DOI: 10.1046/j.1432-1033.2003.03794.x. Investigating RNA polymerase II carboxyl‐terminal domain (CTD) phosphorylation

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

10.1046/j.1432-1033.2003.03794.x

Crossref journal-article

Wiley

European Journal of Biochemistry (311)

Abstract

Phosphorylation of RNA polymerase II's largest subunit C‐terminal domain (CTD) is a key event during mRNA metabolism. Numerous enzymes, including cell cycle‐dependent kinases and TFIIF‐dependent phosphatases target the CTD. However, the repetitive nature of the CTD prevents determination of phosphorylated sites by conventional biochemistry methods. Fortunately, a panel of monoclonal antibodies is available that distinguishes between phosphorylated isoforms of RNA polymerase II's (RNAP II) largest subunit. Here, we review how successful these tools have been in monitoring RNAP II phosphorylation changes in vivo by immunofluorescence, chromatin immunoprecipitation and immunoblotting experiments. The CTD phosphorylation pattern is precisely modified as RNAP II progresses along the genes and is involved in sequential recruitment of RNA processing factors. One of the most popular anti‐phosphoCTD Igs, H5, has been proposed in several studies as a landmark of RNAP II molecules engaged in transcription. Finally, we discuss how global RNAP II phosphorylation changes are affected by the physiological context such as cell stress and embryonic development.

Bibliography

Palancade, B., & Bensaude, O. (2003). Investigating RNA polymerase II carboxylâterminal domain (CTD) phosphorylation. European Journal of Biochemistry, 270(19), 3859â3870. Portico.

Authors 2

Benoît Palancade (first)
Olivier Bensaude (additional)

