DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats.
10.1101/gad.6.3.426
Crossref journal-article
Cold Spring Harbor Laboratory
Genes & Development (246)
Abstract

Isolated transcription complexes contain a protein kinase that phosphorylates the heptapeptide repeats of the carboxy-terminal domain (CTD) of the RNA polymerase II (RNAP II) large subunit in an apparently promoter-dependent manner. We now show that the essential features of this reaction can be reproduced in a reconstituted system containing three macromolecular components: a fusion protein consisting of the CTD of RNAP II fused to a heterologous DNA-binding domain, an activating DNA fragment containing the recognition sequence for the fusion protein, and a protein kinase that binds nonspecifically to DNA. This kinase closely resembles a previously known DNA-dependent protein kinase. Evidently, the association of the CTD with DNA provides a key signal for phosphorylation. There appears to be no absolute requirement for specific contacts with other DNA-bound transcription factors.

Bibliography

Peterson, S. R., Dvir, A., Anderson, C. W., & Dynan, W. S. (1992). DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats. Genes & Development, 6(3), 426–438.

Authors 4
  1. S R Peterson (first)
  2. A Dvir (additional)
  3. C W Anderson (additional)
  4. W S Dynan (additional)
References 56 Referenced 103
  1. 10.1016/S0021-9258(18)61020-8 / J. Biol. Chem. / Cloning and sequence analysis of the mouse genomic locus encoding the largest subunit of RNA polymerase II. (1987)
  2. 10.1073/pnas.86.8.2794
  3. 10.1016/0092-8674(85)90117-5
  4. {'key': '2021111320212923000_6.3.426.4', 'first-page': '321', 'article-title': '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.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / 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. (1988)
  5. 10.1016/S0021-9258(18)94055-X / J. Biol. Chem. / Promoter-dependent transcription by RNA polymerase II using immobilized enzyme complexes. (1989)
  6. 10.1016/S0021-9258(18)92939-X / J. Biol. Chem. / Promoter-dependent phosphorylation of RNA polymerase II by a template-bound kinase. (1991)
  7. 10.1016/S0021-9258(18)67008-5 / J. Biol. Chem. / RNA contacts subunits IIo and IIc in HeLa RNA polymerase II transcription complexes. (1986)
  8. {'key': '2021111320212923000_6.3.426.8', 'first-page': '330', 'article-title': 'Genetic analysis of the repetitive carboxy-terminal domain of the largest subunit of mouse RNA polymerase II.', 'volume': '8', 'year': '1988', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Genetic analysis of the repetitive carboxy-terminal domain of the largest subunit of mouse RNA polymerase II. (1988)
  9. 10.1016/0092-8674(91)90241-P
  10. 10.1016/0092-8674(89)90578-3
  11. 10.1016/S0021-9258(18)45229-5 / J. Biol. Chem. / Messenger RNA synthesis in mammalian cells is catalyzed by the phosphorylated form of RNA polymerase II. (1987)
  12. 10.1016/S0021-9258(19)75926-2 / J. Biol. Chem. / Transcription initiation by RNA polymerase II in vitro. (1987)
  13. {'key': '2021111320212923000_6.3.426.13', 'first-page': '6460', 'article-title': 'A DNA activated protein kinase from HeLa cell nuclei.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / A DNA activated protein kinase from HeLa cell nuclei. (1990)
  14. 10.1128/jvi.65.10.5131-5140.1991 / J. Virol. / The human DNA-activated protein kinase phosphorylates Simian virus 40 T antigen at amino- and carboxy-terminal sites. (1991)
  15. 10.1038/339679a0
  16. 10.1016/0076-6879(91)00148-P
  17. 10.1016/S0021-9258(18)69162-8 / J. Biol. Chem. / ATP activates transcription initiation from promoters by RNA polymerase II in a reversible step prior to RNA synthesis. (1988)
  18. 10.1016/0968-0004(90)90236-5
  19. 10.1073/pnas.82.23.7934
  20. {'key': '2021111320212923000_6.3.426.20', 'first-page': '3332', 'article-title': 'Phosphorylation of eukaryotic DNA-dependent RNA polymerase.', 'volume': '256', 'year': '1981', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. / Phosphorylation of eukaryotic DNA-dependent RNA polymerase. (1981)
  21. Dahmus, M.E. and W.S. Dynan. 1992. Phosphorylation of RNA polymerase II as a transcriptional regulatory mechanism. In Transcriptional regulation (ed. S.L. McKnight and K. Yamamoto), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
  22. 10.1016/0092-8674(91)90298-D
  23. 10.1073/pnas.88.3.999
  24. 10.1016/0092-8674(85)90336-8
  25. 10.1105/tpc.1.8.827
