Investigating RNA polymerase II carboxyl-terminal domain (CTD) phosphorylation

European Journal of Biochemistry

Volumn 270, Issue 19, 2003, Pages 3859-3870

  Palancade, Benoît ^a   Bensaude, Olivier ^a  

^a ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

CTD kinase; CTD phosphatase; CTD phosphorylation; mRNA processing; RNA polymerase II; Transcription

Indexed keywords

RNA POLYMERASE II;

CARBOXY TERMINAL SEQUENCE; CHROMATIN; EXPERIMENT; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VIVO STUDY; MOLECULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; RNA PROCESSING; TRANSCRIPTION INITIATION;

AMINO ACID SEQUENCE; CHROMATIN; EPITOPES; ISOENZYMES; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SERINE; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0141815505     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03794.x     Document Type: Review

References (156)

1. Corden, J.L. (1993) RNA polymerase II transcription cycles. Curr. Opin. Genet. Dev. 3, 213-218.
2. Meininghaus, M., Chapman, R.D. & Eick, D. (2000) Conditional expression of RNA polylmerase II in mammalian cells. Deletion of the carboxy-terminal domain of the large subunit affects early steps in transcription. J. Biol. Chem. 275, 24375-24382.
3. Meisels, E., Gileadis, O. & Corden, J.L. (1995) Partial truncation of the yeast RNA polymerase II carboxy-terminal domain preferentially reduces expression of glycolytic genes. J. Biol. Chem. 270, 31255-31261.
4. Scafe, C., Chao, D., Lopes, J., Hirsch, J.P., Henry, S. & Young, R.A. (1990) RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals. Nature 347, 491-494.
5. Gerber, H.P., Hagmann, M., Seipel, K., Georgiev, O., West, M.A.L., Litingung, Y., Schaffner, W. & Corden, J.L. (1995) RNA polymerase II C-terminal domain required for enhancer-driven transcription. Nature 374, 660-662.
6. Misteli, T. (2000) Cell biology of transcription and pre-mRNA splicing: nuclear architecture meets nuclear function. J. Cell Sci. 113, 1841-1849.
7. Proudfoot, N.J., Furger, A. & Dye, M.J. (2002) Integrating mRNA processing with transcription. Cell 108, 501-512.
8. Howe, K.J. (2002) RNA polymerase II conducts a symphony of pre-mRNA processing activities. Biochim. Biophys. Acta 1577, 308-324.
9. Corden, J.L. (1990) Tails of RNA polymerase II. Trends Biochem. Sci. 15, 383-387.
10. Corden, J.L. & Ingles, C.J. (1992) Carboxy-terminal domain of the largest subunit of RNA polymerase II. In Transcriptional Regulation (McKnight, S.L. & Yamamoto, K.R., eds), pp. 81-128, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
11. Bensaude, O., Bonnet, F., Cassé, C., Dubois, M.-F., Nguyen, V.-T. & Palancade, B. (1999) Regulated phosphorylation of the RNA polymerase II C-terminal domain (CTD). Biochem. Cell Biol. 77, 1-7.
12. Kelly, W.G., Dahmus, M.E. & Hart, G.W. (1993) RNA polymerase II is a glycoprotein: modification of the COOH-terminal domain by O-GlcNAc. J. Biol. Chem. 268, 10416-10424.
13. Dahmus, M.E. (1996) Reversible phosphorylation of the C-terminal domain of RNA polymerase II. J. Biol. Chem. 271, 19009-19012.
14. Riedl, T. & Egly, J.M. (2000) Phosphorylation in transcription: the CTD and more. Gene Expr. 9, 3-13.
15. Oelgeschlager, T. (2002) Regulation of RNA polymerase II activity by CTD phosphorylation and cell cycle control. J. Cell Physiol. 190, 160-169.
16. Kobor, M.S. & Greenblatt, J. (2002) Regulation of transcription elongation by phosphorylation. Biochim. Biophys. Acta 1577, 261-275.
17. Majello, B. & Napolitano, G. (2001) Control of RNA polymerase II activity by dedicated CTD kinases and phosphatases. Front. Biosci. 6, D1358-D1368.
18. Prelich, G. (2002) RNA polymerase II carboxy-terminal domain kinases: emerging clues to their function. Eukaryot. Cell. 1, 153-162.
