Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation

Molecular and Cellular Biology

Volumn 27, Issue 3, 2007, Pages 926-936

  Reyes Reyes, Mariela ^a,b   Hampsey, Michael ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b ADVAXIS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 METHYLGUANOSINE; FUNGAL PROTEIN; HEPTAPEPTIDE; ISOENZYME; MESSENGER RNA PRECURSOR; MUTANT PROTEIN; PHOSPHATASE; PROTEIN SPT4; PROTEIN SPT5; PROTEIN SSU72 2; RNA POLYMERASE II; SERINE; TRANSCRIPTION FACTOR; TYROSYLSERYLPROLYLTHREONYLSERYLPROLYLSERINE; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBUNIT; FUNGAL GENE; FUNGUS MUTANT; GENE DELETION; GENE IDENTIFICATION; GENE MUTATION; GENE REPRESSION; GENETIC TRANSCRIPTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA CAPPING; RPB1 GENE; RPB2 GENE; SPT4 GENE; SPT5 GENE; SSU72 2 GENE;

ALANINE; ALLELES; AMINO ACID SEQUENCE; ARGININE; CARRIER PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA, FUNGAL; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA; SUPPRESSION, GENETIC; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS;

EID: 33846611494     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01361-06     Document Type: Article

References (72)

1. Ansari, A., and M. Hampsey. 2005. A role for the CPF 3′-end processing machinery in RNAP II-dependent gene looping. Genes Dev. 19:2969-2978.
2. Bentley, D. 2002. The mRNA assembly line: transcription and processing machines in the same factory. Curr. Opin. Cell Biol. 14:336-342.
3. Berroteran, R. W., D. E. Ware, and M. Hampsey. 1994. The sua8 suppressors of Saccharomyces cerevisiae encode replacements of conserved residues within the largest subunit of RNA polymerase II and affect transcription start site selection similarly to sua7 (TFIIB) mutations. Mol. Cell. Biol. 14:226-237.
4. Boeke, J. D., F. Lacroute, and G. R. Fink. 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345-346.
5. Buratowski, S. 2005. Connections between mRNA 3′ end processing and transcription termination. Curr. Opin. Cell Biol. 17:257-261.
6. Chen, B. S., S. S. Mandal, and M. Hampsey. 2004. High-resolution protein-DNA contacts for the yeast RNA polymerase II general transcription machinery. Biochemistry 43:12741-12749.
7. Cho, E. J., M. S. Kobor, M. Kim, J. Greenblatt, and S. Buratowski. 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. Cho, E. J., T. Takagi, C. R. Moore, and S. Buratowski. 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 11:3319-3326.
9. Cho, H., T. K. Kim, H. Mancebo, W. S. Lane, O. Flores, and D. Reinberg. 1999. A protein phosphatase functions to recycle RNA polymerase II. Genes Dev. 13:1540-1552.
10. Costa, P. J., and K. M. Arndt. 2000. Synthetic lethal interactions suggest a role for the Saccharomyces cerevisiae Rtf1 protein in transcription elongation. Genetics 156:535-547.
11. Cramer, P., D. A. Bushnell, and R. D. Kornberg. 2001. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292:1863-1876.
12. Dichtl, B., D. Blank, M. Ohnacker, A. Friedlein, D. Reeder, H. Langen, and W. Keller. 2002. A role for SSU72 in balancing RNA polymerase II transcription elongation and termination. Mol. Cell 10:1139-1150.
13. Exinger, F., and F. Lacroute. 1992. 6-Azauracil inhibition of GTP biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 22:9-11.
14. Ganem, C., F. Devaux, C. Torchet, C. Jacq, S. Quevillon-Cheruel, G. Labesse, C. Facca, and G. Faye. 2003. Ssu72 is a phosphatase essential for transcription termination of snoRNAs and specific mRNAs in yeast. EMBO J. 22:1588-1598.
