Transcription factors mediate the enzymatic disassembly of promoter-bound 7sk snrnp to locally recruit p-tefb for transcription elongation

Cell Reports

Volumn 5, Issue 5, 2013, Pages 1256-1268

  McNamara, RyanP ^a   McCann, JenniferL ^a   Gudipaty, Swapna Aravind ^a   D'Orso, Iván ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PP2CGAMMA PROTEIN; PPM1G PROTEIN; REGULATOR PROTEIN; RNA POLYMERASE II; SMALL NUCLEAR RIBONUCLEOPROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION ELONGATION FACTOR B; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; GENE ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPHOSPHORYLATION; TRANSCRIPTION ELONGATION;

HEK293 CELLS; HELA CELLS; HUMANS; NF-KAPPA B; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS, SMALL NUCLEAR; TRANSCRIPTION ELONGATION, GENETIC;

EID: 84890140408     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.11.003     Document Type: Article

References (49)

1. Allemand E., Hastings M.L., Murray M.V., Myers M.P., Krainer A.R. Alternative splicing regulation by interaction of phosphatase PP2Cgamma with nucleic acid-binding protein YB-1. Nat. Struct. Mol. Biol. 2007, 14:630-638.
2. Amir-Zilberstein L., Ainbinder E., Toube L., Yamaguchi Y., Handa H., Dikstein R. Differential regulation of NF-kappaB by elongation factors is determined by core promoter type. Mol. Cell. Biol. 2007, 27:5246-5259.
3. Ammosova T., Washington K., Debebe Z., Brady J., Nekhai S. Dephosphorylation of CDK9 by protein phosphatase 2A and protein phosphatase-1 in Tat-activated HIV-1 transcription. Retrovirology 2005, 2:47.
4. Barboric M., Lenasi T. Kick-sTARting HIV-1 transcription elongation by 7SK snRNP deporTATion. Nat. Struct. Mol. Biol. 2010, 17:928-930.
5. Barboric M., Nissen R.M., Kanazawa S., Jabrane-Ferrat N., Peterlin B.M. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 2001, 8:327-337.
6. Barboric M., Yik J.H., Czudnochowski N., Yang Z., Chen R., Contreras X., Geyer M., Matija Peterlin B., Zhou Q. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res. 2007, 35:2003-2012.
7. Barkett M., Gilmore T.D. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene 1999, 18:6910-6924.
8. Baumli S., Hole A.J., Wang L.Z., Noble M.E., Endicott J.A. The CDK9 tail determines the reaction pathway of positive transcription elongation factor b. Structure 2012, 20:1788-1795.
9. Chen R., Yang Z., Zhou Q. Phosphorylated positive transcription elongation factor b (P-TEFb) is tagged for inhibition through association with 7SK snRNA. J.Biol. Chem. 2004, 279:4153-4160.
10. Chen R., Liu M., Li H., Xue Y., Ramey W.N., He N., Ai N., Luo H., Zhu Y., Zhou N., Zhou Q. PP2B and PP1α cooperatively disrupt 7SK snRNP to release P-TEFb for transcription in response to Ca2+ signaling. Genes Dev. 2008, 22:1356-1368.
11. Core L.J., Lis J.T. Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 2008, 319:1791-1792.
12. D'Orso I., Frankel A.D. RNA-mediated displacement of an inhibitory snRNP complex activates transcription elongation. Nat. Struct. Mol. Biol. 2010, 17:815-821.
13. D'Orso I., Jang G.M., Pastuszak A.W., Faust T.B., Quezada E., Booth D.S., Frankel A.D. Transition step during assembly of HIV Tat:P-TEFb transcription complexes and transfer to TAR RNA. Mol. Cell. Biol. 2012, 32:4780-4793.
14. Das A.K., Helps N.R., Cohen P.T., Barford D. Crystal structure of the protein serine/threonine phosphatase 2C at 2.0 A resolution. EMBO J. 1996, 15:6798-6809.
15. Faust T., Frankel A., D'Orso I. Transcription control by long non-coding RNAs. Transcription 2012, 3:78-86.
16. Francastel C., Schübeler D., Martin D.I., Groudine M. Nuclear compartmentalization and gene activity. Nat. Rev. Mol. Cell Biol. 2000, 1:137-143.
17. Garber M.E., Mayall T.P., Suess E.M., Meisenhelder J., Thompson N.E., Jones K.A. CDK9 autophosphorylation regulates high-affinity binding of the human immunodeficiency virus type 1 tat-P-TEFb complex to TAR RNA. Mol. Cell. Biol. 2000, 20:6958-6969.
18. Ghosh S., Karin M. Missing pieces in the NF-kappaB puzzle. Cell 2002, 109(Suppl):S81-S96.
19. Gomes N.P., Bjerke G., Llorente B., Szostek S.A., Emerson B.M., Espinosa J.M. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 2006, 20:601-612.
20. Hager G.L., McNally J.G., Misteli T. Transcription dynamics. Mol. Cell 2009, 35:741-753.
21. Hargreaves D.C., Horng T., Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145.
22. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., Poitras C., Thérien C., Bergeron D., Bourassa S., Greenblatt J., 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, 27:262-274.