19. Bentley, D. (2002) The mRNA assembly line: transcription and processing machines in the same factory. Curr. Opin. Cell Biol. 14, 336-342.
20. Schwartz, L.B. & 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.
21. Baskaran, R., Dahmus, M.E. & Wang, J.Y.J. (1993) Tyrosine phosphorylation of mammalian RNA polymerase II carboxyl-terminal domain. Proc. Natl Acad. Sci. USA 90, 11167-11171.
22. Zhang, J. & Corden, J.L. (1991) Identification of phosphorylation sites in the repetitive CTD of the mouse RNA polymerase II largest subunit. J. Biol. Chem. 266, 2290-2296.
23. A. J. Biol. Chem. 258, 2303-2307.
24. Payne, J.M. & Dahmus, M.E. (1993) Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxy-terminal domain of RNA polymerase subunit IIa. J. Biol. Chem. 268, 80-87.
25. Jenkins, H.L. & Spencer, C.A. (2001) RNA polymerase II holoenzyme modifications accompany transcription reprogramming in herpes simplex virus type 1-infected cells. J. Virol. 75, 9872-9884.
26. Rice, S.A., Long, M.C., Lam, V. & Spencer, C.A. (1994) RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following Herpes Simplex virus infection. J. Virol. 68, 988-1001.
27. Bonnet, F., Vigneron, M., Bensaude, O. & Dubois, M.-F. (1999) Transcription-independent phosphorylation of the RNA polymerase II carboxy-terminal domain (CTD) recquiring ERK kinase activity. Nucleic Acids Res. 27, 4399-4404.
28. Palancade, B., Bellier, S., Almouzni, G. & Bensaude, O. (2001) Incomplete RNA polymerase II phosphorylation in Xenopus laevis early embryos. J. Cell Sci. 114, 2483-2489.
29. Bellier, S., Chastant, S., Adenot, P., Vincent, M., Renard, J.-P. & Bensaude, O. (1997) Nuclear translocation and carboxyl-terminal domain phosphorylation of RNA polymerase II delineate the two phases of zygotic gene activation in mammalian embryos. EMBO J. 16, 6250-6262.
30. Leclerc, V., Raisin, S. & Leopold, P. (2000) Dominant-negative mutants reveal a role for the Cdk7 kinase at the mid-blastula transition in Drosophila embryos. EMBO J. 19, 1567-1575.
31. Patturajan, M., Schulte, R.J., Sefton, B.M., Berezney, R., Vincent, M., Bensaude, O., Warren, S.L. & Corden, J.L. (1998) Growth-related changes in phosphorylation of yeast RNA polymerase II. J. Biol. Chem. 273, 4689-4694.
32. Kobor, M.S., Archambault, J., Lester, W., Holstege, F.C., Gileadi, O., Jansma, D.B., Jennings, E.G., Kouyoumdjian, F., Davidson, A.R., Young, R.A. & Greenblatt, J. (1999) An unusual eukaryotic protein phosphatase required for transcription by RNA polymerase II and CTD dephosphorylation in S. cerevisiae. Mol. Cell. 4, 55-62.
33. Valay, J.-G., Simon, M., Dubois, M.-F., Bensaude, O., Facca, C. & Faye, G. (1995) The KIN28 gene is required both for RNA polymerase II mediated transcription and phosphorylation of the Rpb1p CTD. J. Mol. Biol. 249, 535-544.
34. Cho, E.J., Kobor, M.S., Kim, M., Greenblatt, J. & Buratowski, S. (2001) Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser2 of the RNA polymerase II C-terminal domain. Genes Dev. 15, 3319-3329.
35. Doyle, O., Corden, J.L., Murphy, C. & Gall, J.G. (2002) The distribution of RNA polymerase II largest subunit (RPB1) in the Xenopus germinal vesicle. J. Struct. Biol. 140, 154-166.
36. Lavoie, S.B., Albert, A.L., Handa, H., Vincent, M. & Bensaude, O. (2001) The peptidyl-prolyl isomerase Pin1 interacts with hSpt5 phosphorylated by Cdk9. J. Mol. Biol. 312, 675-685.
37. Albert, A., Lavoie, S. & Vincent, M. (1999) A hyperphosphorylated form of RNA polymerase II is the major interphase antigen of the phosphoprotein antibody MPM-2 and interacts with the peptidyl-prolyl isomerase Pin1. J. Cell Sci. 112, 2493-2500.