15. Ganem, C., C. Miled, C. Facca, J. G. Valay, G. Labesse, S. Ben Hassine, C. Mann, and G. Faye. 2006. Kinase Cak1 functionally interacts with the PAF1 complex and phosphatase Ssu72 via kinases Ctk1 and Bur1. Mol. Genet. Genomics 275:136-147.
16. Gavin, A. C., M. Bosche, R. Krause, P. Grandi, M. Marzioch, A. Bauer, J. Schultz, J. M. Rick, A. M. Michon, C. M. Crucial, M. Remor, C. Hofert, M. Schelder, M. Brajenovic, H. Ruffner, A. Merino, K. Klein, M. Hudak, D. Dickson, T. Rudi, V. Gnau, A. Bauch, S. Bastuck, B. Huhse, C. Leutwein, M. A. Heurtier, R. R. Copley, A. Edelmann, E. Querfurth, V. Rybin, G. Drewes, M. Raida, T. Bouwmeester, P. Bork, B. Seraphin, B. Kuster, G. Neubauer, and G. Superti-Furga. 2002. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415:141-147.
17. Gietz, D., A. St. John, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
18. Gong, X. Q., C. Zhang, M. Feig, and Z. F. Burton. 2005. Dynamic error correction and regulation of downstream bubble opening by human RNA polymerase II. Mol. Cell 18:461-470.
19. Hahn, S. 2004. Structure and mechanism of the RNA polymerase II transcription machinery. Nat. Struct. Mol. Biol. 11:394-403.
20. Hartzog, G. A., T. Wada, H. Handa, and F. Winston. 1998. Evidence that Spt4, Spt5, and Spt6 control transcription elongation by RNA polymerase II in Saccharomyces cerevisiae. Genes Dev. 12:357-369.
21. Hausmann, S., H. Erdjument-Bromage, and S. Shuman. 2004. Schizosaccharomyces pombe carboxyl-terminal domain (CTD) phosphatase Fcp1: distributive mechanism, minimal CTD substrate, and active site mapping. J. Biol. Chem. 279:10892-10900.
22. Hausmann, S., H. Koiwa, S. Krishnamurthy, M. Hampsey, and S. Shuman. 2005. Different strategies for carboxyl-terminal domain (CTD) recognition by serine 5-specific CTD phosphatases. J. Biol. Chem. 280:37681-37688.
23. Hausmann, S., and S. Shuman. 2002. Characterization of the CTD phosphatase Fcp1 from fission yeast. Preferential dephosphorylation of serine 2 versus serine 5. J. Biol. Chem. 277:21213-21220.
24. He, X., A. U. Khan, H. Cheng, D. L. Pappas, Jr., M. Hampsey, and C. L. Moore. 2003. Functional interactions between the transcription and mRNA 3′ end processing machineries mediated by Ssu72 and Sub1. Genes Dev. 17:1030-1042.
25. Hirose, Y., and J. L. Manley. 2000. RNA polymerase II and the integration of nuclear events. Genes Dev. 14:1415-1429.
26. Kim, M., S. H. Ahn, N. J. Krogan, J. F. Greenblatt, and S. Buratowski. 2004. Transitions in RNA polymerase II elongation complexes at the 3′ ends of genes. EMBO J. 23:354-364.
27. Kobor, M. S., and J. Greenblatt. 2002. Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577:261-275.
28. Koiwa, H., A. W. Barb, L. Xiong, F. Li, M. G. McCully, B. H. Lee, I. Sokolchik, J. Zhu, Z. Gong, M. Reddy, A. Sharkhuu, Y. Manabe, S. Yokoi, J. K. Zhu, R. A. Bressan, and P. M. Hasegawa. 2002. C-terminal domain phosphatase-like family members (AtCPLs) differentially regulate Arabidopsis thaliana abiotic stress signaling, growth, and development. Proc. Natl. Acad. Sci. USA 99:10893-10898.
29. Koiwa, H., R. A. Bressan, and P. M. Hasegawa. 2006. Identification of plant stress-responsive determinants in Arabidopsis by large-scale forward genetic screens. J. Exp. Bot. 57:1119-1128.
30. Koiwa, H., S. Hausmann, W. Y. Bang, A. Ueda, N. Kondo, A. Hiraguri, T. Fukuhara, J. D. Bahk, D. J. Yun, R. A. Bressan, P. M. Hasegawa, and S. Shuman. 2004. Arabidopsis C-terminal domain phosphatase-like 1 and 2 are essential Ser-5-specific C-terminal domain phosphatases. Proc. Natl. Acad. Sci. USA 101:14539-14544.
31. Komarnitsky, P., E. J. Cho, and S. Buratowski. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14:2452-2460.
