Separate Domains of Fission Yeast Cdk9 (P-tefb) Are Required for Capping Enzyme Recruitment and Primed (Ser7-Phosphorylated) Rpb1 Carboxyl-Terminal Domain Substrate Recognition

Molecular and Cellular Biology

Volumn 32, Issue 13, 2012, Pages 2372-2383

  St Amour, Courtney V ^a,b   Sansó, Miriam ^a   Bösken, Christian A ^c   Lee, Karen M ^a   Larochelle, Stéphane ^a   Zhang, Chao ^d,e   Shokat, Kevan M ^d   Geyer, Matthias ^c   Fisher, Robert P ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' CAP METHYLTRANSFERASE PCM1; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE 9; METHYLTRANSFERASE; RNA POLYMERASE II; RNA POLYMERASE II RBP1 SUBUNIT; SERINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME BINDING; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SCHIZOSACCHAROMYCES POMBE; SEQUENCE ANALYSIS;

CATALYTIC DOMAIN; CYCLIN-DEPENDENT KINASE 9; ENZYME ACTIVATION; GENES, FUNGAL; METHYLTRANSFERASES; MODELS, BIOLOGICAL; MUTATION; NUCLEOTIDYLTRANSFERASES; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA POLYMERASE II; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SERINE; SUBSTRATE SPECIFICITY; TRANSCRIPTIONAL ELONGATION FACTORS;

SCHIZOSACCHAROMYCETACEAE;

EID: 84864015492     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.06657-11     Document Type: Article

References (62)

