Nuclear import of RNA polymerase II is coupled with nucleocytoplasmic shuttling of the RNA polymerase II-associated protein 2

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 6881-6891

  Forget, Diane ^a   Lacombe, Andrée Anne ^a   Cloutier, Philippe ^a   Lavallée Adam, Mathieu ^b   Blanchette, Mathieu ^b   Coulombe, Benoit ^a,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN GPN1; RNA POLYMERASE II; RNA POLYMERASE II ASSOCIATED PROTEIN 2; RNA POLYMERASE II ASSOCIATED PROTEIN 4; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NUCLEAR IMPORT; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; CARRIER PROTEINS; CELL NUCLEUS; CYTOPLASM; GTP-BINDING PROTEINS; HELA CELLS; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SORTING SIGNALS; RNA INTERFERENCE; RNA POLYMERASE II;

EID: 84881540559     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt455     Document Type: Article

References (43)

1. Orphanides G., Lagrange T. and Reinberg D. (1996) The general transcription factors of RNA polymerase II. Genes Dev., 10, 2657-2683
2. Coulombe B. and Burton Z.F. (1999) DNA bending and wrapping around RNA polymerase: A ''revolutionary'' model describing transcriptional mechanisms. Microbiol. Mol. Biol. Rev., 63, 457-478
3. Roeder R.G. (2005) Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett., 579, 909-915
4. Marr M.T., Isogai Y., Wright K.J. and Tjian R. (2006) Coactivator cross-Talk specifies transcriptional output. Genes Dev., 20, 1458-1469
5. Hampsey M. (1998) Molecular genetics of the RNA polymerase II general transcriptional machinery. Microbiol. Mol. Biol. Rev., 62, 465-503
6. Li B., Carey M. and Workman J.L. (2007) The role of chromatin during transcription. Cell, 128, 707-719
7. Kornberg R.D. (2007) The molecular basis of eukaryotic transcription. Proc. Natl Acad. Sci. USA, 104, 12955-12961
8. Conaway R.C., Sato S., Tomomori-Sato C., Yao T. and Conaway J.W. (2005) The mammalian Mediator complex and its role in transcriptional regulation. Trends Biochem. Sci., 30, 250-255
9. Buratowski S. (2003) The CTD code. Nat. Struct. Biol., 10, 679-680
10. Phatnani H.P. and Greenleaf A.L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev., 20, 2922-2936
11. Meinhart A., Kamenski T., Hoeppner S., Baumli S. and Cramer P. (2005) A structural perspective of CTD function. Genes Dev., 19, 1401-1415
12. Bensaude O., Bonnet F., Casse C., Dubois M.F., Nguyen V.T. and Palancade B. (1999) Regulated phosphorylation of the RNA polymerase II C-Terminal domain (CTD). Biochem. Cell Biol., 77, 249-255
13. Corden J.L. and Patturajan M. (1997) A CTD function linking transcription to splicing. Trends Biochem. Sci., 22, 413-416
14. 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
15. Laurencikiene J., Kallman A.M., Fong N., Bentley D.L. and Ohman M. (2006) RNA editing and alternative splicing: The importance of co-Transcriptional coordination. EMBO Rep., 7, 303-307
16. Cloutier P. and Coulombe B. (2010) New insights into the biogenesis of nuclear RNA polymerases? Biochem. Cell Biol., 88, 211-221
17. Forget D., Lacombe A.A., Cloutier P., Al Khoury R., Bouchard A., Lavallee-Adam M., Faubert D., Jeronimo C., Blanchette M. and Coulombe B. (2010) The protein interaction network of the human transcription machinery reveals a role for the GTPase RPAP4/GPN1 and microtubule assembly in nuclear import and biogenesis of RNA polymerase II. Mol. Cell Proteomics, 9, 2827-2839
18. Jeronimo C., Langelier M.F., Zeghouf M., Cojocaru M., Bergeron D., Baali D., Forget D., Mnaimneh S., Davierwala A.P., Pootoolal J. et al. (2004) RPAP1, a novel human RNA polymerase II-Associated protein affinity purified with recombinant wild-Type and mutated polymerase subunits. Mol. Cell Biol., 24, 7043-7058
19. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., Poitras C., Therien C., Bergeron D., Bourassa S., Greenblatt J. et al. (2007) Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol. Cell, 27, 262-274
20. Wild T. and Cramer P. (2012) Biogenesis of multisubunit RNA polymerases. Trends Biochem. Sci., 37, 99-105
21. Gras S., Fernandez B., Chaumont V., Carpentier P., Armengaud J. and Housset D. (2005) Expression, purification, crystallization and preliminary crystallographic analysis of the PAB0955 gene product. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 61, 208-211
22. Nitta M., Saijo M., Kodo N., Matsuda T., Nakatsu Y., Tamai H. and Tanaka K. (2000) A novel cytoplasmic GTPase XAB1 interacts with DNA repair protein XPA. Nucleic Acids Res., 28, 4212-4218