32. Krishnamurthy, S., X. He, M. Reyes-Reyes, C. Moore, and M. Hampsey. 2004. Ssu72 Is an RNA polymerase II CTD phosphatase. Mol. Cell 14:387-394.
33. Lee, J. M., and A. L. Greenleaf. 1997. Modulation of RNA polymerase II elongation efficiency by C-terminal heptapeptide repeat domain kinase I. J. Biol. Chem. 272:10990-10993.
34. Lindstrom, D. L., and G. A. Hartzog. 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.
35. Lindstrom, D. L., S. L. Squazzo, N. Muster, T. A. Burckin, K. C. Wachter, C. A. Emigh, J. A. McCleery, J. R. Yates III, and G. A. Hartzog. 2003. Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol. Cell. Biol. 23:1368-1378.
36. Liu, Y., C. Kung, J. Fishburn, A. Z. Ansari, K. M. Shokat, and S. Hahn. 2004. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol. Cell. Biol. 24:1721-1735.
37. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
38. Mandal, S. S., H. Cho, S. Kim, K. Cabane, and D. Reinberg. 2002. FCP1, a phosphatase specific for the heptapeptide repeat of the largest subunit of RNA polymerase II, stimulates transcription elongation. Mol. Cell. Biol. 22:7543-7552.
39. Mason, P. B., and K. Struhl. 2005. Distinction and relationship between elongation rate and processivity of RNA polymerase II in vivo. Mol. Cell. 17:831-840.
40. McCracken, S., N. Fong, E. Rosonina, K. Yankulov, G. Brothers, D. Siderovski, A. Hessel, S. Foster, A. E. Program, S. Shuman, and D. L. Bentley. 1997. 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev. 11:3306-3318.
41. Meinhart, A., T. Kamenski, S. Hoeppner, S. Baumli, and P. Cramer. 2005. A structural perspective of CTD function. Genes Dev. 19:1401-1415.
42. Morillon, A., N. Karabetsou, J. O'Sullivan, N. Kent, N. Proudfoot, and J. Mellor. 2003. Isw1 chromatin remodeling ATPase coordinates transcription elongation and termination by RNA polymerase II. Cell 115:425-435.
43. Myers, L. C., L. Lacomis, H. Erdjument-Bromage, and P. Tempst. 2002. The yeast capping enzyme represses RNA polymerase II transcription. Mol. Cell 10:883-894.
44. Nedea, E., X. He, M. Kim, J. Pootoolal, G. Zhong, V. Canadien, T. Hughes, S. Buratowski, C. L. Moore, and J. Greenblatt. 2003. Organization and function of APT, a subcomplex of the yeast cleavage and polyadenylation factor involved in the formation of mRNA and small nucleolar RNA 3′-ends. J. Biol. Chem. 278:33000-33010.
45. Orphanides, G., and D. Reinberg. 2002. A unified theory of gene expression. Cell 108:439-451.
46. O'Sullivan, J. M., S. M. Tan-Wong, A. Morillon, B. Lee, J. Coles, J. Mellor, and N. J. Proudfoot. 2004. Gene loops juxtapose promoters and terminators in yeast. Nat. Genet. 36:1014-1018.
47. Pappas, D. L., Jr., and M. Hampsey. 2000. Functional interaction between Ssu72 and the Rpb2 subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell. Biol. 20:8343-8351.
48. Patturajan, M., N. K. Conrad, D. B. Bregman, and J. L. Corden. 1999. Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation. J. Biol. Chem. 274:27823-27828.
49. Patturajan, M., R. J. Schulte, B. M. Sefton, R. Berezney, M. Vincent, O. Bensaude, S. L. Warren, and J. L. Corden. 1998. Growth-related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273:4689- 4694.
50. Pokholok, D. K., N. M. Hannett, and R. A. Young. 2002. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol. Cell 9:799-809.
51. Powell, W., and D. Reines. 1996. Mutations in the second largest subunit of RNA polymerase II cause 6-azauracil sensitivity in yeast and increased transcriptional arrest in vitro. J. Biol. Chem. 271:6866-6873.
