate Spt5. Proc. Natl. Acad. Sci. USA 106, 6956-6961 (2009).
24. Chu, Y., Simic, R., Warner, M., Arndt, K. & Prelich, G. Regulation of histone modifcation and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J. 26, 4646-4656 (2007).
25. Keogh, M.C., Podolny, V. & Buratowski, S. Bur1 kinase is required for effcient transcription elongation by RNA polymerase II. Mol. Cell. Biol. 23, 7005-7018 (2003).
26. Proudfoot, N.J., Furger, A. & Dye, M.J. Integrating mRNA processing with transcription. Cell 108, 501-512 (2002).
27. Licatalosi, D.D. et al. Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol. Cell 9, 1101-1111 (2002).
28. Ahn, S.H., Kim, M. & Buratowski, S. Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell 13, 67-76 (2004).
29. Cho, E.J., Kobor, M.S., Kim, M., Greenblatt, J. & Buratowski, S. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15, 3319-3329 (2001).
30. Krishnamurthy, S., He, X., Reyes-Reyes, M., Moore, C. & Hampsey, M. Ssu72 is an RNA polymerase II CTD phosphatase. Mol. Cell 14, 387-394 (2004).
31. Steinmetz, E.J., Conrad, N., Brow, D. & Corden, J. RNA-binding protein Nrd1 directs poly (A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413, 327-331 (2001).
32. Egloff, S. et al. Serine-7 of the RNA polymerase II CTD is specifcally required for snRNA gene expression. Science 318, 1777-1779 (2007).
33. Baillat, D. et al. Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123, 265-276 (2005).
34. Chapman, R.D. et al. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318, 1780-1782 (2007).
35. Stiller, J.W., Mcconaughy, B. & Hall, B. Evolutionary complementation for polymerase II CTD function. Yeast 16, 57-64 (2000).
36. Egloff, S. & Murphy, S. Cracking the RNA polymerase II CTD code. Trends Genet. 24, 280-288 (2008).
37. Jenuwein, T. & Allis, C. Translating the histone code. Science 293, 1074-1080 (2001).
38. Gomes, N.P. et al. Gene-specifc requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 20, 601-612 (2006).
39. Medlin, J. et al. P-TEFb is not an essential elongation factor for the intronless human U2 snRNA and histone H2b genes. EMBO J. 24, 4154-4165 (2005).
40. Kanin, E.I. et al. Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. USA 104, 5812-5817 (2007).
41. Lee, K.M. et al. Impairment of the TFIIH-associated CDK-activating kinase selectively affects cell cycle-regulated gene expression in fssion yeast. Mol. Biol. Cell 16, 2734-2745 (2005).
42. Serizawa, H., Conaway, J. & Conaway, R. Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363, 371-374 (1993).
43. Akhtar, M.S. et al. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 34, 387-393 (2009).
44. Kim, M., Suh, H., Cho, E. & Buratowski, S. Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem. 284, 26421-26426 (2009).
45. Glover-Cutter, K. et al. 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 (2009).
46. Patturajan, M., Conrad, N., Bregman, D. & Corden, J. Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation. J. Biol. Chem. 274, 27823-27828 (1999).
47. Viladevall, L. et al. TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specifc genes in fssion yeast. Mol. Cell 33, 738-751 (2009).
48. Qiu, H., Hu, C. & Hinnebusch, A. Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 33, 752-762 (2009).
49. Steinmetz, E.J. et al. Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 24, 735-746 (2006).
50. Neil, H. et al. Widespread bidirectional promoters are the major source of cryptic transcripts in yeast. Nature 457, 1038-1042 (2009).
51. Xu, Z. et al. Bidirectional promoters generate pervasive transcription in yeast. Nature 457, 1033-1037 (2009).
52. Holstege, F.C. & Young, R. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717-728 (1998).
53. Venters, B.J. & Pugh, B. A canonical promoter organization of the transcription machinery and its regulators in the Saccharomyces genome. Genome Res. 19, 360-371 (2009).
54. Knight, Z.A. & Shokat, K.M. Features of selective kinase inhibitors. Chem. Biol. 12, 621-637 (2005).
55. Ahn, S.H., Keogh, M. & Buratowski, S. Ctk1 promotes dissociation of basal transcription factors from elongating RNA polymerase II EMBO Open. EMBO J. 28, 205-212 (2009).
56. Arigo, J.T., Eyler, D., Carroll, K. & Corden, J. Termination of cryptic unstable transcripts is directed by yeast RNA-binding proteins Nrd1 and Nab3. Mol. Cell 23, 841-851 (2006).
57. Thiebaut, M., Kisseleva-Romanova, E., Rougemaille, M., Boulay, J. & Libri, D. Transcription termination and nuclear degradation of cryptic unstable transcripts: a role for the nrd1-nab3 pathway in genome surveillance. Mol. Cell 23, 853-864 (2006).
58. Kim, M. et al. Distinct pathways for snoRNA and mRNA termination. Mol. Cell 24, 723-734 (2006).
59. Sheldon, K.E., Mauger, D. & Arndt, K. A requirement for the Saccharomyces cerevisiae Paf1 complex in snoRNA 3′ end formation. Mol. Cell 20, 225-236 (2005).
60. Lee, W. et al. A high-resolution atlas of nucleosome occupancy in yeast. Nat. Genet. 39, 1235-1244 (2007).
61. Kanin, E.I. et al. Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. USA 104, 5812-5817 (2007).
62. Rousseeuw, P. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J. Comput. Appl. Math. 20, 53-65 (1987).
63. Harbison, C.T. et al. Transcriptional regulatory code of a eukaryotic genome. Nature 431, 99-104 (2004).
64. Ansari, A.Z., Ogirala, A. & Ptashne, M. Transcriptional activating regions target attached substrates to a cyclin-dependent kinase. Proc. Natl. Acad. Sci. USA 102, 2346-2349 (2005).