Fcp1 dephosphorylation of the RNA Polymerase II C-terminal domain is required for efficient transcription of heat shock genes

Molecular and Cellular Biology

Volumn 32, Issue 17, 2012, Pages 3428-3437

  Fuda, Nicholas J ^a   Buckley, Martin S ^a   Wei, Wenxiang ^b,c   Core, Leighton J ^a   Waters, Colin T ^a   Reinberg, Danny ^b   Lis, John T ^a  

^a Department of Obstetrics Gynecology   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FCP1; HEAT SHOCK PROTEIN 26; HEAT SHOCK PROTEIN 70; MESSENGER RNA; PHOSPHATASE; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; DROSOPHILA; GENE LOCATION; GENETIC TRANSCRIPTION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE;

ANIMALS; CELL LINE; DROSOPHILA; DROSOPHILA PROTEINS; GENE DELETION; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HSP70 HEAT-SHOCK PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; RNA POLYMERASE II; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION;

EID: 84866176227     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00247-12     Document Type: Article

References (48)

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. Ardehali MB, et al. 2009. Spt6 enhances the elongation rate of RNA polymerase II in vivo. EMBO J. 28:1067-1077.
3. Aygün O, Svejstrup J, Liu Y. 2008. A RECQ5-RNA polymerase II association identified by targeted proteomic analysis of human chromatin. Proc. Natl. Acad. Sci. U. S. A. 105:8580-8584.
4. Bartkowiak B, et al. 2010. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev. 24:2303-2316.
5. Buratowski S. 2005. Connections between mRNA 3= end processing and transcription termination. Curr. Opin. Cell Biol. 17:257-261.
6. Calvo O, Manley JL. 2005. The transcriptional coactivator PC4/Sub1 has multiple functions in RNA polymerase II transcription. EMBO J. 24: 1009-1020.
7. Chambers RS, Wang BQ, Burton ZF, Dahmus ME. 1995. The activity of COOH-terminal domain phosphatase is regulated by a docking site on RNA polymerase II and by the general transcription factors IIF and IIB. J. Biol. Chem. 270:14962-14969.
8. Chapman RD, et al. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318:1780-1782.
9. Chesnut JD, Stephens JH, Dahmus ME. 1992. The interaction of RNA polymerase I1 with the adenovirus-2 major of the C-terminal late promoter is precluded by phosphorylation domain of subunit IIa. J. Biol. Chem. 267:10500-10506.
10. 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.
11. Cho H, et al. 1999. A protein phosphatase functions to recycle RNA polymerase II. Genes Dev. 13:1540-1552.
12. Core LJ, Lis JT. 2008. Transcription regulation through promoterproximal pausing of RNA polymerase II. Science 319:1791-1792.
13. Egloff S, Murphy S. 2008. Cracking the RNA polymerase II CTD code. Trends Genet. 24:280-288.
14. Fabrega C, Shen V, Shuman S, Lima CD. 2003. Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II. Mol. Cell 11:1549-1561.
15. Ghosh A, Shuman S, Lima CD. 2011. Structural insights to how mammalian capping enzyme reads the CTD code. Mol. Cell 43:299-310.
16. Gilmour DS, Lis JT. 1985. In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol. Cell. Biol. 5:2009-2018.
17. Harlow E, Lane D. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, NY.
18. Hausmann S, Koiwa H, Krishnamurthy S, Hampsey M, Shuman S. 2005. Different strategies for carboxyl-terminal domain (CTD) recognition by serine 5-specific CTD phosphatases. J. Biol. Chem. 280:37681-37688.
19. Hausmann S, Shuman S. 2002. Characterization of the CTD phosphatase Fcp1 from fission yeast. Preferential dephosphorylation of serine 2 versus serine 5. J. Biol. Chem. 277:21213-21220.
20. Kamenski T, Heilmeier S, Meinhart A, Cramer P. 2004. Structure and mechanism of RNA polymerase II CTD phosphatases. Mol. Cell 15:399-407.
21. Kang ME, Dahmus ME. 1993. RNA polymerases IIA and IIO have distinct roles during transcription from the TATA-less murine dihydrofolate reductase promoter. J. Biol. Chem. 268:25033-25040.
22. Kimura M, Suzuki H, Ishihama A. 2002. Formation of a carboxyterminal domain phosphatase (Fcp1)/TFIIF/RNA polymerase II (pol II) complex in Schizosaccharomyces pombe involves direct interaction between Fcp1 and the Rpb4 Subunit of pol II. Mol. Cell. Biol. 22:1577-1588.