38. Ramanathan, Y., Rajpara, S.M., Reza, S.M., Lees, E., Shuman, S., Mathews, M.B. & Pe'ery, T. (2001) Three RNA polymerase II carboxyl-terminal domain kinases display distinct substrate preferences. J. Biol. Chem. 276, 10913-10920.
39. Trigon, S., Serizawa, H., Conaway, J.W., Conaway, R.C., Jackson, S.P. & Morange, M. (1998) Characterization of the residues phosphorylated in vitro by different C-terminal domain kinases. J. Biol. Chem. 273, 6769-6775.
40. Roy, R., Adamczewski, J.P., Seroz, T., Vermeulen, W., Tassan, J.-P., Schaeffer, L., Nigg, E.A., Hoeijmakers, J.H.J. & Egly, J.-M. (1994) The MO15 cell cycle kinase is associated with the TFIIH transcription-DNA repair factor. Cell 79, 1093-1101.
41. Gebara, M.M., Sayre, M.H. & Corden, J.L. (1997) Phosphorylation of the carboxy-terminal repeat domain in RNA polymerase II by cyclin-dependent kinases is sufficient to inhibit transcription. J. Cell Biochem. 64, 390-402.
42. Hengartner, C.J., Myer, V.E., Liao, S.M., Wilson, C.J., Koh, S.S. & Young, R.A. (1998) Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol. Cell. 2, 43-53.
43. Rickert, P., Corden, J.L. & Lees, E. (1999) Cyclin C/CDK8 and cyclin H/CDK7/p36 are biochemically distinct CTD kinases. Oncogene 18, 1093-1102.
44. Deng, L., Ammosova, T., Pumfery, A., Kashanchi, F. & Nekhai, S. (2002) HIV-1 Tat interaction with RNA polymerase II CTD and a dynamic association with CDK2 induce CTD phosphorylation and transcription from HIV-1 promoter. J. Biol. Chem. 277, 33922-33929.
45. Dubois, M.-F., Vincent, M., Adamczewski, J., Egly, J.M. & Bensaude, O. (1997) Heat shock inactivation of the TFIIH-associated kinase and change in the phosphorylation sites on RNA polymerase II largest subunit. Nucleic Acids Res. 25, 694-700.
46. Sun, X., Zhang, Y., Cho, H., Rickert, P., Lees, E., Lane, W. & Reinberg, D. (1998) NAT, a human complex containing Srb polypeptides that functions as a negative regulator of activated transcription. Mol. Cell. 2, 213-222.
47. Zhou, M., Nekhai, S., Bharucha, D.C., Kumar, A., Ge, H., Price, D.H., Egly, J.M. & Brady, J.N. (2001) TFIIH inhibits CDK9 phosphorylation during human immunodeficiency virus type 1 transcription. J. Biol. Chem. 276, 44633-44640.
48. Yamamoto, S., Watanabe, Y., van der Spek, P.J., Watanabe, T., Fujimoto, H., Hanaoka, F. & Ohkuma, Y. (2001) Studies of nematode TFIIE function reveal a link between Ser-5 phosphorylation of RNA polymerase II and the transition from transcription initiation to elongation. Mol. Cell Biol. 21, 1-15.
49. Kim, Y.K., Bourgeois, C.F., Isel, C., Churcher, M.J. & Karn, J. (2002) Phosphorylation of the RNA polymerase II carboxyl-terminal domain by CDK9 is directly responsible for human immunodeficiency virus type 1 Tat-activated transcriptional elongation. Mol. Cell Biol. 22, 4622-4637.
50. Zhou, M., Halanski, M.A., Radonovich, M.F., Kashanki, F., Peng, J., Price, D.H. & Brady, J.N. (2000) Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxy-terminal domain during immunodeficiency virus type 1 transcription. Mol. Cell Biol. 20, 5077-5086.
51. Rossignol, M., Kolb-Cheynel, I. & Egly, J.-M. (1997) Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH. EMBO J. 16, 1628-1637.
52. Mancebo, H.S., Lee, G., Flygare, J., Tomassini, J., Luu, P., Zhu, Y., Peng, J., Blau, C., Hazuda, D., Price, D. & Flores, O. (1997) P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev. 11, 2633-2644.
