A function for the hnRNP A1/A2 proteins in transcription elongation

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Lemieux, Bruno ^a   Blanchette, Marco ^b   Monette, Anne ^c   Mouland, Andrew J ^c   Wellinger, Raymund J ^a   Chabot, Benoit ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

^b STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^c MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

5,6 DICHLOROBENZIMIDAZOLE RIBOSIDE; 7SK RNA; CYCLIN DEPENDENT KINASE 9; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A2; MITOGEN ACTIVATED PROTEIN KINASE P38; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; RNA; RNA POLYMERASE II; SORBITOL; TRANSCRIPTOME; UNCLASSIFIED DRUG; CDK9 PROTEIN, HUMAN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN GROUP A B; HNRNP A1; HNRNP A2; SMALL INTERFERING RNA;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; GENE; GENE EXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; KITLG GENE; MYCUP1 GENE; OSMOTIC STRESS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN RNA BINDING; PROTEIN SYNTHESIS INHIBITION; PROTEIN TRANSPORT; REPORTER GENE; RNA ANALYSIS; RNA INTERFERENCE; TRANSCRIPTION ELONGATION; ALTERNATIVE RNA SPLICING; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; CELL LINE; CYTOPLASM; GENETICS; HCT 116 CELL LINE; METABOLISM; OSMOTIC PRESSURE;

ALTERNATIVE SPLICING; CELL LINE; CYCLIN-DEPENDENT KINASE 9; CYTOPLASM; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; GENES, REPORTER; HCT116 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; MODELS, BIOLOGICAL; OSMOTIC PRESSURE; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; RNA INTERFERENCE; RNA POLYMERASE II; RNA, SMALL INTERFERING; TRANSCRIPTION ELONGATION, GENETIC;

EID: 84959489713     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126654     Document Type: Article

References (52)