23. Lembo F., Pero R., Angrisano T., Vitiello C., Iuliano R., Bruni C.B. and Chiariotti L. (2003) MBDin, a novel MBD2-interacting protein, relieves MBD2 repression potential and reactivates transcription from methylated promoters. Mol. Cell Biol., 23, 1656-1665
24. Staresincic L., Walker J., Dirac-Svejstrup A.B., Mitter R. and Svejstrup J.Q. (2011) GTP-dependent binding and nuclear transport of RNA polymerase II by Npa3 protein. J. Biol. Chem., 286, 35553-35561
25. Carre C. and Shiekhattar R. (2011) Human GTPases associate with RNA polymerase II to mediate its nuclear import. Mol. Cell Biol., 31, 3953-3962
26. Boulon S., Pradet-Balade B., Verheggen C., Molle D., Boireau S., Georgieva M., Azzag K., Robert M.C., Ahmad Y., Neel H. et al. (2010) HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol. Cell, 39, 912-924
27. Gstaiger M., Luke B., Hess D., Oakeley E.J., Wirbelauer C., Blondel M., Vigneron M., Peter M. and Krek W. (2003) Control of nutrient-sensitive transcription programs by the unconventional prefoldin URI. Science, 302, 1208-1212
28. Sardiu M.E., Cai Y., Jin J., Swanson S.K., Conaway R.C., Conaway J.W., Florens L. and Washburn M.P. (2008) Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc. Natl Acad. Sci. USA, 105, 1454-1459
29. Cloutier P., Al Khoury R., Lavallee-Adam M., Faubert D., Jiang H., Poitras C., Bouchard A., Forget D., Blanchette M. and Coulombe B. (2009) High-resolution mapping of the protein interaction network for the human transcription machinery and affinity purification of RNA polymerase II-Associated complexes. Methods, 48, 381-386
30. Czeko E., Seizl M., Augsberger C., Mielke T. and Cramer P. (2011) Iwr1 directs RNA polymerase II nuclear import. Mol. Cell, 42, 261-266
31. Gibney P.A., Fries T., Bailer S.M. and Morano K.A. (2008) Rtr1 is the Saccharomyces cerevisiae homolog of a novel family of RNA polymerase II-binding proteins. Eukaryot. Cell, 7, 938-948
32. Egloff S., Zaborowska J., Laitem C., Kiss T. and Murphy S. (2012) Ser7 phosphorylation of the CTD recruits the RPAP2 Ser5 phosphatase to snRNA genes. Mol. Cell, 45, 111-122
33. Mosley A.L., Pattenden S.G., Carey M., Venkatesh S., Gilmore J.M., Florens L., Workman J.L. and Washburn M.P. (2009) Rtr1 is a CTD phosphatase that regulates RNA polymerase II during the transition from serine 5 to serine 2 phosphorylation. Mol. Cell, 34, 168-178
34. Zwijsen R.M., Buckle R.S., Hijmans E.M., Loomans C.J. and Bernards R. (1998) Ligand-independent recruitment of steroid receptor coactivators to estrogen receptor by cyclin D1. Genes Dev., 12, 3488-3498
35. Sorokin A.V., Kim E.R. and Ovchinnikov L.P. (2007) Nucleocytoplasmic transport of proteins. Biochemistry, 72, 1439-1457
36. Pouton C.W., Wagstaff K.M., Roth D.M., Moseley G.W. and Jans D.A. (2007) Targeted delivery to the nucleus. Adv. Drug Deliv. Rev., 59, 698-717
37. Douziech M., Forget D., Greenblatt J. and Coulombe B. (1999) Topological localization of the carboxyl-Terminal domain of RNA polymerase II in the initiation complex. J. Biol. Chem., 274, 19868-19873
38. Robert F., Blanchette M., Maes O., Chabot B. and Coulombe B. (2002) A human RNA polymerase II-containing complex associated with factors necessary for spliceosome assembly. J. Biol. Chem., 277, 9302-9306
39. Reyes-Pardo H., Barbosa-Camacho A.A., Perez-Mejia A.E., Lara-Chacon B., Salas-Estrada L.A., Robledo-Rivera A.Y., Montero-Moran G.M., Lara-Gonzalez S., Calera M.R. and Sanchez-Olea R. (2012) A nuclear export sequence in GPN-loop GTPase 1, an essential protein for nuclear targeting of RNA polymerase II, is necessary and sufficient for nuclear export. Biochim. Biophys. Acta, 1823, 1756-1766
40. Amouyal M. and Buc H. (1987) Topological unwinding of strong and weak promoters by RNA polymerase. A comparison between the lac wild-Type and the UV5 sites of Escherichia coli. J. Mol. Biol., 195, 795-808
41. Roy A., Kucukural A. and Zhang Y. (2010) I-TASSER: A unified platform for automated protein structure and function prediction. Nat. Protoc., 5, 725-738
42. Lonhienne T.G., Forwood J.K., Marfori M., Robin G., Kobe B. and Carroll B.J. (2009) Importin-beta is a GDP-To-GTP exchange factor of Ran: Implications for the mechanism of nuclear import. J. Biol. Chem., 284, 22549-22558
43. Xiang K., Manley J.L. and Tong L. (2012) The yeast regulator of transcription protein Rtr1 lacks an active site and phosphatase activity. Nat. Commun., 3, 946