CTD serine-2 plays a critical role in splicing and termination factor recruitment to RNA polymerase II in vivo

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 1591-1603

  Gu, Bo ^a   Eick, Dirk ^a   Bensaude, Olivier ^a,b,c,d  

^a PSL RESEARCH UNIVERSITY   (France)

^b CNRS   (France)

^c INSERM   (France)

^d Munich Center for Integrated Protein Science   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; CELL PROTEIN; MESSENGER RNA; RNA POLYMERASE II; RPB1 PROTEIN; SERINE; SMALL NUCLEAR RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE SWITCHING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA CLEAVAGE; RNA SPLICING; SIGNAL TRANSDUCTION;

ALANINE; AMINO ACID SUBSTITUTION; CELL LINE; HUMANS; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTO-ONCOGENE PROTEINS C-FOS; RIBONUCLEOPROTEINS; RNA 3' END PROCESSING; RNA CLEAVAGE; RNA POLYMERASE II; RNA SPLICING; RNA, SMALL NUCLEAR; SERINE; TRANSCRIPTION, GENETIC;

EID: 84873676209     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1327     Document Type: Article

References (56)

1. Will,C.L. and Luhrmann,R. (2011) Spliceosome structure and function. Cold Spring Harb. Perspect. Biol., 3.
2. Proudfoot,N.J. (2011) Ending the message: poly(A) signals then and now. Genes Dev., 25, 1770-1782.
3. Martinson,H.G. (2011) An active role for splicing in 30-end formation. Wiley Interdiscip. Rev. RNA, 2, 459-470.
4. Niwa,M., Rose,S.D. and Berget,S.M. (1990) In vitro polyadenylation is stimulated by the presence of an upstream intron. Genes Dev., 4, 1552-1559.
5. Niwa,M. and Berget,S.M. (1991) Mutation of the AAUAAA polyadenylation signal depresses in vitro splicing of proximal but not distal introns. Genes Dev., 5, 2086-2095.
6. de Almeida,S.F. and Carmo-Fonseca,M. (2008) The CTD role in cotranscriptional RNA processing and surveillance. FEBS Lett., 582, 1971-1976.
7. Perales,R. and Bentley,D. (2009) ''Cotranscriptionality'': the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell, 36, 178-191.
8. Chapman,R.D., Heidemann,M., Hintermair,C. and Eick,D. (2008) Molecular evolution of the RNA polymerase II CTD. Trends Genet., 24, 289-296.
9. Egloff,S., Dienstbier,M. and Murphy,S. (2012) Updating the RNA polymerase CTD code: adding gene-specific layers. Trends Genet., 28, 333-341.
10. 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.
11. 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.
12. Phatnani,H.P. and Greenleaf,A.L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev., 20, 2922-2936.
13. Egloff,S. and Murphy,S. (2008) Cracking the RNA polymerase II CTD code. Trends Genet., 24, 630-642.
14. Buratowski,S. (2009) Progression through the RNA polymerase II CTD cycle. Mol. Cell, 36, 541-546.
15. Hsin,J.P. and Manley,J.L. (2012) The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev., 26, 2119-2137.
16. Tietjen,J.R., Zhang,D.W., Rodriguez-Molina,J.B., White,B.E., Akhtar,M.S., Heidemann,M., Li,X., Chapman,R.D., Shokat,K., Keles,S. et al. (2010) Chemical-genomic dissection of the CTD code. Nat. Struct. Mol. Biol., 17, 1154-1161.
17. Kim,H., Erickson,B., Luo,W., Seward,D., Graber,J.H., Pollock,D.D., Megee,P.C. and Bentley,D.L. (2010) Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat. Struct. Mol. Biol., 17, 1279-1286.
18. Mayer,A., Lidschreiber,M., Siebert,M., Leike,K., Soding,J. and Cramer,P. (2010) Uniform transitions of the general RNA polymerase II transcription complex. Nat. Struct. Mol. Biol., 17, 1272-1278.