53. Cujec, T., Okamoto, H., Fujinaga, K., Meyer, J., Chamberlin, H., Morgan, D.O. & Peterlin, B.M. (1997) The HIV transactivator TAT binds to the CDK-activating kinase and activates the phosphorylation of the carboxy-terminal domain of RNA polymerase II. Genes Dev. 11, 2645-2657.
54. Kanazawa, S., Okamoto, T. & Peterlin, B.M. (2000) Tat competes with CIITA for the binding to P-TEFb and blocks the expression of MHC class II genes in HIV infection. Immunity 12, 61-70.
55. Lee, D.K., Duan, H.O. & Chang, C. (2001) Androgen receptor interacts with the positive elongation factor P-TEFb and enhances the efficiency of transcriptional elongation. J. Biol. Chem. 276, 9978-9984.
56. Eberhardy, S.R. & Farnham, P.J. (2001) c-Myc mediates activation of the cad promoter via a post-RNA polymerase II recruitment mechanism. J. Biol. Chem. 276, 48562-48571.
57. Barboric, M., Nissen, R.M., Kanazawa, S., Jabrane-Ferrat, N. & Peterlin, B.M. (2001) NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell. 8, 327-337.
58. Nissen, R.M. & Yamamoto, K.R. (2000) The glucocorticoid receptor inhibits NFkB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 14, 2314-2329.
59. Lin, P.S., Marshall, N.F. & Dahmus, M.E. (2002) CTD phosphatase: role in RNA polymerase II cycling and the regulation of transcript elongation. Prog. Nucleic Acid Res. Mol. Biol. 72, 333-365.
60. Yeo, M., Lin, P.S., Dahmus, M.E. & Gill, G.N. (2003) A novel RNA polymerase II C-terminal domain phosphatase that preferentially dephosphorylates serine 5. J. Biol. Chem. 278, 26078-26085.
61. Bharucha, D.C., Zhou, M., Nekhai, S., Brady, J.N., Shukla, R.R. & Kumar, A. (2002) A protein phosphatase from human T cells augments tat transactivation of the human immunodeficiency virus type 1 long-terminal repeat. Virology 296, 6-16.
62. Washington, K., Ammosova, T., Beullens, M., Jerebtsova, M., Kumar, A., Bollen, M. & Nekhai, S. (2002) Protein phosphatase-1 dephosphorylates the C-terminal domain of RNA polymerase-II. J. Biol. Chem. 15, 15.
63. Ganem, C., Devaux, F., Torchet, C., Jacq, C., Quevillon-Cheruel, S., Labesse, G., Facca, C. & Faye, G. (2003) Ssu72 is a phosphatase essential for transcription termination of snoRNAs and specific mRNAs in yeast. EMBO J. 22, 1-11.
64. Meinhart, A., Silberzahn, T. & Cramer, P. (2003) The mRNA transcription/processing factor Ssu72 is a potential tyrosine phosphatase. J. Biol. Chem. 18, 15917-15921.
65. Cho, H., Kim, T.K., Mancebo, H., Lane, W.S., Flores, O. & Reinberg, D. (1999) A protein phosphatase functions to recycle RNA polymerase II. Genes Dev. 13, 1540-1552.
66. Lin, P.S., Dubois, M.-F. & Dahmus, M.E. (2002) TFIIF-associating carboxyl-terminal domain phosphatase dephosphorylates phosphoserines 2 and 5 of RNA polymerase II. J. Biol. Chem. 277, 45949-45956.
67. Cadena, D.L. & 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.
68. Payne, J.M., Laybourn, P.J. & 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.
69. 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. USA 88, 10004-10008.
70. Chesnut, J.D., Stephens, J.H. & Dahmus, M.E. (1992) The interaction of RNA polymerase II with the adenovirus-2 major late promoter precluded by phosphorylation of the C-terminal domain of subunit IIa. J. Biol. Chem. 267, 10500-10506.
71. Lehman, A.L. & Dahmus, M.E. (2000) The sensitivity of RNA polymerase II in elongation complexes to C-terminal domain phosphatase. J. Biol. Chem. 275, 14923-14932.
72. Marshall, N.F. & Dahmus, M.E. (2000) C-terminal domain phosphatase sensitivity of RNA polymerase II in early elongation complexes on the HIV-1 and adenovirus 2 major late templates. J. Biol. Chem. 275, 32430-32437.
73. O'Brien, T., Hardin, S., Greenleaf, A. & Lis, J.T. (1994) Phosphorylation of RNA polymerase II C-terminal domain and transcriptional elongation. Nature 370, 75-77.
