The last CTD repeat of the mammalian RNA polymerase II large subunit is important for its stability

Nucleic Acids Research

Volumn 32, Issue 1, 2004, Pages 35-44

  Chapman, Rob D ^b   Palancade, Benoit ^a,c   Lang, Andreas ^b   Bensaude, Olivier ^a   Eick, Dirk ^b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; POL PROTEIN; PROTEIN SUBUNIT; RNA POLYMERASE II; PEPTIDE FRAGMENT;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME STABILITY; GENE DISRUPTION; GENETIC TRANSCRIPTION; HELA CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MAMMAL CELL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION; AMINO ACID SEQUENCE; CELL SURVIVAL; CHEMISTRY; GENE DELETION; GENE EXPRESSION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

MAMMALIA;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CELL SURVIVAL; ENZYME STABILITY; GENE EXPRESSION; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; POINT MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; REPETITIVE SEQUENCES, AMINO ACID; RNA POLYMERASE II; SEQUENCE DELETION; TRANSCRIPTION, GENETIC;

EID: 1242309371     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh172     Document Type: Article

References (76)

1. Corden,J.L., Cadena,D.L., Ahearn,J.M.,Jr and Dahmus,M.E. (1985) A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II. Proc. Natl Acad. Sci. USA, 82, 7934-7939.
2. Stiller,J.W. and Hall,B.D. (2002) Evolution of the RNA polymerase II C-terminal domain. Proc. Natl Acad. Sci. USA, 99, 6091-6096.
3. Fong,N. and Bentley,D.L. (2001) Capping, splicing and 3′ processing are independently stimulated by RNA polymerase II: different functions for different segments of the CTD. Genes Dev., 15, 1783-1795.
4. Allison,L.A., Wong,J.K., Fitzpatrick,V.D., Moyle,M. and Ingles,C.J. (1988) The C-terminal domain of the largest subunit of RNA polymerase II of Saccharomyces cerevisiae, Drosophila melanogaster and mammals: a conserved structure with an essential function. Mol. Cell. Biol., 8, 321-329.
5. Pinna,L.A. (1990) Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim. Biophys. Acta, 1054, 267-284.
6. Baskaran,R., Escobar,S.R. and Wang,J.Y. (1999) Nuclear c-Abl is a COOH-terminal repeated domain (CTD)-tyrosine (CTD)-tyrosine kinase-specific for the mammalian RNA polymerase II: possible role in transcription elongation. Cell Growth Differ., 10, 387-396.
7. Baskaran,R., Chiang,G.G., Mysliwiec,T., Kruh,G.D. and Wang,J.Y. (1997) Tyrosine phosphorylation of RNA polymerase II carboxyl-terminal domain by the Abl-related gene product. J. Biol. Chem., 272, 18905-18909.
8. Litingtung,Y., Lawler,A.M., Sebald,S.M., Lee,E., Gearhart,J.D., Westphal,H. and Corden,J.L. (1999) Growth retardation and neonatal lethality in mice with a homozygous deletion in the C-terminal domain of RNA polymerase II. Mol. Gen. Genet., 261, 100-105.
9. Meininghaus,M. and Eick,D. (1999) Requirement of the carboxy-terminal domain of RNA polymerase II for the transcriptional activation of chromosomal c-fos and hsp70A genes. FEBS Lett., 446, 173-176.
10. Meininghaus,M., Chapman,R.D., Horndasch,M. and Eick,D. (2000) Conditional expression of RNA polymerase II in mammalian cells. Deletion of the carboxyl-terminal domain of the large subunit affects early steps in transcription. J. Biol. Chem., 275, 24375-24382.
11. McCracken,S., Fong,N., Yankulov,K., Ballantyne,S., Pan,G., Greenblatt,J., Patterson,S.D., Wickens,M. and Bentley,D.L. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature, 385, 357-361.
12. Dahmus,M.E. (1996) Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem., 271, 19009-19012.
13. Palancade,B. and Bensaude,O. (2003) Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation. Eur. J. Biochem., 270, 1-12.