1. Bentley DL. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol. 2005; 17(3):251-256. PMID: 15901493
2. Kornblihtt AR, de la Mata M, Fededa JP, Munoz MJ, Nogues G. Multiple links between transcription and splicing. RNA. 2004; 10(10):1489-1498. PMID: 15383674
3. Maniatis T, Reed R. An extensive network of coupling among gene expression machines. Nature. 2002; 416(6880):499-506. PMID: 11932736
4. Neugebauer KM. On the importance of being co-transcriptional. J Cell Sci. 2002; 115(Pt 20):3865-3871. PMID: 12244124
5. Buratowski S. The CTD code. Nat Struct Biol. 2003; 10(9):679-680. PMID: 12942140
6. Egloff S, Murphy S. Cracking the RNA polymerase II CTD code. Trends Genet. 2008; 24(6):280-288. doi: 10.1016/j.tig.2008.03.008 PMID: 18457900
7. Zhou Q, Li T, Price DH. RNA polymerase II elongation control. Annual review of biochemistry. 2012; 81:119-143. doi: 10.1146/annurev-biochem-052610-095910 PMID: 22404626
8. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell. 2006; 23(3):297-305. PMID: 16885020
9. Barrandon C, Bonnet F, Nguyen VT, Labas V, Bensaude O. The transcription-dependent dissociation of P-TEFb-HEXIM1-7SK RNA relies upon formation of hnRNP-7SK RNA complexes. Mol Cell Biol. 2007; 27(20):6996-7006. PMID: 17709395
10. Van Herreweghe E, Egloff S, Goiffon I, Jady BE, Froment C, Monsarrat B, et al. Dynamic remodelling of human 7SK snRNP controls the nuclear level of active P-TEFb. EMBO J. 2007; 26(15):3570-3580. PMID: 17611602
11. Allemand E, Batsche E, Muchardt C. Splicing, transcription, and chromatin: a menage a trois. Curr Opin Genet Dev. 2008; 18(2):145-151. doi: 10.1016/j.gde.2008.01.006 PMID: 18372167
12. Ip JY, Schmidt D, Pan Q, Ramani AK, Fraser AG, Odom DT, et al. Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation. Genome Res. 2011; 21(3):390-401. doi: 10. 1101/gr.111070.110 PMID: 21163941
13. Moldon A, Malapeira J, Gabrielli N, Gogol M, Gomez-Escoda B, Ivanova T, et al. Promoter-driven splicing regulation in fission yeast. Nature. 2008; 455(7215):997-1000. doi: 10.1038/nature07325 PMID: 18815595
14. Fong YW, Zhou Q. Stimulatory effect of splicing factors on transcriptional elongation. Nature. 2001; 414 (6866):929-933. PMID: 11780068
15. Yan D, Perriman R, Igel H, Howe KJ, Neville M, Ares M Jr. CUB, a yeast homolog of human Tat-SF1, rescues function of misfolded U2 through an unusual RNA recognition motif. Mol Cell Biol. 1998; 18 (9):5000-5009. PMID: 9710584
16. Das R, Yu J, Zhang Z, Gygi MP, Krainer AR, Gygi SP, et al. SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol Cell. 2007; 26(6):867-881. PMID: 17588520
17. Lin S, Coutinho-Mansfield G, Wang D, Pandit S, Fu XD. The splicing factor SC35 has an active role in transcriptional elongation. Nat Struct Mol Biol. 2008; 15(8):819-826. doi: 10.1038/nsmb.1461 PMID: 18641664
18. Martinez-Contreras R, Cloutier P, Shkreta L, Fisette JF, Revil T, Chabot B. hnRNP proteins and splicing control. Adv Exp Med Biol. 2007; 623:123-147. PMID: 18380344
19. Zhao TT, Graber TE, Jordan LE, Cloutier M, Lewis SM, Goulet I, et al. hnRNP A1 regulates UV-induced NF-kappaB signalling through destabilization of cIAP1 mRNA. Cell Death Differ. 2008; 16:244-252. doi: 10.1038/cdd.2008.146 PMID: 18846111
20. Beriault V, Clement JF, Levesque K, Lebel C, Yong X, Chabot B, et al. A late role for the association of hnRNP A2 with the HIV-1 hnRNP A2 response elements in genomic RNA, Gag, and Vpr localization. J Biol Chem. 2004; 279(42):44141-44153. PMID: 15294897
21. Guil S, Caceres JF. The multifunctional RNA-binding protein hnRNP A1 is required for processing of miR-18a. Nat Struct Mol Biol. 2007; 14(7):591-596. PMID: 17558416
22. Zhang QS, Manche L, Xu RM, Krainer AR. hnRNP A1 associates with telomere ends and stimulates telomerase activity. RNA. 2006; 12(6):1116-1128. PMID: 16603717
23. Fiset S, Chabot B. hnRNP A1 may interact simultaneously with telomeric DNA and the human telomerase RNA in vitro. Nucleic Acids Res. 2001; 29(11):2268-2275. PMID: 11376145
24. LaBranche H, Dupuis S, Ben-David Y, Bani MR, Wellinger RJ, Chabot B. Telomere elongation by hnRNP A1 and a derivative that interacts with telomeric repeats and telomerase. Nat Genet. 1998; 19 (2):199-202. PMID: 9620782
25. Flynn RL, Centore RC, O\'Sullivan RJ, Rai R, Tse A, Songyang Z, et al. TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature. 2011; 471(7339):532-536. doi: 10.1038/nature09772 PMID: 21399625
26. Xia H. Regulation of gamma-fibrinogen chain expression by heterogeneous nuclear ribonucleoprotein A1. J Biol Chem. 2005; 280(13):13171-13178. PMID: 15671034
27. Michelotti EF, Michelotti GA, Aronsohn AI, Levens D. Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol Cell Biol. 1996; 16(5):2350-2360. PMID: 8628302
28. Kukalev A, Nord Y, Palmberg C, Bergman T, Percipalle P. Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol. 2005; 12(3):238-244. PMID: 15711563