23. Ji X., Zhou Y., Pandit S., Huang J., Li H., Lin C.Y., Xiao R., Burge C.B., Fu X.D. SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 2013, 153:855-868.
24. Kim Y.K., Bourgeois C.F., Isel C., Churcher M.J., Karn J. Phosphorylation of the RNA polymerase II carboxyl-terminal domain by CDK9 is directly responsible for human immunodeficiency virus type 1 Tat-activated transcriptional elongation. Mol. Cell. Biol. 2002, 22:4622-4637.
25. Kim D.E., Chivian D., Baker D. Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res. 2004, 32(Web Server issue):W526-W531.
26. Kim Y.K., Mbonye U., Hokello J., Karn J. T-cell receptor signaling enhances transcriptional elongation from latent HIV proviruses by activating P-TEFb through an ERK-dependent pathway. J.Mol. Biol. 2011, 410:896-916.
27. Krueger B.J., Jeronimo C., Roy B.B., Bouchard A., Barrandon C., Byers S.A., Searcey C.E., Cooper J.J., Bensaude O., Cohen E.A., 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, 36:2219-2229.
28. Krueger B.J., Varzavand K., Cooper J.J., Price D.H. The mechanism of release of P-TEFb and HEXIM1 from the 7SK snRNP by viral and cellular activators includes a conformational change in 7SK. PLoS ONE 2010, 5:e12335.
29. Li Q., Price J.P., Byers S.A., Cheng D., Peng J., Price D.H. Analysis of the large inactive P-TEFb complex indicates that it contains one 7SK molecule, a dimer of HEXIM1 or HEXIM2, and two P-TEFb molecules containing Cdk9 phosphorylated at threonine 186. J.Biol. Chem. 2005, 280:28819-28826.
30. Lis J.T., Mason P., Peng J., Price D.H., Werner J. P-TEFb kinase recruitment and function at heat shock loci. Genes Dev. 2000, 14:792-803.
31. Luecke H.F., Yamamoto K.R. The glucocorticoid receptor blocks P-TEFb recruitment by NFkappaB to effect promoter-specific transcriptional repression. Genes Dev. 2005, 19:1116-1127.
32. Mancebo H.S., Lee G., Flygare J., Tomassini J., Luu P., Zhu Y., Peng J., Blau C., Hazuda D., Price D., Flores O. P-TEFb kinase is required for HIV Tat transcriptional activation invivo and invitro. Genes Dev. 1997, 11:2633-2644.
33. Marshall N.F., Price D.H. Control of formation of two distinct classes of RNA polymerase II elongation complexes. Mol. Cell. Biol. 1992, 12:2078-2090.
34. Muniz L., Egloff S., Ughy B., Jády B.E., Kiss T. Controlling cellular P-TEFb activity by the HIV-1 transcriptional transactivator Tat. PLoS Pathog. 2010, 6:e1001152.
35. Nissen R.M., Yamamoto K.R. The glucocorticoid receptor inhibits NFkappaB by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev. 2000, 14:2314-2329.
36. Ott M., Geyer M., Zhou Q. The control of HIV transcription: keeping RNA polymerase II on track. Cell Host Microbe 2011, 10:426-435.
37. Peterlin B.M., Price D.H. Controlling the elongation phase of transcription with P-TEFb. Mol. Cell 2006, 23:297-305.
38. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J.Comput. Chem. 2004, 25:1605-1612.
39. Rahl P.B., Lin C.Y., Seila A.C., Flynn R.A., McCuine S., Burge C.B., Sharp P.A., Young R.A. c-Myc regulates transcriptional pause release. Cell 2010, 141:432-445.
40. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
41. Sedore S.C., Byers S.A., Biglione S., Price J.P., Maury W.J., Price D.H. Manipulation of P-TEFb control machinery by HIV: recruitment of P-TEFb from the large form by Tat and binding of HEXIM1 to TAR. Nucleic Acids Res. 2007, 35:4347-4358.
42. Sidoti-de Fraisse C., Rincheval V., Risler Y., Mignotte B., Vayssière J.L. TNF-α activates at least two apoptotic signaling cascades. Oncogene 1998, 17:1639-1651.
43. Smith E., Shilatifard A. Transcriptional elongation checkpoint control in development and disease. Genes Dev. 2013, 27:1079-1088.
44. Sobhian B., Laguette N., Yatim A., Nakamura M., Levy Y., Kiernan R., Benkirane M. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol. Cell 2010, 38:439-451.
45. Tahirov T.H., Babayeva N.D., Varzavand K., Cooper J.J., Sedore S.C., Price D.H. Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature 2010, 465:747-751.
46. Wang Y., Dow E.C., Liang Y.Y., Ramakrishnan R., Liu H., Sung T.L., Lin X., Rice A.P. Phosphatase PPM1A regulates phosphorylation of Thr-186 in the Cdk9 T-loop. J.Biol. Chem. 2008, 283:33578-33584.
47. Wei P., Garber M.E., Fang S.M., Fischer W.H., Jones K.A. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 1998, 92:451-462.
48. Yamaguchi Y., Takagi T., Wada T., Yano K., Furuya A., Sugimoto S., Hasegawa J., Handa H. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 1999, 97:41-51.
49. Zhou Q., Li T., Price D.H. RNA polymerase II elongation control. Annu. Rev. Biochem. 2012, 81:119-143.