14. Cadena,D.L. and Dahmus,M.E. (1987) Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. J. Biol. Chem., 262, 12468-12474.
15. Payne,J.M., Laybourn,P.J. and Dahmus,M.E. (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.
16. Majello,B. and Napolitano,G. (2001) Control of RNA polymerase II activity by dedicated CTD kinases and phosphatases. Front. Biosci., 6, D1358-D1368.
17. Bregman,D.B., Pestell,R.G. and Kidd,V.J. (2000) Cell cycle regulation and RNA polymerase II. Front. Biosci. 5, D244-D257.
18. Kobor,M. and Greenblatt,J. (2002) Regulation of transcription elongation by phosphorylation Biochim. Biophys. Acta, 1577, 261.
19. Oelgeschlager,T. (2002) Regulation of RNA polymerase II activity by CTD phosphorylation and cell cycle control. J. Cell. Physiol., 190, 160-169.
20. Bonnet,F., Vigneron,M., Bensaude,O. and Dubois,M.F. (1999) Transcription-independent phosphorylation of the RNA polymerase II C-terminal domain (CTD) involves ERK kinases (MEK1/2). Nucleic Acids Res., 27, 4399-4404.
21. Dubois,M.F., Nguyen,V.T., Dahmus,M.E., Pages,G., Pouyssegur,J. and Bensaude,O. (1994) Enhanced phosphorylation of the C-terminal domain of RNA polymerase II upon serum stimulation of quiescent cells: possible involvement of MAP kinases. EMBO J., 13, 4787-4797.
22. Hengartner,C.J., Myer,V.E., Liao,S.M., Wilson,C.J., Koh,S.S. and Young,R.A. (1998) Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell, 2, 43-53.
23. Baskaran,R., Dahmus,M.E. and Wang,J.Y. (1993) Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc. Natl Acad. Sci. USA, 90, 11167-11171.
24. Zhang,J. and Corden,J.L. (1991) Identification of phosphorylation sites in the repetitive carboxyl-terminal domain of the mouse RNA polymerase II largest subunit. J. Biol. Chem., 266, 2290-2296.
25. Komarnitsky,P., Cho.E.J. and Buratowski,S. (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev., 14. 2452-2460.
26. Sudol,M., Sliwa,K. and Russo,T. (2001) Functions of WW domains in the nucleus. FEBS Lett., 490, 190-195.
27. Lu,P.J., Zhou,X.Z., Shen,M. and Lu,K.P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science, 283, 1325-1328.
28. Duyster,J., Baskaran,R. and Wang,J.Y. (1995) Src homology 2 domain as a specificity determinant in the c-Abl-mediated tyrosine phosphorylation of the RNA polymerase II carboxyl-terminal repeated domain. Proc. Natl Acad. Sci. USA, 92, 1555-1559.
29. Cho,E.J., Takagi,T., Moore,C.R. and Buratowski,S. (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.
30. Pei,Y., Hausmann,S., Ho,C.K., Schwer,B. and 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.
31. Morris,D.P. and Greenleaf,A.L. (2000) The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem., 275, 39935-39943.
32. Hirose,Y., Tacke,R. and Manley,J.L. (1999) Phosphorylated RNA polymerase II stimulates pre-mRNA splicing. Genes Dev., 13, 1234-1239.
33. Goldstrohm,A.C., Albrecht,T.R., Sune,C., Bedford,M.T. and Garcia-Blanco,M.A. (2001) The transcription elongation factor CA150 interacts with RNA polymerase II and the pre-mRNA splicing factor SF1. Mol. Cell. Biol., 21, 7617-7628.
34. Dichtl,B., Blank,D., Sadowski,M., Hubner,W., Weiser,S. and Keller,W. (2002) Yhh1p/Cft1p directly links poly(A) site recognition and RNA polymerase II transcription termination. EMBO J., 21, 4125-4135.
35. Licatalosi,D.D., Geiger,G., Minet,M., Schroeder,S., Cilli,K., McNeil,J.B. and Bentley,D.L. (2002) Functional interaction of yeast pre-mRNA 3′ end processing factors with RNA polymerase II. Mol. Cell, 9, 1101-1111.
36. Proudfoot,N.J., Furger,A. and Dye,M.J. (2002) Integrating mRNA processing with transcription, Cell, 108, 501-512.
37. Howe,K. (2002) RNA polymerase II conducts a symphony of pre-mRNA processing activities. Biochim. Biophys. Acta, 1577, 308.