19. Hintermair,C., Heidemann,M., Koch,F., Descostes,N., Gut,M., Gut,I., Fenouil,R., Ferrier,P., Flatley,A., Kremmer,E. et al. (2012) Threonine-4 of mammalian RNA polymerase II CTD is targeted by Polo-like kinase 3 and required for transcriptional elongation. EMBO J., 31, 2784-2797.
20. Ahn,S.H., Kim,M. and Buratowski,S. (2004) Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 30 end processing. Mol. Cell, 13, 67-76.
21. Ni,Z., Schwartz,B.E., Werner,J., Suarez,J.R. and Lis,J.T. (2004) Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol. Cell, 13, 55-65.
22. Bird,G., Zorio,D.A. and Bentley,D.L. (2004) RNA polymerase II carboxy-terminal domain phosphorylation is required for cotranscriptional pre-mRNA splicing and 30-end formation. Mol. Cell. Biol., 24, 8963-8969.
23. Bartkowiak,B., Mackellar,A.L. and Greenleaf,A.L. (2011) Updating the CTD story: from tail to epic. Genet. Res. Int., 2011, 623718.
24. Blazek,D., Kohoutek,J., Bartholomeeusen,K., Johansen,E., Hulinkova,P., Luo,Z., Cimermancic,P., Ule,J. and Peterlin,B.M. (2011) The Cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev., 25, 2158-2172.
25. Mancebo,H.S., Lee,G., Flygare,J., Tomassini,J., Luu,P., Zhu,Y., Peng,J., Blau,C., Hazuda,D., Price,D. et al. (1997) P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev., 11, 2633-2644.
26. Knight,Z.A. and Shokat,K.M. (2005) Features of selective kinase inhibitors. Chem. Biol., 12, 621-637.
27. Bensaude,O. (2011) Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription, 2, 103-108.
28. Zhou,Q., Li,T. and Price,D.H. (2012) RNA polymerase II elongation control. Ann. Rev. Biochem., 81, 119-143.
29. Hsin,J.P., Sheth,A. and Manley,J.L. (2011) RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 30 end processing. Science, 334, 683-686.
30. Egloff,S., O'Reilly,D., Chapman,R.D., Taylor,A., Tanzhaus,K., Pitts,L., Eick,D. and Murphy,S. (2007) Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression. Science, 318, 1777-1779.
31. Chapman,R.D., Heidemann,M., Albert,T.K., Mailhammer,R., Flatley,A., Meisterernst,M., Kremmer,E. and Eick,D. (2007) Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science, 318, 1780-1782.
32. Brody,Y., Neufeld,N., Bieberstein,N., Causse,S.Z., Bohnlein,E.M., Neugebauer,K.M., Darzacq,X. and Shav-Tal,Y. (2011) The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing. PLoS Biol., 9, e1000573.
33. Cramer,P., Pesce,C.G., Baralle,F.E. and Kornblihtt,A.R. (1997) Functional association between promoter structure and transcript alternative splicing. Proc. Natl Acad. Sci. USA, 94, 11456-11460.
34. Spiluttini,B., Gu,B., Belagal,P., Smirnova,A.S., Nguyen,V.T., Hébert,C., Schmidt,U., Bertrand,E., Darzacq,X. and Bensaude,O. (2010) Splicing-independent recruitment of U1 snRNP to a transcription unit in living cells. J. Cell. Sci., 123, 2085-2093.
35. Janicki,S.M., Tsukamoto,T., Salghetti,S.E., Tansey,W.P., Sachidanandam,R., Prasanth,K.V., Ried,T., Shav-Tal,Y., Bertrand,E., Singer,R.H. et al. (2004) From silencing to gene expression: real-time analysis in single cells. Cell, 116, 683-698.
36. Pacheco,T.R., Coelho,M.B., Desterro,J.M., Mollet,I. and Carmo-Fonseca,M. (2006) In vivo requirement of the small subunit of U2AF for recognition of a weak 30 splice site. Mol. Cell. Biol., 26, 8183-8190.
37. Zhao,J., Sun,B.K., Erwin,J.A., Song,J.J. and Lee,J.T. (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science, 322, 750-756.