74. Cheng, C. & Sharp, P.A. (2003) RNA polymerase II accumulation in the promoter-proximal region of the dihydrofolate reductase and gamma-actin genes. Mol. Cell Biol. 23, 1961-1967.
75. Komarnitsky, P., Cho, E.J. & Buratowski, S. (2000) Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev. 14, 2452-2460.
76. Schroeder, S.C., Schwer, B., Shuman, S. & Bentley, D. (2000) Dynamic association of capping enzymes with transcribing RNA polymerase II. Genes Dev. 14, 2435-2440.
77. West, M.L. & Corden, J.L. (1995) Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics 140, 1223-1233.
78. Yuryev, A. & Corden, J.L. (1996) Suppression analysis reveals a functional difference between the serines in positions two and five in the consensus sequence of the C-terminal domain of yeast RNA polymerase II. Genetics 143, 661-671.
79. Carty, S.M. & Greenleaf, A.L. (2002) Hyperphosphorylated C-terminal repeat domain-associating proteins in the nuclear proteome link transcription to DNA/chromatin modification and RNA processing. Mol. Cell Proteomics 1, 598-610.
80. Ho, C.K. & Shuman, S. (1999) Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian capping enzyme. Mol. Cell 3, 405-411.
81. 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.
82. Takagi, T., Walker, A.K., Sawa, C., Diehn, F., Takase, Y., Blackwell, T.K. & Buratowski, S. (2003) The Caenorhabditis elegans mRNA 5′-capping enzyme: in vitro and in vivo characterization. J. Biol. Chem. 278, 14174-14184.
83. Greenleaf, A.L. (1993) A positive addition to a negative tail's tale. Proc. Natl Acad. Sci. USA 90, 10896-10897.
84. Patturajan, M., Wei, X., Berezney, R. & Corden, J.L. (1998) A nuclear matrix protein interacts with the phosphorylated C-terminal domain of RNA polymerase II. Mol. Cell Biol. 18, 2406-2415.
85. Kim, E.L., Bregman, D.B. & Warren, S.L. (1997) Splicing factors associate with hyperphosphorylated RNA polymerase II in the absence of pre-mRNA. J. Cell Biol. 136, 19-28.
86. McCracken, S., Fong, N., Yankulov, K., Ballantyne, S., Pan, G., Greenblatt, J., Patterson, S.D., Wickens, M. & Bentley, D.L. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385, 357-361.
87. Skaar, D.A. & Greenleaf, A.L. (2002) The RNA polymerase II CTD kinase CTDK-I affects pre-mRNA-3′ cleavage/polyadenylation through the processing component Pti1p. Mol. Cell 10, 1429-1439.
88. Licatalosi, D.D., Geiger, G., Miner, M., Schroeder, S., Cilli, K., McNeil, J.B. & Bentley, D.L. (2002) Functional interactions of yeast pre-mRNA-3′ end processing factors with RNA polymerase II. Mol. Cell 9, 1101-1111.
89. Ryan, K., Murthy, K.G., Kaneko, S. & Manley, J.L. (2002) Requirements of the RNA polymerase II C-terminal domain for reconstituting pre-mRNA-3′ cleavage. Mol. Cell Biol. 22, 1684-1692.
90. Fong, N. & 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.
91. Hampsey, M. & Reinberg, D. (2003) Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 113, 429-432.
92. Ng, H.H., Robert, F., Young, R.A. & Struhl, K. (2003) Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell. 11, 709-719.
93. Krogan, N.J., Dover, J., Wod, A., Schneider, J., Heidt, J., Boateng, M.A., Dean, K., Ryan, O.W., Golshani, A., Johnston, M., Greenblatt, J.F. & Shilatifard, A. (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.
94. Li, J., Moazed, D. & Gygi, S.P. (2002) Association of the histone methyltransferase Set2 with RNA polymerase II plays a role in transcription elongation. J. Biol. Chem. 277, 49383-49388.
95. Xiao, T., Hall, H., Kizer, K.O., Shibata, Y., Hall, M.C., Borchers, C.H. & Strahl, B.D. (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17, 654-663.
96. Venetianer, A., Dubois, M.-F., Nguyen, V.T., Seo, S.J., Bellier, S. & Bensaude, O. (1995) Phosphorylation state of RNA polymerase II C-terminal domain (CTD) in heat-shocked cells: possible involvement of the stress activated MAP kinases. Eur. J. Biochem. 233, 83-92.
