Phosphorylation of the carboxy-terminal repeat domain in RNA polymerase II by cyclin-dependent kinases is sufficient to inhibit transcription

Journal of Cellular Biochemistry

Volumn 64, Issue 3, 1997, Pages 390-402

  Gebara, Maha M ^a   Sayre, Michael H ^b   Corden, Jeffry L ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c NONE   (United States)

Author keywords

carboxy terminal repeat domain (CTD); cyclin dependent kinases; phosphorylation; RNA polymerase II; transcription

Indexed keywords

CYCLIN DEPENDENT KINASE; RNA POLYMERASE II;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME PHOSPHORYLATION; ENZYME SPECIFICITY; MITOSIS; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

CYCLIN-DEPENDENT KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; PHOSPHORYLATION; REPETITIVE SEQUENCES, NUCLEIC ACID; RNA POLYMERASE II; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 0031035486     PISSN: 07302312     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4644(19970301)64:3<390::AID-JCB6>3.0.CO;2-Q     Document Type: Article

References (63)

1. Arias JA, Peterson SR, Dynan WS (1991): Promoter-dependent phosphorylation of RNA polymerase II by a template-bound kinase. Association with transcriptional initiation. J Biol Chem 266:8055-8061.
2. Bartholomew B, Dahmus ME, Meares CF (1986): RNA contacts subunits IIo and IIc in HeLa RNA polymerase II transcription complexes. J Biol Chem 261:14226-14231.
3. Baskaran R, Dahmus ME, Wang J (1993): Tyrosine phosphorylation of mammalian RNA polymerase-II carboxylterminal domain. Proc Natl Acad Sci U S A 90:11167-11171.
4. Bregman DB, Du L, van der Zee S, Warren SL (1995): Transcription-dependent redistribution of the largest subunit of RNA polymerase II to discrete nuclear domains. J Cell Biol 129:287-298.
5. Buratowski S, Sopta M, Greenblatt J, Sharp PA (1991): RNA polymerase II-associated proteins are required for a DNA conformation change in the transcription initiation complex. Proc Natl Acad Sci U S A 88:7509-7513.
6. Cadena DL, Dahmus ME (1987): Messenger RNAsynthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. J Biol Chem 262:12468-12474.
7. Chambers RS, Dahmus ME (1994): Purification and characterization of a phosphatase from HeLa cells which dephosphorylates the C-terminal domain of RNA polymerase II. J Biol Chem 269:26243-26248.
8. 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.
9. Chesnut JD, Stephens JH, Dahmus ME (1992): The interaction of RNA polymerase II with the adenovirus-2 major late promoter is precluded by phosphorylation of the C-terminal domain of subunit IIa. J Biol Chem 267: 10500-10506.
10. Cisek LJ, Corden JL (1989): Phosphorylation of RNA polymerase by the murine homologue of the cell-cycle control protein cdc2. Nature 339:679-684.
11. Cisek LJ, Corden JL (1991): Purification of protein kinases that phosphorylate the repetitive carboxyl-terminal domain of eukaryotic RNA polymerase II. Methods Enzymol 200:301-325.
12. Cismowski MJ, Laff GM, Solomon MJ, Reed SI (1995): Kin28 encodes a C-terminal domain kinase that controls mRNA transcription in Saccharomyces cerevisiae but lacks cyclin-dependent kinase-activating kinase (CAK) activity. Mol Cell Biol 15:2983-2992.
13. Conaway RC, Bradsher JN, Conaway JW (1992): Mechanism of assembly of the RNA polymerase II preinitiation complex. Evidence for a functional interaction between the carboxyl-terminal domain of the largest subunit of RNA polymerase II and a high molecular mass form of the TATA factor. J Biol Chem 267:8464-8467.
14. Conaway RC, Garrett KP, Hanley JP, Conaway JW (1991): Mechanism of promoter selection by RNA polymerase II: Mammalian transcription factors alpha and beta gamma promote entry of polymerase into the preinitiation complex. Proc Natl Acad Sci U S A 88:6205-6209.