29. Obrdlik A, Kukalev A, Louvet E, Farrants AK, Caputo L, Percipalle P. The histone acetyltransferase PCAF associates with actin and hnRNP U for RNA polymerase II transcription. Mol Cell Biol. 2008; 28 (20):6342-6357. doi: 10.1128/MCB.00766-08 PMID: 18710935
30. Jeronimo C, Forget D, Bouchard A, Li Q, Chua G, Poitras C, et al. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol Cell. 2007; 27(2):262-274. PMID: 17643375
31. Hogg JR, Collins K. RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA. 2007; 13(6):868-880. PMID: 17456562
32. Krueger BJ, Jeronimo C, Roy BB, Bouchard A, Barrandon C, Byers SA, et al. LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated. Nucleic Acids Res. 2008; 36(7):2219-2229. doi: 10.1093/nar/gkn061 PMID: 18281698
33. Yang Z, Zhu Q, Luo K, Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature. 2001; 414(6861):317-322. PMID: 11713532
34. Nguyen VT, Kiss T, Michels AA, Bensaude O. 7SK small nuclear RNA binds to and inhibits the activity of CDK9/cyclin T complexes. Nature. 2001; 414(6861):322-325. PMID: 11713533
35. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000; 132:365-386. PMID: 10547847
36. van der Houven van Oordt W, Diaz-Meco MT, Lozano J, Krainer AR, Moscat J, Caceres JF. The MKK (3/6)-p38-signaling cascade alters the subcellular distribution of hnRNP A1 and modulates alternative splicing regulation. J Cell Biol. 2000; 149(2):307-316. PMID: 10769024
37. Lévesque K, Halvorsen M, Abrahamyan L, Chatel-Chaix L, Poupon V, Gordon H, et al. Trafficking of HIV-1 RNA is mediated by heterogeneous nuclear ribonucleoprotein A2 expression and impacts on viral assembly. Traffic. 2006; 7(9):1177-1193. PMID: 17004321
38. Svotelis A, Gevry N, Gaudreau L. Chromatin immunoprecipitation in mammalian cells. Methods Mol Biol. 2009; 543:243-251. doi: 10.1007/978-1-60327-015-1-16 PMID: 19378170
39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009; 25(16):2078-2079. doi: 10.1093/bioinformatics/btp352 PMID: 19505943
40. Bartholomeeusen K, Xiang Y, Fujinaga K, Peterlin BM. Bromodomain and extra-terminal (BET) bromodomain inhibition activate transcription via transient release of positive transcription elongation factor b (P-TEFb) from 7SK small nuclear ribonucleoprotein. J Biol Chem. 2012; 287(43):36609-36616. doi: 10.1074/jbc.M112.410746 PMID: 22952229
41. Singh J, Padgett RA. Rates of in situ transcription and splicing in large human genes. Nat Struct Mol Biol. 2009; 16(11):1128-1133. doi: 10.1038/nsmb.1666 PMID: 19820712
42. Allemand E, Guil S, Myers M, Moscat J, Caceres JF, Krainer AR. Regulation of heterogenous nuclear ribonucleoprotein A1 transport by phosphorylation in cells stressed by osmotic shock. Proc Natl Acad Sci U S A. 2005; 102(10):3605-3610. PMID: 15738418
43. Buxade M, Parra JL, Rousseau S, Shpiro N, Marquez R, Morrice N, et al. The Mnks are novel components in the control of TNF alpha biosynthesis and phosphorylate and regulate hnRNP A1. Immunity. 2005; 23(2):177-189. PMID: 16111636
44. Guil S, Long JC, Caceres JF. hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol Cell Biol. 2006; 26(15):5744-5758. PMID: 16847328
45. Venables JP, Koh CS, Froehlich U, Lapointe E, Couture S, Inkel L, et al. Multiple and specific mRNA processing targets for the major human hnRNP proteins. Mol Cell Biol. 2008; 28(19):6033-6043. doi: 10.1128/MCB.00726-08 PMID: 18644864
46. Huelga SC, Vu AQ, Arnold JD, Liang TY, Liu PP, Yan BY, et al. Integrative genome-wide analysis reveals cooperative regulation of alternative splicing by hnRNP proteins. Cell reports. 2012; 1(2):167-178. PMID: 22574288
47. Bensaude O. Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription. 2011; 2(3):103-108. PMID: 21922053
48. Markert A, Grimm M, Martinez J, Wiesner J, Meyerhans A, Meyuhas O, et al. The La-related protein LARP7 is a component of the 7SK ribonucleoprotein and affects transcription of cellular and viral polymerase II genes. EMBO Rep. 2008; 9(6):569-575. doi: 10.1038/embor.2008.72 PMID: 18483487
49. Ji X, Zhou Y, Pandit S, Huang J, Li H, Yin CY, et al. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell. 2013; 153(May 9, 2013):855-868. doi: 10. 1016/j.cell.2013.04.028 PMID: 23663783
50. Martinez-Contreras R, Fisette JF, Nasim FU, Madden R, Cordeau M, Chabot B. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol. 2006; 4(2):e21. PMID: 16396608
51. Levine M. Paused RNA polymerase II as a developmental checkpoint. Cell. 2011; 145(4):502-511. doi: 10.1016/j.cell.2011.04.021 PMID: 21565610
52. Barboric M, Lenasi T, Chen H, Johansen EB, Guo S, Peterlin BM. 7SK snRNP/P-TEFb couples transcription elongation with alternative splicing and is essential for vertebrate development. Proc Natl Acad Sci U S A. 2009; 106(19):7798-7803. doi: 10.1073/pnas.0903188106 PMID: 19416841