97. Dubois, M.F., Nguyen, V.T., Bellier, S. & Bensaude, O. (1994) Inhibitors of transcription such as 5,6-dichloro-1-β-D-ribofuranosyl benzimidazole (DRB) and isoquinoline sulfonamide derivatives (H-8 and H-7*), promote the dephosphorylation of the C-terminal domain (CTD) of RNA polymerase II largest subunit. J. Biol. Chem. 269, 13331-13336.
98. Palancade, B., Dubois, M.F., Dahmus, M.E. & Bensaude, O. (2001) Transcription-independent RNA polymerase II dephosphorylation by the FCP1 CTD-phosphatase in Xenopus laevis early embryos. Mol. Cell Biol. 21, 6359-6368.
99. Bellier, S., Dubois, M.-F., Nishida, E., Almouzni, G. & Bensaude, O. (1997) Phosphorylation of RNA polymerase II largest subunit during Xenopus laevis oocyte maturation. Mol. Cell Biol. 17, 1434-1440.
100. Valay, J.G., Dubois, M.-F., Bensaude, O. & Faye, G. (1996) Cc11, a cyclin associated with protein kinase Kin28 controls the phosphorylation of RNA polymerase II largest subunit and mRNA transcription. C.R. Acad Sci. Paris 319, 183-190.
101. Cassé, C., Giannoni, F., Nguyen, V.T., Dubois, M.-F. & Bensaude, O. (1999) The transcriptional inhibitors, actinomycin D and α-amanitin, activate the HIV-1 promoter and favor phosphorylation of the RNA polymerase II C-terminal domain. J. Biol. Chem. 274, 16097-16106.
102. Nguyen, V.T., Giannoni, F., Dubois, M.-F., Seo, S.-J., Vigneron, M., Kédinger, C. & Bensaude, O. (1996) In vivo degradation of RNA polymerase II largest subunit triggered by α-amanitin. Nucleic Acids Res. 24, 2924-2929.
103. Bregman, D.B., Halaban, R., Van Gool, A.J., Henning, K.A., Friedberg, E.C. & Warren, S.L. (1996) UV-induced ubiquitination of RNA polymerase II: a novel modification deficient in Cockayne syndrome cells. Proc. Natl Acad. Sci. USA 93, 11586-11590.
104. Nguyen, V.T., Kiss, T., Michels, A.A. & Bensaude, O. (2001) 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature 414, 322-325.
105. Yang, Z., Zhu, Q., Luo, K. & Zhou, Q. (2001) The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 414, 317-322.
106. Ostapenko, D. & Solomon, M.J. (2003) Budding yeast CTDK-I is required for DNA damage-induced transcription. Eukaryot. Cell 2, 274-283.
107. Akoulitchev, S., Chuikov, S. & Reinberg, D. (2000) TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 407, 102-106.
108. Weeks, J.R., Hardin, S.E., Shen, J., Lee, J.M. & Greenleaf, A. (1993) Locus-specific variation in phosphorylation state of RNA polymerase II in vivo: correlations with gene activity and transcript processing. Genes Dev. 7, 2329-2344.
109. Zeng, C., Kim, E., Warren, S.L. & Berget, S.M. (1997) Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 16, 1401-1412.
110. Bregman, D.B.L., van der Zee, S. & Warren, S.L. (1995) Transcription-dependent redistribution of the large subunit of RNA polymerase II to discrete nuclear domains. J. Cell Biol. 129, 287-298.
111. Prasanth, K.V., Sacco-Bubulya, P.A., Prasanth, S.G. & Spector, D.L. (2003) Sequential entry of components of gene expression machinery into daughter nuclei. Mol. Biol. Cell 14, 1043-1057.
112. Seydoux, G. & Dunn, M.A. (1997) Transcriptionally-repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of C. elegans and D. melanogaster. Development 124, 2191-2201.
113. Knaut, H., Pelegri, F.K.B., Schwarz, H. & Nusslein-Volhard, C. (2000) Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol. 149, 875-888.
114. Tenenhaus, C., Schubert, C. & Seydoux, G. (1998) Genetic requirements for PIE-1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans. Dev. Biol. 200, 212-224.
115. Shim, E.Y., Walker, A.K., Shi, Y. & Blackwell, T.K. (2002) CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16, 2135-2146.