15. Cottrelle P, Thiele D, Price VL, Memet S, Micouin JY, Marck C, Buhler JM, Sentenac A, Fromageot P (1985): Cloning, nucleotide sequence, and expression of one of two genes coding for yeast elongation factor 1 alpha. J Biol Chem 260:3090-3096.
16. Dahmus ME (1995): Phosphorylation of the C-terminal domain of RNA polymerase II. Biochim Biophys Acta 1261:171-182.
17. Desai D, Gu Y, Morgan DO (1992): Activation of human cyclin-dependent kinases in vitro. Mol Biol Cell 3:571-582.
18. Dubois MF, Nguyen VT, Dahmus ME, Pages G, Pouyssegur 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.
19. Feaver WJ, Gileadi O, Li Y, Kornberg RD (1991): CTD kinase associated with yeast RNA polymerase II initiation factor b. Cell 67:1223-1230.
20. Feaver WJ, Svejstrup JQ, Henry NL, Kornberg RD (1994): Relationship of Cdk-activating kinase and RNA polymerase II CTD Kinase TFIIH/TFIIK. Cell 79:1103-1109.
21. Fisher RP, Morgan DO (1994): A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 78:713-724.
22. Gottesfeld JM, Wolf VJ, Dang T, Forbes DJ, Hartl P (1994): Mitotic repression of RNA polymerase III transcription in vitro mediated by phosphorylation of a TFIIIB component. Science 263:81-84.
23. Guilfoyle TJ (1989): A protein kinase from wheat germ that phosphorylates the largest subunit of RNA polymerase II. Plant Cell 1:827-836.
24. Ha I, Roberts S, Maldonado E, Sun XQ, Kim LU, Green M, Reinberg D (1993): Multiple functional domains of human transcription factor-IIB - distinct interactions with two general transcription factors and RNA polymerase II. Genes Dev 7:1021-1032.
25. Kamps, MP, Sefton BM (1989): Acid and base hydrolysis of phosphoproteins bound to immobilon facilitates analysis of phosphoamino acids in gel-fractionated proteins. Anal Biochem 176:22-27.
26. 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.
27. Kim WY, Dahmus ME (1986): Immunochemical analysis of mammalian RNA polymerase II subspecies. Stability and relative in vivo concentration. J Biol Chem 261:14219-14225.
28. Laybourn PJ, Dahmus ME (1989): Transcription-dependent structural changes in the C-terminal domain of mammalian RNA polymerase subunit IIa/o. J Biol Chem 264:6693-6698.
29. 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.
30. Lee JM, Greenleaf AL (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.
31. Lee JM, Greenleaf AL (1991): CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr 1:149-167.
32. Legagneux V, Morange M, Bensaude O (1990): Heat-shock and related stress enhance RNA polymerase II C-terminal-domain kinase activity in HeLa cell extracts. Eur J Biochem 193:121-126.
33. Li Y, Kornberg RD (1994): Interplay of positive and negative effectors in function of the C-terminal repeat domain of RNA polymerase II. Proc Natl Acad Sci U S A 91:2362-2366.
34. Liao SM, Taylor IC, Kingston RE, Young RA (1991): RNA polymerase II carboxy-terminal domain contributes to the response to multiple acidic activators in vitro. Genes Dev 5:2431-2440.
35. Liao SM, Zhang J, Jeffery DA, Koleske AJ, Thompson CM, Chao DM, Viljoen M, van Vuuren HJ, Young RA (1995): A kinase-cyclin pair in the RNA polymerase II holoenzyme. Nature 374:193-196.
36. Lu H, Flores O, Weinmann R, Reinberg D (1991): The nonphosphorylated form of RNA polymerase II prefferentially associates with the preinitiation complex. Proc Natl Acad Sci U S A 88:1004-1008.
37. Lu H, Zawel L, Fisher L, Egly JM, Reinberg D (1992): Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358:641-645.
38. Lue NF, Flanagan PM, Sugimoto K, Kornberg RD (1989): Initiation by yeast RNA polymerase II at the adenoviral major late promoter in vitro. Science 246:661-664.
39. Nonet M, Sweetser D, Young RA (1987): Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 50:909-915.