38. Baskaran,R., Wood,L.D., Whitaker,L.L., Canman,C.E., Morgan,S.E., Xu,Y., Barlow,C., Baltimore,D., Wynshaw-Boris,A., Kastan,M.B. et al. (1997) Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature, 387, 516-519.
39. Perego,R., Ron,D. and Kruh,G.D. (1991) Arg encodes a widely expressed 145 kDa protein-tyrosine kinase. Oncogene, 6, 1899-1902.
40. Dahmus,M.E. (1981) Phosphorylation of eukaryotic DNA-dependent RNA polymerase. Identification of calf thymus RNA polymerase subunits phosphorylated by two purified protein kinases, correlation with in vivo sites of phosphorylation in HeLa cell RNA polymerase II. J. Biol. Chem., 256, 3332-3339.
41. Allendes,J.E. and Allende,C.C. (1995) Protein kinases. 4. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J., 9, 313-323.
42. Egyhazi,E., Ossoinak,A., Filhol-Cochet,O., Cochet,C. and Pigon,A. (1999) The binding of the alpha subunit of protein kinase CK2 and RAP74 subunit of TFIIF to protein-coding genes in living cells is DRB sensitive. Mol. Cell. Biochem., 191, 149-159.
43. Trembley,J.H., Hu,D., Slaughter,C.A., Lahti,J.M. and Kidd,V.J. (2003) Casein kinase 2 interacts with cyclin-dependent kinase II (CDKII) in vivo and phosphorylates both the RNA polymerase II carboxyl-terminal domain and CDKII in vitro. J. Biol. Chem., 278, 2265-2270.
44. Pulvertaft,R.J.V. (1964) Cytology of Burkitt's tumour (African lymphoma). Lancet, 1, 238-240.
45. Dignam,J.D., Lebovitz,R.M. and Roeder,R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11, 147-1489.
46. Palancade,B., Dubois,M.F. and Bersaude,O. (2002) FCP1 phosphorylation by casein kinase 2 enhances binding to TFIIF and RNA polymerase II carboxyl-terminal domain phosphatase activity. J. Biol. Chem., 277, 36061-36067.
47. Thompson,N.E., Steinberg,T.H., Aronson,D.B. and Burgess,R.R. (1989) Inhibition of in vivo and in vitro transcription by monoclonal antibodies prepared against wheat germ RNA polymerase II that react with the heptapeptide repeat of eukaryotic RNA polymerase II. J. Biol. Chem., 264, 11511-11520.
48. Kontermann,R.E., Liu,Z., Schulze,R.A., Sommer,K.A., Queitsch,I., Dubel,S., Kipriyanov,S.M., Breitling,F. and Bautz,E.K. (1995) Characterization of the epitope recognized by a monoclonal antibody directed against the largest subunit of Drosophila RNA polymerase II. Biol. Chem. Hoppe Seyler, 376, 473-481.
49. Peterson,S.R., Dvir,A., Anderson,C.W. and Dynan,W.S. (1992) DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev., 6, 426-438.
50. Gerber,H.P., Hagmann,M., Seipel,K., Georgiev,O., West,M.A., Litingtung,Y., Schaffner,W. and Corden,J.L. (1995) RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature, 374, 660-662.
51. Dahmus,M.E. (1983) Structural relationship between the large subunits of calf thymus RNA polymerase II. J. Biol. Chem., 258, 3956-3960.
52. Kim,W.Y. and Dahmus,M.E. (1986) Immunochemical analysis of mammalian RNA polymerase II subspecies. Stability and relative in vivo concentration. J. Biol. Chem., 261, 14219-14225.
53. Dahmus,M.E. (1981) Purification and properties of calf thymus casein kinases I and II. J. Biol. Chem., 256, 3319-3325.
54. Dahmus,G.K., Glover,C.V., Brutlag,D.L. and Dahmus,M.E. (1984) Similarities in structure and function of calf thymus and Drosophila casein kinase II. J. Biol. Chem., 259, 9001-9006.
55. Shafman,T., Khanna,K.K., Kedar,P., Spring,K., Kozlov,S., Yen,T., Hobson,K., Gatei,M., Zhang,N., Watters,D. et al. (1997) Interaction between ATM protein and c-Abl in response to DNA damage. Nature, 387, 520-523.
56. Kipreos,E.T. and Wang,J.Y. (1992) Cell cycle-regulated binding of c-Abl tyrosine kinase to DNA. Science, 256, 382-385.