  26. 10.1016/0092-8674(90)90296-Q
  27. 10.1016/S0021-9258(18)94046-9 / J. Biol. Chem. / The major late promoter of adenovirus-2 is accurately transcribed by RNA polymerase IIo, IIa and IIb. (1989)
  28. {'key': '2021111320212923000_6.3.426.28', 'first-page': '260', 'article-title': 'Primary structure of the Saccharomyces cerevisiae GAL4 gene.', 'volume': '4', 'year': '1984', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Primary structure of the Saccharomyces cerevisiae GAL4 gene. (1984)
  29. 10.1016/S0021-9258(18)83483-4 / J. Biol. Chem. / Transcription-dependent structural changes in the C-terminal domain of mammalian RNA polymerase subunit IIa/o. (1989)
  30. 10.1016/S0021-9258(19)38281-X / J. Biol. Chem. / Phosphorylation of RNA polymerase IIa occurs subsequent to interaction with the promoter and before the initiation of transcription. (1990)
  31. 10.1073/pnas.86.10.3624
  32. {'key': '2021111320212923000_6.3.426.32', 'first-page': '149', 'article-title': 'CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiac.', 'volume': '1', 'year': '1991', 'journal-title': 'Gene Expression'} / Gene Expression / CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiac. (1991)
  33. 10.1016/S0021-9258(18)71488-9 / J. Biol. Chem. / The human double-stranded DNA-activated protein kinase phosphorylates the 90-kD heat-shock protein, HSP90α at two NH2-terminal threonine residues. (1989)
  34. {'key': '2021111320212923000_6.3.426.34', 'first-page': '6472', 'article-title': 'Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku antigen.', 'volume': '10', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku antigen. (1990)
  35. 10.1016/S0092-8674(88)80010-2
  36. 10.1073/pnas.88.3.1004
  37. 10.1002/prot.340070204
  38. 10.1093/genetics/123.4.715 / Genetics / Intragenic and extragenic suppressors of mutations in the heptapeptide repeat domain of Saccharomyces cerevisiae RNA polymerase II. (1989)
  39. 10.1016/0092-8674(87)90517-4
  40. 10.1016/S0021-9258(19)47159-7 / J. Biol. Chem. / The transition of RNA polymerase II from initiation to elongation is associated with phosphorylation of the carboxy-terminal domain of subunit IIa. (1989)
  41. 10.1016/0092-8674(91)90268-4
  42. 10.1101/gad.3.5.620
  43. 10.1038/347491a0
  44. {'key': '2021111320212923000_6.3.426.44', 'first-page': '2424', 'article-title': 'In vitro activation and nuclear translocation of NF-κB catalyzed by cyclic AMP-dependent protein kinase and protein kinase C.', 'volume': '9', 'year': '1989', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / In vitro activation and nuclear translocation of NF-κB catalyzed by cyclic AMP-dependent protein kinase and protein kinase C. (1989)
  45. 10.1038/333210a0
  46. 10.1016/0378-1119(88)90005-4
  47. 10.1016/S0092-8674(88)91219-6
  48. 10.1016/0006-291X(89)90022-3
  49. 10.1038/344562a0
  50. 10.1016/S0021-9258(18)60493-4 / J. Biol. Chem. / 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. (1989)
  51. 10.1016/0968-0004(88)90047-3
  52. 10.1126/science.3413495
  53. 10.1002/j.1460-2075.1985.tb02328.x / EMBO J. / Double-stranded DNA induces the phosphorylation of several proteins including the 90,000 mol. wt. heat-shock protein in animal cell extracts. (1985)
  54. 10.1073/pnas.85.11.3698
  55. 10.1016/S0021-9258(18)52242-0 / J. Biol. Chem. / Identification of phosphorylation in the repetitive carboxyl terminal domain of the mouse RNA polymerase II largest subunit. (1991)
  56. 10.1016/S0021-9258(18)52243-2 / J. Biol. Chem. / Phosphorylation causes a conformational change in the carboxyl terminal domain of the mouse RNA polymerase II largest subunit. (1991)
Dates
Type When
Created 18 years, 2 months ago (June 5, 2007, 5:15 p.m.)
Deposited 3 years, 9 months ago (Nov. 13, 2021, 11:24 p.m.)
Indexed 1 month, 3 weeks ago (July 2, 2025, 2:46 p.m.)
Issued 33 years, 5 months ago (March 1, 1992)
Published 33 years, 5 months ago (March 1, 1992)
Published Online 33 years, 5 months ago (March 1, 1992)
Published Print 33 years, 5 months ago (March 1, 1992)
Funders 0

None

@article{Peterson_1992, title={DNA binding provides a signal for phosphorylation of the RNA polymerase II heptapeptide repeats.}, volume={6}, ISSN={1549-5477}, url={http://dx.doi.org/10.1101/gad.6.3.426}, DOI={10.1101/gad.6.3.426}, number={3}, journal={Genes & Development}, publisher={Cold Spring Harbor Laboratory}, author={Peterson, S R and Dvir, A and Anderson, C W and Dynan, W S}, year={1992}, month=mar, pages={426–438} }