40. Payne JM, Dahmus ME (1993): Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxyl-terminal domain of RNA polymerase subunit IIa. J Biol Chem 268:80-87.
41. 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.
42. Peterson SR, Dvir A, Anderson CW, Dynan WS (1992): DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes Dev 6:426-438.
43. Prescott DM, Bender MA (1962): Synthesis of RNA and protein during mitosis in mammalian tissue culture cells. Exp Cell Res 26:260-268.
44. Roy R, Adamczewski JP, Seroz T, Vermeulen W, Tassan JP, Schaeffer L, Nigg EA, Hoeijmakers JHJ, Egly JM (1994): e Mo15 cell cycle kinase is associated with the TFIIH transcription DNA repair factor. Cell 79:1093-1101.
45. Sawadogo M, Roeder RG (1985): Factors involved in specific transcription by human RNA polymerase II: Analysis by a rapid and quantitative in vitro assay. Proc Natl Acad Sci U S A 82:4394-4398.
46. Sayre MH, Tschochner H, Kornberg RD (1992): Reconstitution of transcription with five purified initiation factors and RNA polymerase II from Saccharomyces cerevisiae. J Biol Chem 267:23376-23382.
47. Serizawa H, Conaway RC, Conaway JW (1992): A carboxylterminal-domain kinase associated with RNA polymerase II transcription factor delta from rat liver. Proc Natl Acad Sci U S A 89:7476-7480.
48. Serizawa H, Conaway JW, Conaway RC (1993): Phosphorylation of C-terminal domain of RNA polymerase II is not required in basal transcription. Nature 363:371-374.
49. Shiekhattar R, Mermelstein F, Fisher RP, Drapkin R, Dynlacht B, Wessling HC, Morgan DO, Reinberg D (1995): Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374:283-287.
50. Stone N, Reinberg D (1992): Protein kinases from Aspergillus nidulans that phosphorylate the carboxyl-terminal domain of the largest subunit of RNA polymerase II. J Biol Chem 267:6353-6360.
51. Svejstrup JQ, Wang Z, Feaver WJ, Wu X, Bushnell DA, Donahue TF, Friedberg EC, Kornberg RD (1995): Different forms of TFIIH for transcription and DNA repair: Holo-TFIIH and a nucleotide excision repairosome. Cell 80:21-28.
52. Taylor J (1960): Nucleic acid synthesis in relation to the cell division cycle. Ann N Y Acad Sci 90:409-421.
53. Tazi J, Kornstadt U, Rossi F, Jeanteur P, Cathala G, Brunel C, Luhrmann R (1993): Thiophosphorylation of U1-70K protein inhibits pre-mRNA splicing. Nature 363:283-286.
54. Thompson NE, Steinberg TH, Aronson DB, Burgess RR (1989): Inhibition of in vivo and in vitro transcription by noclonal 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.
55. Valay JG, Simon M, Dubois MF, 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.
56. Weeks JR, Hardin SE, Shen JJ, Lee JM, Greenleaf AL (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.
57. West MAL, Corden JL (1995): Construction and analysis of yeast RNA polymerase II CTD deletion and substitution mutations. Genetics 140:1223-1233.
58. White RJ, Gottlieb TM, Downes CS, Jackson SP (1995): Mitotic regulation of a TATA-binding-protein-containing complex. Mol Cell Biol 15:1983-1992.
59. Wilson IA, Niman HL, Houghten RA, Cherenson AR, Connolly ML, Lerner RA (1984): The structure of an antigenic determinant in a protein. Cell 37:767-778.
60. Woontner M, Wade PA, Bonner J, Jaehning JA (1991): Transcriptional activation in an improved whole-cell extract from Saccharomyces cerevisiae. Mol Cell Biol 11: 4555-4560.
61. Xu H, Boeke JD (1990): Localization of sequences required in cis for yeast Ty1 element transposition near the long terminal repeats: Analysis of mini-Ty1 elements. Mol Cell Biol 10:2695-2702.
62. Zawel L, Lu H, Cisek LJ, Corden JL, Reinberg D (1993): The cycling of RNA polymerase II during transcription. Cold Spring Harbor Symp Quant Biol 58:187-198.
63. Zhang J, Corden JL (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.