23. Kobor MS, et al. 1999. An unusual eukaryotic protein phosphatase required for transcription by RNA polymerase II and CTD dephosphorylation in S. cerevisiae. Mol. Cell 4:55-62.
24. Kong SE, et al. 2005. Interaction of Fcp1 phosphatase with elongating RNA polymerase II holoenzyme, enzymatic mechanism of action, and genetic interaction with elongator. J. Biol. Chem. 280:4299-4306.
25. Krishnamurthy S, He X, Reyes-Reyes M, Moore C, Hampsey M. 2004. Ssu72 Is an RNA polymerase II CTD phosphatase. Mol. Cell 14:387-394.
26. Laybourn PJ, Dahmus ME. 1990. Phosphorylation of RNA polymerase IIA occurs subsequent to interaction with the promoter and before the initiation of transcription. J. Biol. Chem. 265:13165-13173.
27. Licatalosi DD, et al. 2002. Functional interaction of yeast pre-mRNA 3= end processing factors with RNA polymerase II. Mol. Cell 9:1101-1111.
28. Lin PS, Dubois M-F, Dahmus ME. 2002. TFIIF-associating carboxylterminal domain phosphatase dephosphorylates phosphoserines 2 and 5 of RNA polymerase II. J. Biol. Chem. 277:45949-45956.
29. Lis J. 1998. Promoter-associated pausing in promoter architecture and postinitiation transcriptional regulation. Cold Spring Harbor Symp. Quant. Biol. 63:347-356.
30. Liu J, et al. 2011. Solution structure of tandem SH2 domains from Spt6 protein and their binding to the phosphorylated RNA polymerase II Cterminal domain. J. Biol. Chem. 286:29218-29226.
31. Lu H, Flores O, Weinmann R, Reinberg D. 1991. The nonphosphorylated form of RNA polymerase II preferentially associates with the preinitiation complex. Proc. Natl. Acad. Sci. U. S. A. 88:10004-10008.
32. Marshall NF, Peng J, Xie Z, Price DH, Chem JB. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal Domain kinase. J. Biol. Chem. 271:27176-27183.
33. Meinhart A, Cramer P. 2004. Recognition of RNA polymerase II carboxy-terminal domain by 3=-RNA-processing factors. Nature 430:223-226.
34. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P. 2005. A structural perspective of CTD function. Genes Dev. 19:1401-1415.
35. Morris DP, and a Greenleaf L. 2000. The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem. 275:39935-39943.
36. Mosley AL, et al. 2009. 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.
37. Ni Z, et al. 2008. P-TEFb is critical for the maturation of RNA polymerase II into productive elongation in vivo. Mol. Cell. Biol. 28:1161-1170.
38. O'Connor D, Lis JT. 1981. Two closely linked transcription units within the 63B heat shock puff locus of D. melanogaster display strikingly different regulation. Nucleic Acids Res. 9:5075-5092.
39. Payne JM, Laybourn PJ, Dahmus ME. 1989. The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxyl-terminal domain of subunit IIa. J. Biol. Chem. 264: 19621-19629.
40. Reyes-Reyes M, Hampsey M. 2007. Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation. Mol. Cell. Biol. 27:926-936.
41. Saunders A, Core LJ, Lis JT. 2006. Breaking barriers to transcription elongation. Nat. Rev. Mol. Cell Biol. 7:557-567.
42. Schwartz BE, Werner JK, Lis JT. 2004. Indirect immunofluorescent labeling of Drosophila polytene chromosomes: visualizing protein interactions with chromatin in vivo. Methods Enzymol. 376:393-404.
43. Suh M-H, et al. 2005. Fcp1 directly recognizes the C-terminal domain (CTD) and interacts with a site on RNA polymerase II distinct from the CTD. Proc. Natl. Acad. Sci. U. S. A. 102:17314-17319.
44. Tietjen JR, et al. 2010. Chemical-genomic dissection of the CTD code. Nat. Struct. Mol. Biol. 17:1154-1161.
45. Tombácz I, Schauer T, Juhász I, Komonyi O, Boros I. 2009. The RNA Pol II CTD phosphatase Fcp1 is essential for normal development in Drosophila melanogaster. Gene 446:58-67.
46. Watanabe Y, et al. 2000. Modulation of TFIIH-associated kinase activity by complex formation and its relationship with CTD phosphorylation of RNA polymerase II. Genes Cells 5:407-423.
47. Yeo M, Lin PS, Dahmus ME, Gill GN. 2003. A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine J. Biol. Chem. 278:26078-26085.
48. Zobeck KL, Buckley MS, Zipfel WR, Lis JT. 2010. Recruitment timing and dynamics of transcription factors at the Hsp70 loci in living cells. Mol. Cell 40:965-975.