116. Dantonel, J.C., Quintin, S., Lakatos, L., Labouesse, M. & Tora, L. (2000) TBP-like factor is required for embryonic RNA polymerase II transcription in C. elegans. Mol. Cell 6, 715-722.
117. Kaltenbach, L., Horner, M.A., Rothman, J.H., Mango, S.E. & Sharp, P.A. (2000) The TBP-like factor CeTLF is required to activate RNA polymerase II transcription during C. elegans embryogenesis. Mol. Cell 6, 705-713.
118. Wallenfang, M.R. & Seydoux, G. (2002) cdk-7 is required for mRNA transcription and cell cycle progression in Caenorhabditis elegans embryos. Proc. Natl Acad. Sci. USA 99, 5527-5532.
119. Shim, E.Y., Walker, A.K. & Blackwell, T.K. (2002) Broad requirement for the mediator subunit RGR-1 for transcription in the C. elegans embryo. J. Biol. Chem. 277, 30413-30416.
120. Walker, A.K., Rothman, J.H., Shi, Y. & Blackwell, T.K. (2001) Distinct requirements for C.elegans TAFIIs in early embryonic transcription. EMBO J. 20, 5269-5279.
121. Muller, F., Lakatos, L., Dantonel, J., Strahle, U. & Tora, L. (2001) TBP is not universally required for zygotic RNA polymerase II transcription in zebrafish. Curr. Biol. 11, 282-287.
122. Rossi, D.J., Londesborough, A., Korsisaari, N., Pihlak, A., Lehtonen, E., Henkemeyer, M. & Makela, T.P. (2001) Inability to enter S phase and defective RNA polymerase II CTD phosphorylation in mice lacking Mat1. EMBO J. 20, 2844-2856.
123. Thompson, N.E., Steinberg, T.H., Aronson, D.B. & 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.
124. Mortillaro, M.J., Blencowe, B.J., Wei, X., Du Nakayasu, H.L., Warren, S.L., Sharp, P.A. & Berezney, R. (1996) A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl Acad. Sci. USA 93, 8253-8257.
125. Vincent, M., Lauriault, P., Dubois, M.-F., Lavoie, S., Bensaude, O. & Chabot, B. (1996) The nuclear matrix protein p255 is a highly phosphorylated form of RNA polymerase II largest subunit which associates with the spliceosome. Nucleic Acids Res. 24, 4649-4652.
126. Michels, A.A., Nguyen, V.T., Fraldi, A., Labas, V., Edwards, M., Bonnet, F., Lania, L. & Bensaude, O. (2003) MAQ1 ('ménage à quatre') and 7SK RNA interact with CDK9/CyclinT complexes in a transcription-dependent manner. Mol. Cell Biol. 23, 4859-4869.
127. Cisek, L.J. & Corden, J.L. (1989) Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2. Nature 339, 679-684.
128. Nigg, E.A. (1995) Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays. 17, 471-480.
129. Zhao, J., Dynlacht, B., Imai, T., Hori, T. & Harlow, E. (1998) Expression of NPAT, a novel substrate of cyclin E-CDK2, promotes S-phase entry. Genes Dev. 12, 456-461.
130. Svejstrup, J.Q., Vichi, P. & Egly, J.-M. (1996) The multiple roles of transcription/repair factor TFIIH. Trends Biochem. Sci. 21, 346-350.
131. Fisher, R.P. & Morgan, D.O. (1994) A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 78, 713-724.
132. Ko, L.J., Shieh, S.Y., Chen, X., Jayaraman, L., Tamai, K., Taya, Y., Prives, C. & Pan, Z.Q. (1997) p53 is phosphorylated by CDK7-cyclin H in a p36-MAT1 dependent manner. Mol. Cell Biol. 17, 7220-7229.
133. Ohkuma, Y. & Roeder, R.G. (1994) Regulation of TFIIH ATPase and kinase activities by TFIIE during active initiation complex formation. Nature 368, 160-163.
134. Liao, S.-M., Zhang, J., Jeffery, D.A., Koleske, A.J., Thompson, C.M., Chao, D.M., Viljoen, M., van Vuuren, H.J.J. & Young, R.A. (1995) A kinase-cyclin pair in the RNA polymerase II holoenzyme. Nature 374, 193-196.