52. Prelich, G. 2002. RNA polymerase II carboxy-terminal domain kinases: emerging clues to their function. Eukaryot. Cell 1:153-162.
53. Proudfoot, N. J., A. Purger, and M. J. Dye. 2002. Integrating mRNA processing with transcription. Cell 108:501-512.
54. Qiu, H., C. Hu, C. M. Wong, and A. G. Hinnebusch. 2006. The Spt4p subunit of yeast DSIF stimulates association of the Paf1 complex with elongating RNA polymerase II. Mol. Cell. Biol. 26:3135-3148.
55. Rodriguez, C. R., E. J. Cho, M. C. Keogh, C. L. Moore, A. L. Greenleaf, and S. Buratowski. 2000. Kin28, the TFIIH-associated carboxy-terminal domain kinase, facilitates the recruitment of mRNA processing machinery to RNA polymerase II. Mol. Cell. Biol. 20:104-112.
56. Rondon, A. G., M. Garcia-Rubio, S. Gonzalez-Barrera, and A. Aguilera. 2003. Molecular evidence for a positive role of Spt4 in transcription elongation. EMBO J. 22:612-620.
57. Rothstein, R. 1991. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194:281-301.
58. Sanders, S. L., J. Jennings, A. Canutescu, A. J. Link, and P. A. Weil. 2002. Proteomics of the eukaryotic transcription machinery: identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry. Mol. Cell. Biol. 22:4723-4738.
59. Scafe, C., C. Martin, M. Nonet, S. Podos, S. Okamura, and R. A. Young. 1990. Conditional mutations occur predominantly in highly conserved residues of RNA polymerase II subunits. Mol. Cell. Biol. 10:1270-1275.
60. Schroeder, S. C., B. Schwer, S. Shuman, and D. Bentley. 2000. Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14:2435-2440.
61. Schroeder, S. C., D. A. Zorio, B. Schwer, S. Shuman, and D. Bentley. 2004. A function of yeast mRNA cap methyltransferase, Abd1, in transcription by RNA polymerase II. Mol. Cell 13:377-387.
62. Shaw, R. J., and D. Reines. 2000. Saccharomyces cerevisiae transcription elongation mutants are defective in PUR5 induction in response to nucleotide depletion. Mol. Cell. Biol. 20:7427-7437.
63. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
64. Sherman, F., and J. Hicks. 1991. Micromanipulation and dissection of asci. Methods Enzymol. 194:21-37.
65. Sims, R. J., III, R. Belotserkovskaya, and D. Reinberg. 2004. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 18:2437-2468.
66. Steinmetz, E. J., and D. A. Brow. 2003. Ssu72 protein mediates both poly(A)-coupled and poly(A)-independent termination of RNA polymerase II transcription. Mol. Cell. Biol. 23:6339-6349.
67. St-Pierre, B., X. Liu, L. C. Kha, X. Zhu, O. Ryan, Z. Jiang, and E. Zacksenhaus. 2005. Conserved and specific functions of mammalian ssu72. Nucleic Acids Res. 33:464-477.
68. Sun, Z.-W., and M. Hampsey. 1996. Synthetic enhancement of a TFIIB defect by a mutation in SSU72, an essential gene encoding a novel protein that affects transcription start site selection in vivo. Mol. Cell. Biol. 16:1557-1566.
69. Wood, A., J. Schneider, J. Dover, M. Johnston, and A. Shilatifard. 2005. The Bur1/Bur2 complex is required for histone H2B monoubiquitination by Rad6/Bre1 and histone methylation by COMPASS. Mol. Cell 20:589-599.
70. Wu, W.-H., I. Pinto, B.-S. Chen, and M. Hampsey. 1999. Mutational analysis of yeast TFIIB: a functional relationship between Ssu72 and Sub1/Tsp1 defined by allele-specific interactions with TFIIB. Genetics 153:643-652.
71. Yeo, M., P. S. Lin, M. E. Dahmus, and G. N. Gill. 2003. A novel RNA polymeras II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J. Biol. Chem. 278:26078-26085.
72. Yue, Z., E. Maldonado, R. Pillutla, H. Cho, D. Reinberg, and A. J. Shatkin. 1997. 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 94:12898-12903.