1. Akhtar MS, et al. 2009. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell 34:387-393.
2. Bahler J, et al. 1998. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14:943-951.
3. Bartkowiak B, et al. 2010. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 24:2303-2316.
4. Blazek D, et al. 2011. The Cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev. 25:2158-2172.
5. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Mol. Cell 36:541-546.
6. Chapman RD, et al. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318:1780-1782.
7. Cho EJ, Kobor MS, Kim M, Greenblatt J, Buratowski S. 2001. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev. 15:3319-3329.
8. Czudnochowski N, Bösken CA, Geyer M. Serine-7 but not serine-5 phosphorylation primesRNApolymerase IICTDfor P-TEFb recognition. Nat. Commun., in press.
9. Desmoucelles C, Pinson B, Saint-Marc C, Daignan-Fornier B. 2002. Screening the yeast "disruptome" for mutants affecting resistance to the immunosuppressive drug, mycophenolic acid. J. Biol. Chem. 277:27036-27044.
10. Egloff S, et al. 2007. Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science 318:1777-1779.
11. Escobar-Henriques M, Balguerie A, Monribot C, Boucherie H, Daignan-Fornier B. 2001. Proteome analysis and morphological studies reveal multiple effects of the immunosuppressive drug mycophenolic acid specifically resulting from guanylic nucleotide depletion. J. Biol. Chem. 276: 46237-46242.
12. Exinger F, Lacroute F. 1992. 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 22:9-11.
13. Feaver WJ, Svejstrup JQ, Henry NL, Kornberg RD. 1994. Relationship of CDK-activating kinase and RNA polymerase II CTD kinase TFIIH/ TFIIK. Cell 79:1103-1109.
14. Fuda NJ, Ardehali MB, Lis JT. 2009. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461:186-192.
15. Glover-Cutter K, et al. 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.
16. Grohmann D, et al. 2011. The initiation factor tfe and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43:263-274.
17. Guiguen A, et al. 2007. Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J. 26:1552-1559.
18. Hengartner CJ, et al. 1998. Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell 2:43-53.
19. Hsin JP, Sheth A, Manley JL. 2011. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3= end processing. Science 334: 683-686.
20. Jang MK, et al. 2005. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase IIdependent transcription. Mol. Cell 19:523-534.
21. Kanin EI, et al. 2007. Chemical inhibition of the TFIIH-associated kinase Cdk7/Kin28 does not impair global mRNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 104:5812-5817.
22. Karagiannis J, Balasubramanian MK. 2007. A cyclin-dependent kinase that promotes cytokinesis through modulating phosphorylation of the carboxy terminal domain of the RNA Pol II Rpb1p sub-unit. PLoS One 2:e433. doi:10.1371/journal.pone.0000433.
23. Keogh MC, Podolny V, Buratowski S. 2003. Bur1 kinase is required for efficient transcription elongation by RNA polymerase II. Mol. Cell. Biol. 23:7005-7018.
24. Kim H, et al. 2010. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat. Struct. Mol. Biol. 17:1279-1286.
25. Kim M, Suh H, Cho EJ, Buratowski S. 2009. Phosphorylation of the yeast Rpb1 C-terminal domain at serines 2, 5, and 7. J. Biol. Chem. 284:26421-26426.
26. Klein BJ, et al. 2011. RNA polymerase and transcription elongation factor Spt4/5 complex structure. Proc. Natl. Acad. Sci. U. S. A. 108:546-550.
27. Komarnitsky P, Cho EJ, Buratowski S. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14:2452-2460.
28. Larochelle S, et al. 2006. Dichotomous but stringent substrate selection by the dual-function Cdk7 complex revealed by chemical genetics. Nat. Struct. Mol. Biol. 13:55-62.
29. Larochelle S, et al. 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.
30. Liu Y, et al. 2004. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol. Cell. Biol. 24:1721-1735.
31. Liu Y, et al. 2009. Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol. Cell. Biol. 29:4852-4863.
32. Martinez-Rucobo FW, Sainsbury S, Cheung AC, Cramer P. 2011. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J. 30:1302-1310.
33. Mayer A, et al. 2010. Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol. 17:1272-1278.
34. Moreno S, Klar A, Nurse P. 1991. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194:795-823.
35. Park JH, Ahn SH. 2010. IMP dehydrogenase is recruited to the transcription complex through serine 2 phosphorylation of RNA polymerase II. Biochem. Biophys. Res. Commun. 392:588-592.
36. Pei Y, et al. 2006. Cyclin-dependent kinase 9 (Cdk9) of fission yeast is activated by the CDK-activating kinase Csk1, overlaps functionally with the TFIIH-associated kinase Mcs6, and associates with the mRNA cap methyltransferase Pcm1 in vivo. Mol. Cell. Biol. 26:777-788.
37. Pei Y, Hausmann S, Ho CK, Schwer B, Shuman S. 2001. The length, phosphorylation state, and primary structure of the RNA polymerase II carboxyl-terminal domain dictate interactions with mRNA capping enzymes. J. Biol. Chem. 276:28075-28082.
38. Pei Y, Schwer B, 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.
39. Pei Y, Shuman S. 2003. Characterization of the Schizosaccharomyces pombe Cdk9/Pch1 protein kinase: Spt5 phosphorylation, autophosphorylation, and mutational analysis. J. Biol. Chem. 278:43346-43356.
40. Pei Y, Shuman S. 2002. Interactions between fission yeast mRNA capping enzymes and elongation factor Spt5. J. Biol. Chem. 277:19639-19648.
41. Perales R, Bentley D. 2009. "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36:178-191.
42. Peterlin BM, Price DH. 2006. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 23:297-305.
43. Phatnani HP, Greenleaf AL. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20:2922-2936.
44. Qiu H, Hu C, Hinnebusch AG. 2009. Phosphorylation of the Pol II CTD by KIN28 enhances BUR1/BUR2 recruitment and Ser2 CTD phosphorylation near promoters. Mol. Cell 33:752-762.
45. Rickert P, Corden JL, Lees E. 1999. Cyclin C/CDK8 and cyclin H/CDK7/ p36 are biochemically distinct CTD kinases. Oncogene 18:1093-1102.
46. Roy R, et al. 1994. The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell 79:1093-1101.
47. 45a.Saiz JE, Fisher RP. 2002. A CDK-activating kinase network is required in cell cycle control and transcription in fission yeast. Curr. Biol. 12:1100-1105.
48. Sanso M, et al. 2011. Gcn5 facilitates Pol II progression, rather than recruitment to nucleosome-depleted stress promoters, in Schizosaccharomyces pombe. Nucleic Acids Res. 39:6369-6379.
49. Schneider S, Pei Y, Shuman S, Schwer B. 2010. 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. 30:2353-2364.
50. Schroeder SC, Schwer B, Shuman S, Bentley D. 2000. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14:2435-2440.
51. Schwer B, Shuman S. 2011. Deciphering the RNA polymerase II CTD code in fission yeast. Mol. Cell 43:311-318.
52. Shaw RJ, Wilson JL, Smith KT, Reines D. 2001. Regulation of an IMP dehydrogenase gene and its overexpression in drug-sensitive transcription elongation mutants of yeast. J. Biol. Chem. 276:32905-32916.
53. Shuman S. 2001. Structure, mechanism, and evolution of the mRNA capping apparatus. Prog. Nucleic Acid Res. Mol. Biol. 66:1-40.
54. Taube R, Lin X, Irwin D, Fujinaga K, Peterlin BM. 2002. Interaction between P-TEFb and the C-terminal domain of RNA polymerase II activates transcriptional elongation from sites upstream or downstream of target genes. Mol. Cell. Biol. 22:321-331.
55. Tietjen JR, et al. 2010. Chemical-genomic dissection of the CTD code. Nat. Struct. Mol. Biol. 17:1154-1161.
56. Trigon S, et al. 1998. Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases. J. Biol. Chem. 273:6769-6775.
57. Viladevall L, et al. 2009. TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol. Cell 33:738-751.
58. 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.
59. Wen Y, Shatkin AJ. 1999. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev. 13:1774-1779.
60. Yamada T, et al. 2006. P-TEFb-mediated phosphorylation of hSpt5 Cterminal repeats is critical for processive transcription elongation. Mol. Cell 21:227-237.
61. Yamaguchi Y, et al. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97: 41-51.
62. Yang Z, et al. 2005. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol. Cell 19:535-545.