Identification of novel CDK9 and Cyclin T1-associated protein complexes (CCAPs) whose siRNA depletion enhances HIV-1 Tat function

Retrovirology

Volumn 9, Issue , 2012, Pages

  Ramakrishnan, Rajesh ^a   Liu, Hongbing ^a   Donahue, Hart ^a   Malovannaya, Anna ^a   Qin, Jun ^a   Rice, Andrew P ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIBODY; CYCLIN DEPENDENT KINASE 9; CYCLIN T1; F BOX PROTEIN; FBXO11 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCLONAL ANTIBODY CD28; PHOSPHOPROTEIN PHOSPHATASE 1; PPP1R10 PROTEIN; PROTEIN; RNA; SMALL INTERFERING RNA; THYROID TRANSCRIPTION FACTOR 2; TOX3 PROTEIN; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; WDR82 PROTEIN;

ARTICLE; GENE EXPRESSION; HELA CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LEUKEMIA CELL LINE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SUBUNIT; PROVIRUS; VIRUS GENE;

CYCLIN T; CYCLIN-DEPENDENT KINASE 9; GENE EXPRESSION REGULATION, VIRAL; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MULTIPROTEIN COMPLEXES; RNA, SMALL INTERFERING; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC; VIRULENCE FACTORS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84867902019     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-9-90     Document Type: Article

References (74)

1. Karn J, Stoltzfus CM. Transcriptional and Posttranscriptional Regulation of HIV-1 Gene Expression. Cold Spring Harb Perspect Med 2012, 2:a006916. 3281586, 22355797.
2. He N, Zhou Q. New Insights into the Control of HIV-1 Transcription: When Tat Meets the 7SK snRNP and Super Elongation Complex (SEC). J Neuroimmune Pharmacol 2011, 6:260-8. 10.1007/s11481-011-9267-6, 3087102, 21360054.
3. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006, 23:297-305. 10.1016/j.molcel.2006.06.014, 16885020.
4. Ott M, Geyer M, Zhou Q. The Control of HIV Transcription: Keeping RNA Polymerase II on Track. Cell Host Microbe 2011, 10:426-435. 10.1016/j.chom.2011.11.002, 22100159.
5. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007, 130:77-88. 10.1016/j.cell.2007.05.042, 3200295, 17632057.
6. Glover-Cutter K, Kim S, Espinosa J, Bentley DL. RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat Struct Mol Biol 2008, 15:71-78. 10.1038/nsmb1352, 2836588, 18157150.
7. Jang MK, Mochizuki K, Zhou M, Jeong HS, Brady JN, