The PAF Complex and Prf1/Rtf1 Delineate Distinct Cdk9-Dependent Pathways Regulating Transcription Elongation in Fission Yeast

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Mbogning, Jean ^a   Nagy, Stephen ^a   Pagé, Viviane ^a   Schwer, Beate ^b   Shuman, Stewart ^c   Fisher, Robert P ^d   Tanny, Jason C ^a  

^a MCGILL UNIVERSITY   (Canada)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 9; HISTONE H2B; POLYMERASE ASSOCIATED FACTOR; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PRF1; TRANSCRIPTION FACTOR RRF1; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE FUNCTION; GENETIC VARIABILITY; HISTONE UBIQUITINATION; NONHUMAN; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION;

BINDING SITES; CHROMATIN; CYCLIN-DEPENDENT KINASE 9; HISTONES; PHOSPHORYLATION; RNA, MESSENGER; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 84892766966     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004029     Document Type: Article

References (66)

1. Zhou Q, Li T, Price DH, (2012) RNA polymerase II elongation control. Annu Rev Biochem 81: 119-143.
2. Marshall NF, Price DH, (1995) Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J Biol Chem 270: 12335-12338.
3. 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.
4. Yamada T, Yamaguchi Y, Inukai N, Okamoto S, Mura T, et al. (2006) P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 21: 227-237.
5. Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A, et al. (1999) NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97: 41-51.
6. Murray S, Udupa R, Yao S, Hartzog G, Prelich G, (2001) Phosphorylation of the RNA polymerase II carboxy-terminal domain by the Bur1 cyclin-dependent kinase. Mol Cell Biol 21: 4089-4096.
7. Pei Y, Du H, Singer J, St Amour C, Granitto S, 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.
8. 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.
9. 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.
10. 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.
11. Sanso M, Lee KM, Viladevall L, Jacques PE, Page V, et al. (2012) A Positive Feedback Loop Links Opposing Functions of P-TEFb/Cdk9 and Histone H2B Ubiquitylation to Regulate Transcript Elongation in Fission Yeast. PLoS Genet 8: e1002822.
12. Viladevall L, St Amour CV, Rosebrock A, Schneider S, Zhang C, et al. (2009) TFIIH and P-TEFb coordinate transcription with capping enzyme recruitment at specific genes in fission yeast. Mol Cell 33: 738-751.
13. Peterlin BM, Price DH, (2006) Controlling the elongation phase of transcription with P-TEFb. Mol Cell 23: 297-305.
14. Hsin JP, Manley JL, (2012) The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 26: 2119-2137.
15. Zhou K, Kuo WH, Fillingham J, Greenblatt JF, (2009) Control of transcriptional elongation and cotranscriptional histone modification by the yeast BUR kinase substrate Spt5. Proc Natl Acad Sci U S A 106: 6956-6961.
16. Liu Y, Warfield L, Zhang C, Luo J, Allen J, 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.
17. Shchebet A, Karpiuk O, Kremmer E, Eick D, Johnsen SA, (2012) Phosphorylation by cyclin-dependent kinase-9 controls ubiquitin-conjugating enzyme-2A function. Cell Cycle 11: 2122-2127.
18. Wood A, Schneider J, Dover J, Johnston M, Shilatifard A, (2005) The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol Cell 20: 589-599.
19. 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.
20. Tomson BN, Arndt KM, (2013) The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim Biophys Acta 1829: 116-126.
21. Chen Y, Yamaguchi Y, Tsugeno Y, Yamamoto J, Yamada T, et al. (2009) DSIF, the Paf1 complex, and Tat-SF1 have nonredundant, cooperative roles in RNA polymerase II elongation. Genes Dev 23: 2765-2777.
22. Kim J, Guermah M, Roeder RG, (2010) The human PAF1 complex acts in chromatin transcription elongation both independently and cooperatively with SII/TFIIS. Cell 140: 491-503.
23. Rondon AG, Gallardo M, Garcia-Rubio M, Aguilera A, (2004) Molecular evidence indicating that the yeast PAF complex is required for transcription elongation. EMBO Rep 5: 47-53.
24. Pavri R, Zhu B, Li G, Trojer P, Mandal S, et al. (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703-717.
25. Krogan NJ, Dover J, Wood A, Schneider J, Heidt J, et al. (2003) The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol Cell 11: 721-729.
26. Zhu B, Mandal SS, Pham AD, Zheng Y, Erdjument-Bromage H, et al. (2005) The human PAF complex coordinates transcription with events downstream of RNA synthesis. Genes Dev 19: 1668-1673.
27. Penheiter KL, Washburn TM, Porter SE, Hoffman MG, Jaehning JA, (2005) A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol Cell 20: 213-223.
28. Rozenblatt-Rosen O, Nagaike T, Francis JM, Kaneko S, Glatt KA, et al. (2009) The tumor suppressor Cdc73 functionally associates with CPSF and CstF 3′ mRNA processing factors. Proc Natl Acad Sci U S A 106: 755-760.
29. Laribee RN, Krogan NJ, Xiao T, Shibata Y, Hughes TR, et al. (2005) BUR kinase selectively regulates H3 K4 trimethylation and H2B ubiquitylation through recruitment of the PAF elongation complex. Curr Biol 15: 1487-1493.
30. Qiu H, Hu C, Gaur NA, Hinnebusch AG, (2012) Pol II CTD kinases Bur1 and Kin28 promote Spt5 CTR-independent recruitment of Paf1 complex. Embo J 31: 3494-3505.
31. Mayekar MK, Gardner RG, Arndt KM, (2013) The recruitment of the Saccharomyces cerevisiae Paf1 complex to active genes requires a domain of Rtf1 that directly interacts with the Spt4-Spt5 complex. Mol Cell Biol 33: 3259-3273.
32. Nordick K, Hoffman MG, Betz JL, Jaehning JA, (2008) Direct interactions between the Paf1 complex and a cleavage and polyadenylation factor are revealed by dissociation of Paf1 from RNA polymerase II. Eukaryot Cell 7: 1158-1167.
33. Adelman K, Wei W, Ardehali MB, Werner J, Zhu B, et al. (2006) Drosophila Paf1 modulates chromatin structure at actively transcribed genes. Mol Cell Biol 26: 250-260.
34. Langenbacher AD, Nguyen CT, Cavanaugh AM, Huang J, Lu F, et al. (2011) The PAF1 complex differentially regulates cardiomyocyte specification. Dev Biol 353: 19-28.
35. Rozenblatt-Rosen O, Hughes CM, Nannepaga SJ, Shanmugam KS, Copeland TD, et al. (2005) The parafibromin tumor suppressor protein is part of a human Paf1 complex. Mol Cell Biol 25: 612-620.
36. Krogan NJ, Kim M, Ahn SH, Zhong G, Kobor MS, et al. (2002) RNA polymerase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol Cell Biol 22: 6979-6992.
37. Mueller CL, Jaehning JA, (2002) Ctr9, Rtf1, and Leo1 are components of the Paf1/RNA polymerase II complex. Mol Cell Biol 22: 1971-1980.
38. Akanuma T, Koshida S, Kawamura A, Kishimoto Y, Takada S, (2007) Paf1 complex homologues are required for Notch-regulated transcription during somite segmentation. EMBO Rep 8: 858-863.
39. Bai X, Kim J, Yang Z, Jurynec MJ, Akie TE, et al. (2010) TIF1gamma controls erythroid cell fate by regulating transcription elongation. Cell 142: 133-143.
40. He Y, Doyle MR, Amasino RM, (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18: 2774-2784.
41. Ding L, Paszkowski-Rogacz M, Nitzsche A, Slabicki MM, Heninger AK, et al. (2009) A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell 4: 403-415.
42. Betz JL, Chang M, Washburn TM, Porter SE, Mueller CL, et al. (2002) Phenotypic analysis of Paf1/RNA polymerase II complex mutations reveals connections to cell cycle regulation, protein synthesis, and lipid and nucleic acid metabolism. Mol Genet Genomics 268: 272-285.
43. Chu Y, Simic R, Warner MH, Arndt KM, Prelich G, (2007) Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. Embo J 26: 4646-4656.
44. Keogh MC, Kurdistani SK, Morris SA, Ahn SH, Podolny V, et al. (2005) Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