57. Welch,P.J. and Wang,J.Y. (1993) A C-terminal protein-binding domain in the retinoblastoma protein regulates nuclear c-Abl tyrosine kinase in the cell cycle. Cell, 75, 779-790.
58. Yuan,Z.M., Shioya,H., Ishiko,T., Sun,X., Gu,J., Huang,Y.Y., Lu,H., Kharbanda,S., Weichselbaum,R. and Kufe,D. (1999) p73 is regulated by tyrosine kinase c-Abl in the apoptotic response to DNA damage. Nature, 399, 814-817.
59. Kharbanda,S., Pandey,P., Jin,S., Inoue,S., Bharti,A., Yuan,Z.M., Weichselbaum,R., Weaver,D. and Kufe,D. (1997) Functional interaction between DNA-PK and c-Abl in response to DNA damage. Nature, 386, 732-735.
60. Birchenall-Roberts,M.C., Yoo,Y.D., Bertolette,D.C., 3rd, Lee,K.H., Turley,J.M., Bang,O.S., Ruscetti,F.W. and Kim,S.J. (1997) The p120-v-Abl protein interacts with E2F-1 and regulates E2F-1 transcriptional activity. J. Biol. Chem., 272, 8905-8911.
61. Fong,N., Bird,G., Vigneron,M. and Bentley,D.L. (2003) A 10 residue motif at the C-terminus of the RNA pol II CTD is required for transcription, splicing and 3′ end processing. EMBO J., 22, 4274-4282.
62. Schwartz,L.B. and Roeder,R.G. (1975) Purification and subunit structure of deoxyribonucleic acid-dependent ribonucleic acid polymerase II from the mouse plasmacytoma. MOPC 315. J. Biol. Chem., 250, 3221-3228.
63. Dahmus,M.E. and Kedinger,C. (1993) Transcription of adenovirus-2 major late promoter inhibited by monoclonal antibody directed against RNA polymerases IIO and IIA. J. Biol. Chem., 258, 2303-2307.
64. Cramer,P., Bushnell,D.A., Fu,J., Gnatt,A.L., Maier-Davis,B., Thompson,N.E., Burgess,R.R., Edwards,A.M., David,P.R. and Kornberg,R.D. (2000) Architecture of RNA polymerase II and implications for the transcription mechanism. Science, 288, 640-649.
65. Zhang,F., Barboric,M., Blackwell,T.K. and Peterlin,B.M. (2003) A model of repression: CTD analogs and PIE-1 inhibit transcriptional elongation by P-TEFb. Genes Dev., 17, 748-758.
66. Wang,J.Y. (2000) Regulation of cell death by the Abl tyrosine kinase. Oncogene, 19, 5643-5650.
67. Wang,J.Y. and Ki,S.W. (2001) Choosing between growth arrest and apoptosis through the retinoblastoma tumour suppressor protein, Abl and p73. Biochem. Soc. Trans, 29, 666-673.
68. Cao,C., Ren,X., Kharbanda,S., Koleske,A., Prasad,K.V. and Kufe,D. (2001) The ARG tyrosine kinase interacts with Siva-1 in the apoptotic response to oxidative stress. J. Biol. Chem., 276, 11465-11468.
69. Misteli,T. and Spector,D.L. (1999) RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo. Mol. Cell, 3, 697-705.
70. Kleiman,F.E. and Manley,J.L. (2001) The BARD1-CstF-50 interaction links mRNA 3′ end formation to DNA damage and tumor suppression. Cell, 104, 743-753.
71. Citterio,E., Vermeulen,W. and Hoeijmakers,J.H. (2000) Transcriptional healing. Cell, 101, 447-450.
72. Ratner,J.N., Balasubramanian,B., Corden,J., Warren,S.L. and Bregman,D.B. (1998) Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II. Implications for transcription-coupled DNA repair. J. Biol. Chem., 273, 5184-5189.
73. Luo,Z., Zheng,J., Lu,Y. and Bregman,D.B. (2001) Ultraviolet radiation alters the phosphorylation of RNA polymerase II large subunit and accelerates its proteasome-dependent degradation. Mutat. Res., 486, 259-274.
74. Mitsui,A. and Sharp,P.A. (1999) Ubiquitination of RNA polymerase II large subunit signaled by phosphorylation of carboxyl-terminal domain. Proc. Natl Acad. Sci. USA, 96, 6054-6059.
75. Muratani,M. and Tansey,W.P. (2003) How the ubiquitin-proteasome system controls transcription. Nature Rev. Mol. Cell. Biol., 4, 192-201.
76. Chang,A., Cheang,S., Espanel,X. and Sudol,M. (2000) Rsp5 WW domains interact directly with the carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem., 275, 20562-20571.