135. Leclerc, V., Tassan, J.P., O'Farrell, P.H., Nigg, E.A. & Léopold, P. (1996) Drosophila cdk8, a kinase partner of cyclin C that interacts with the large subunit of RNA polymerase II. Mol. Biol. Cell 7, 505-513.
136. Rickert, P., Seghezzi, W., Shanahan, F., Cho, H. & Lees, E. (1996) Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II. Oncogene 12, 2631-2640.
137. Chi, Y., Huddleston, M.J., Zhang, X., Young, R.A., Annan, R.S., Carr, S.A. & Deshaies, R.J. (2001) Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15, 1078-1092.
138. Hirst, M., Kobor, M.S., Kuriakose, N., Greenblatt, J. & Sadowski, I. (1999) GAL4 is regulated by the RNA polymerase II holoenzyme-associated cyclin-dependent kinase SRB10/CDK8. Mol. Cell 3, 673-678.
139. Zhu, Y., Pe'ery, T., Peng, J., Ramanathan, Y., Marshall, N., Marshall, T., Amendt, B., Mathews, M.B. & Price, D.H. (1997) Transcription elongation factor P-TEFb is required for HIV-1 Tat transactivation in vitro. Genes Dev. 11, 2622-2632.
140. Price, D.H. (2000) P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II. Mol. Cell Biol. 20, 2629-2634.
141. Ramanathan, Y., Reza, S.M., Young, T.M., Mathews, M.B. & Pe'ery, T. (1999) Human and rodent transcription elongation factor P-TEFb: interactions with human immunodeficiency virus type 1 Tat and carboxy-terminal domain substrate. J. Virol. 73, 5448-5458.
142. Kim, J.B. & Sharp, P.A. (2001) Positive transcription elongation factor b phosphorylates hSPT5 and RNA polymerase II carboxy-terminal domain independently of cyclin-dependent kinase activating kinase. J. Biol. Chem. 276, 12317-12323.
143. Simone, C., Bagella, L., Bellan, C. & Giordano, A. (2002) Physical interaction between pRb and cdk9/cyclin T2 complex. Oncogene 21, 4158-4165.
144. Simone, C., Stiegler, P., Bagella, L., Pucci, B., Bellan, C., De Falco, G., De Luca, A., Guanti, G., Puri, P.L. & Giordano, A. (2002) Activation of MyoD-dependent transcription by CDK9/cyclin T2. Oncogene 21, 4137-4148.
145. Lee, J.M. & Greenleaf, A.L. (1989) A protein kinase that phosphorylates the C-terminal repeat domain of the largest subunit of RNA polymerase II. Proc. Natl Acad. Sci. USA 86, 3624-3628.
146. Sterner, D.E., Lee, J.M., Hardin, S.E. & Greenleaf, A.L. (1995) The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol. Cell Biol. 15, 5716-5724.
147. Patturajan, M., Conrad, N.K., Bregman, D.B. & Corden, J.L. (1999) Yeast carboxyl-terminal domain kinase I positively and negatively regulates RNA polymerase II carboxyl-terminal domain phosphorylation. J. Biol. Chem. 274, 27823-27828.
148. 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.
149. Dubois, M.-F., Nguyen, V.T., Dahmus, M.E., Pagès, G., Pouysségur, J. & 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.
150. Treisman, R. (1996) Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8, 205-215.
151. Dvir, A., Peterson, S.R., Knuth, M.W., Lu, H. & Dynan, W.S. (1992) Ku antigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc. Natl Acad. Sci. USA 89, 11920-11924.
152. Smith, G.C. & Jackson, S.P. (1999) The DNA-dependent protein kinase. Genes Dev. 13, 916-934.
153. Van Etten, R.A. (1999) Cycling, stressed-out and nervous: cellular functions of c-ab1. Trends Cell Biol. 9, 179-186.
154. Zohn, I.E. & Brivanlou, A.H. (2001) Expression cloning of Xenopus Os4, an evolutionarily conserved gene, which induces mesoderm and dorsal axis. Dev. Biol. 239, 118-131.
155. Bollen, M. & Beullens, M. (2002) Signaling by protein phosphatases in the nucleus. Trends Cell Biol. 12, 138-145.
156. Keriel, A., Stary, A., Sarasin, A., Rochette-Egly, C. & Egly, J.M. (2002) XPD mutations prevent TFIH-dependent transactivation by nuclear receptors and phosphorylation of RARα. Cell 109, 125-135.