References 156 Referenced 195

10.1016/0959-437X(93)90025-K
10.1074/jbc.M001883200
10.1074/jbc.270.52.31255
10.1038/347491a0
10.1038/374660a0
10.1242/jcs.113.11.1841
10.1016/S0092-8674(02)00617-7
10.1016/S0167-4781(02)00460-8
10.1016/0968-0004(90)90236-5
{'key': 'e_1_2_16_11_2', 'first-page': '81', 'volume-title': 'Transcriptional Regulation', 'author': 'Corden J.L.', 'year': '1992'} / Transcriptional Regulation by Corden J.L. (1992)
10.1139/o99-047 / Biochem. Cell Biol. / Regulated phosphorylation of the RNA polymerase II C‐terminal domain (CTD) by Bensaude O. (1999)
10.1016/S0021-9258(18)82216-5
10.1074/jbc.271.32.19009
10.3727/000000001783992704
10.1002/jcp.10058
10.1016/S0167-4781(02)00457-8
10.2741/Majello
10.1128/EC.1.2.153-162.2002
10.1016/S0955-0674(02)00333-2
10.1016/S0021-9258(19)41503-2 / J. Biol. Chem. / Purification and subunit structure of deoxyribonucleic acid‐dependent ribonucleic acid polymerase II from the mouse plasmacytoma, MOPC 315 by Schwartz L.B. (1975)
10.1073/pnas.90.23.11167
10.1016/S0021-9258(18)52242-0 / J. Biol. Chem. / Identification of phosphorylation sites in the repetitive CTD of the mouse RNA polymerase II largest subunit by Zhang J. (1991)
10.1016/S0021-9258(18)32923-5 / J. Biol. Chem. / Transcription of adenovirus‐2 major late promoter inhibited by monoclonal antibody directed against RNA polymerases II0 and IIA by Dahmus M.E. (1983)
10.1016/S0021-9258(18)54117-X / J. Biol. Chem. / Partial purification and characterization of two distinct protein kinases that differentially phosphorylate the carboxy‐terminal domain of RNA polymerase subunit IIa by Payne J.M. (1993)
10.1128/JVI.75.20.9872-9884.2001
10.1128/jvi.68.2.988-1001.1994 / J. Virol. / RNA polymerase II is aberrantly phosphorylated and localized to viral replication compartments following Herpes Simplex virus infection by Rice S.A. (1994)
10.1093/nar/27.22.4399
10.1242/jcs.114.13.2483 / J. Cell Sci. / Incomplete RNA polymerase II phosphorylation in Xenopus laevis early embryos by Palancade B. (2001)
10.1093/emboj/16.20.6250
10.1093/emboj/19.7.1567
10.1074/jbc.273.8.4689
10.1016/S1097-2765(00)80187-2
10.1006/jmbi.1995.0316
10.1101/gad.935901
10.1016/S1047-8477(02)00547-6
10.1006/jmbi.2001.4991
10.1242/jcs.112.15.2493
10.1074/jbc.M010975200
10.1074/jbc.273.12.6769
10.1016/0092-8674(94)90039-6
10.1002/(SICI)1097-4644(19970301)64:3<390::AID-JCB6>3.0.CO;2-Q
10.1016/S1097-2765(00)80112-4
10.1038/sj.onc.1202399
10.1074/jbc.M111349200
10.1093/nar/25.4.694
10.1016/S1097-2765(00)80131-8
10.1074/jbc.M107466200
10.1128/MCB.21.1.1-15.2001
10.1128/MCB.22.13.4622-4637.2002
10.1128/MCB.20.14.5077-5086.2000
10.1093/emboj/16.7.1628
10.1101/gad.11.20.2633
10.1101/gad.11.20.2645
10.1016/S1074-7613(00)80159-4
10.1074/jbc.M002285200
10.1074/jbc.M109014200
10.1016/S1097-2765(01)00314-8
10.1101/gad.827900
10.1016/S0079-6603(02)72074-6
10.1074/jbc.M301791200
10.1006/viro.2002.1438
{'key': 'e_1_2_16_63_2', 'first-page': '15', 'article-title': 'Protein phosphatase‐1 dephosphorylates the C‐terminal domain of RNA polymerase‐II', 'volume': '15', 'author': 'Washington K.', 'year': '2002', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. / Protein phosphatase‐1 dephosphorylates the C‐terminal domain of RNA polymerase‐II by Washington K. (2002)
10.1093/emboj/cdg141
10.1074/jbc.M301643200
10.1101/gad.13.12.1540
10.1074/jbc.M208588200
10.1016/S0021-9258(18)45229-5
10.1016/S0021-9258(19)47159-7
10.1073/pnas.88.22.10004
10.1016/S0021-9258(19)50045-X / J. Biol. Chem. / The interaction of RNA polymerase II with the adenovirus‐2 major late promoter precluded by phosphorylation of the C‐terminal domain of subunit IIa by Chesnut J.D. (1992)
10.1074/jbc.275.20.14923
10.1074/jbc.M005898200
10.1038/370075a0
10.1128/MCB.23.6.1961-1967.2003
10.1101/gad.824700
10.1101/gad.836300
10.1093/genetics/140.4.1223
10.1093/genetics/143.2.661
10.1074/mcp.M200029-MCP200