38. Darzacq,X., Shav-Tal,Y., de Turris,V., Brody,Y., Shenoy,S.M., Phair,R.D. and Singer,R.H. (2007) In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol., 14, 796-806.
39. Bartolomei,M.S. and Corden,J.L. (1987) Localization of an a-amanitin resistance mutation in the gene encoding the largest subunit of mouse RNA polymerase II. Mol. Cell. Biol., 7, 586-594.
40. Bittencourt,D. and Auboeuf,D. (2012) Analysis of co-transcriptional RNA processing by RNA-ChIP assay. Methods Mol. Biol., 809, 563-577.
41. Martins,S.B., Rino,J., Carvalho,T., Carvalho,C., Yoshida,M., Klose,J.M., de Almeida,S.F. and Carmo-Fonseca,M. (2011) Spliceosome assembly is coupled to RNA polymerase II dynamics at the 30 end of human genes. Nat. Struct. Mol. Biol., 18, 1115-1123.
42. 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 30 end processing factors with RNA polymerase II. Mol. Cell., 9, 1101-1111.
43. Millhouse,S. and Manley,J.L. (2005) The C-terminal domain of RNA polymerase II functions as a phosphorylation-dependent splicing activator in a heterologous protein. Mol. Cell. Biol., 25, 533-544.
44. Tsao,D.C., Park,N.J., Nag,A. and Martinson,H.G. (2012) Prolonged alpha-amanitin treatment of cells for studying mutated polymerases causes degradation of DSIF160 and other proteins. RNA, 18, 222-229.
45. Pei,Y., Schwer,B. and 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.
46. Guiguen,A., Soutourina,J., Dewez,M., Tafforeau,L., Dieu,M., Raes,M., Vandenhaute,J., Werner,M. and Hermand,D. (2007) Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J., 21, 1552-1559.
47. Lenasi,T., Peterlin,B.M. and Barboric,M. (2011) Cap-binding protein complex links pre-mRNA capping to transcription elongation and alternative splicing through positive transcription elongation factor b (P-TEFb). J. Biol. Chem., 286, 22758-22768.
48. Valcarcel,J., Gaur,R.K., Singh,R. and Green,M.R. (1996) Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA [corrected]. Science, 273, 1706-1709.
49. David,C.J., Boyne,A.R., Millhouse,S.R. and Manley,J.L. (2011) The RNA polymerase II C-terminal domain promotes splicing activation through recruitment of a U2AF65-Prp19 complex. Genes Dev., 25, 972-983.
50. Das,R., Yu,J., Zhang,Z., Gygi,M.P., Krainer,A.R., Gygi,S.P. and Reed,R. (2007) SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol. Cell, 26, 867-881.
51. Sims,R.J. 3rd, Millhouse,S., Chen,C.F., Lewis,B.A., Erdjument-Bromage,H., Tempst,P., Manley,J.L. and Reinberg,D. (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell, 28, 665-676.
52. Gunderson,F.Q., Merkhofer,E.C. and Johnson,T.L. (2011) Dynamic histone acetylation is critical for cotranscriptional spliceosome assembly and spliceosomal rearrangements. Proc. Natl Acad. Sci. USA, 108, 2004-2009.
53. Allemand,E., Batsche,E. and Muchardt,C. (2008) Splicing, transcription, and chromatin: a menage a trois. Curr. Opin. Genet. Dev., 18, 145-151.
54. Meinhart,A. and Cramer,P. (2004) Recognition of RNA polymerase II carboxy-terminal domain by 30-RNA-processing factors. Nature, 430, 223-226.
55. Lunde,B.M., Reichow,S.L., Kim,M., Suh,H., Leeper,T.C., Yang,F., Mutschler,H., Buratowski,S., Meinhart,A. and Varani,G. (2010) Cooperative interaction of transcription termination factors with the RNA polymerase II C-terminal domain. Nat. Struct. Mol. Biol., 17, 1195-1201.
56. Vagner,S., Vagner,C. and Mattaj,I.W. (2000) The carboxyl terminus of vertebrate poly(A) polymerase interacts with U2AF 65 to couple 30-end processing and splicing. Genes Dev., 14, 403-413.