45. Lenstra TL, Benschop JJ, Kim T, Schulze JM, Brabers NA, et al. (2011) The specificity and topology of chromatin interaction pathways in yeast. Mol Cell 42: 536-549.
46. Piro AS, Mayekar MK, Warner MH, Davis CP, Arndt KM, (2012) Small region of Rtf1 protein can substitute for complete Paf1 complex in facilitating global histone H2B ubiquitylation in yeast. Proc Natl Acad Sci U S A 109: 10837-10842.
47. Eydmann T, Sommariva E, Inagawa T, Mian S, Klar AJ, et al. (2008) Rtf1-mediated eukaryotic site-specific replication termination. Genetics 180: 27-39.
48. Racine A, Page V, Nagy S, Grabowski D, Tanny JC, (2012) Histone H2B ubiquitylation promotes activity of the intact Set1 histone methyltransferase complex in fission yeast. J Biol Chem 287: 19040-19047.
49. Tanny JC, Erdjument-Bromage H, Tempst P, Allis CD, (2007) Ubiquitylation of histone H2B controls RNA polymerase II transcription elongation independently of histone H3 methylation. Genes Dev 21: 835-847.
50. Chandrasekharan MB, Huang F, Sun ZW, (2010) Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. Epigenetics 5: 460-468.
51. St Amour CV, Sanso M, Bosken CA, Lee KM, Larochelle S, et al. (2012) Separate domains of fission yeast Cdk9 (P-TEFb) are required for capping enzyme recruitment and primed (Ser7-phosphorylated) CTD substrate recognition. Mol Cell Biol 32: 2372-2383.
52. Phatnani HP, Jones JC, Greenleaf AL, (2004) Expanding the functional repertoire of CTD kinase I and RNA polymerase II: novel phosphoCTD-associating proteins in the yeast proteome. Biochemistry 43: 15702-15719.
53. Schwer B, Shuman S, (2011) Deciphering the RNA polymerase II CTD code in fission yeast. Mol Cell 43: 311-318.
54. Wier AD, Mayekar MK, Heroux A, Arndt KM, Vandemark AP, (2013) Structural basis for Spt5-mediated recruitment of the Paf1 complex to chromatin. Proc Natl Acad Sci U S A 110: 17290-17295.
55. Warner MH, Roinick KL, Arndt KM, (2007) Rtf1 is a multifunctional component of the Paf1 complex that regulates gene expression by directing cotranscriptional histone modification. Mol Cell Biol 27: 6103-6115.
56. Mueller CL, Porter SE, Hoffman MG, Jaehning JA, (2004) The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol Cell 14: 447-456.
57. Lindstrom DL, Hartzog GA, (2001) Genetic interactions of Spt4-Spt5 and TFIIS with the RNA polymerase II CTD and CTD modifying enzymes in Saccharomyces cerevisiae. Genetics 159: 487-497.
58. Fleming AB, Kao CF, Hillyer C, Pikaart M, Osley MA, (2008) H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol Cell 31: 57-66.
59. Chandrasekharan MB, Huang F, Sun ZW, (2009) Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc Natl Acad Sci U S A 106: 16686-16691.
60. Batta K, Zhang Z, Yen K, Goffman DB, Pugh BF, (2011) Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev 25: 2254-2265.
61. Weinberger L, Voichek Y, Tirosh I, Hornung G, Amit I, et al. (2012) Expression Noise and Acetylation Profiles Distinguish HDAC Functions. Mol Cell 47: 193-202.
62. Shema E, Kim J, Roeder RG, Oren M, (2011) RNF20 Inhibits TFIIS-Facilitated Transcriptional Elongation to Suppress Pro-oncogenic Gene Expression. Mol Cell 42: 477-488.
63. Fujinaga K, Irwin D, Huang Y, Taube R, Kurosu T, et al. (2004) Dynamics of human immunodeficiency virus transcription: P-TEFb phosphorylates RD and dissociates negative effectors from the transactivation response element. Mol Cell Biol 24: 787-795.
64. Tasto JJ, Carnahan RH, McDonald WH, Gould KL, (2001) Vectors and gene targeting modules for tandem affinity purification in Schizosaccharomyces pombe. Yeast 18: 657-662.
65. Moreno S, Klar A, Nurse P, (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol 194: 795-823.
66. Guiguen A, Soutourina J, Dewez M, Tafforeau L, Dieu M, 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.