10.1016/S1097-2765(00)80468-2
10.1074/jbc.M211713200
10.1074/jbc.M212101200
10.1073/pnas.90.23.10896
10.1128/MCB.18.4.2406
10.1083/jcb.136.1.19
10.1038/385357a0
10.1016/S1097-2765(02)00731-1
10.1016/S1097-2765(02)00518-X
10.1128/MCB.22.6.1684-1692.2002
10.1101/gad.889101
10.1016/S0092-8674(03)00360-X
10.1016/S1097-2765(03)00092-3
10.1016/S1097-2765(03)00091-1
10.1074/jbc.M209294200
10.1101/gad.1055503
10.1111/j.1432-1033.1995.083_1.x
10.1016/S0021-9258(17)36837-0 / J. Biol. Chem. / 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 by Dubois M.F. (1994)
10.1128/MCB.21.19.6359-6368.2001
10.1128/MCB.17.3.1434
{'key': 'e_1_2_16_101_2', 'first-page': '183', 'article-title': 'Ccl1, a cyclin associated with protein kinase Kin28 controls the phosphorylation of RNA polymerase II largest subunit and mRNA transcription', 'volume': '319', 'author': 'Valay J.G.', 'year': '1996', 'journal-title': 'C.R. Acad. Sci. Paris'} / C.R. Acad. Sci. Paris / Ccl1, a cyclin associated with protein kinase Kin28 controls the phosphorylation of RNA polymerase II largest subunit and mRNA transcription by Valay J.G. (1996)
10.1074/jbc.274.23.16097
10.1093/nar/24.15.2924
10.1073/pnas.93.21.11586
10.1038/35104581
10.1038/35104575
10.1128/EC.2.2.274-283.2003
10.1038/35024111
10.1101/gad.7.12a.2329
10.1093/emboj/16.6.1401
10.1083/jcb.129.2.287
10.1091/mbc.E02-10-0669
10.1242/dev.124.11.2191 / Development / Transcriptionally‐repressed germ cells lack a subpopulation of phosphorylated RNA polymerase II in early embryos of C. elegans and D. melanogaster by Seydoux G. (1997)
10.1083/jcb.149.4.875
10.1006/dbio.1998.8940
10.1101/gad.999002
10.1016/S1097-2765(00)00069-1
10.1016/S1097-2765(00)00068-X
10.1073/pnas.082618399
10.1074/jbc.C200305200
10.1093/emboj/20.18.5269
10.1016/S0960-9822(01)00076-8
10.1093/emboj/20.11.2844
10.1016/S0021-9258(18)60493-4
10.1073/pnas.93.16.8253
10.1093/nar/24.23.4649
10.1128/MCB.23.14.4859-4869.2003
10.1038/339679a0
10.1002/bies.950170603
10.1101/gad.12.4.456
10.1016/0968-0004(96)10046-3
10.1016/0092-8674(94)90535-5
10.1128/MCB.17.12.7220
10.1038/368160a0
10.1038/374193a0
10.1091/mbc.7.4.505
{'key': 'e_1_2_16_137_2', 'first-page': '2631', 'article-title': 'Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II', 'volume': '12', 'author': 'Rickert P.', 'year': '1996', 'journal-title': 'Oncogene'} / Oncogene / Cyclin C/CDK8 is a novel CTD kinase associated with RNA polymerase II by Rickert P. (1996)
10.1101/gad.867501
10.1016/S1097-2765(00)80360-3
10.1101/gad.11.20.2622
10.1128/MCB.20.8.2629-2634.2000
10.1128/JVI.73.7.5448-5458.1999
10.1074/jbc.M010908200
10.1038/sj.onc.1205511
10.1038/sj.onc.1205493
10.1073/pnas.86.10.3624
10.1128/MCB.15.10.5716
10.1074/jbc.274.39.27823
10.1128/MCB.21.13.4089-4096.2001
10.1002/j.1460-2075.1994.tb06804.x
10.1016/S0955-0674(96)80067-6
10.1073/pnas.89.24.11920
10.1101/gad.13.8.916
10.1016/S0962-8924(99)01549-4
10.1006/dbio.2001.0420
10.1016/S0962-8924(01)02247-4
10.1016/S0092-8674(02)00692-X

Dates

Type	When
Created	21 years, 11 months ago (Sept. 17, 2003, 3:56 a.m.)
Deposited	1 year, 10 months ago (Oct. 16, 2023, 4:58 a.m.)
Indexed	2 months ago (June 27, 2025, 7:03 p.m.)
Issued	21 years, 11 months ago (Sept. 9, 2003)
Published	21 years, 11 months ago (Sept. 9, 2003)
Published Online	21 years, 11 months ago (Sept. 9, 2003)
Published Print	21 years, 10 months ago (Oct. 1, 2003)

Funders 0

None

BibTeX

@article{Palancade_2003, title={Investigating RNA polymerase II carboxyl‐terminal domain (CTD) phosphorylation}, volume={270}, ISSN={1432-1033}, url={http://dx.doi.org/10.1046/j.1432-1033.2003.03794.x}, DOI={10.1046/j.1432-1033.2003.03794.x}, number={19}, journal={European Journal of Biochemistry}, publisher={Wiley}, author={Palancade, Benoît and Bensaude, Olivier}, year={2003}, month=sep, pages={3859–3870} }

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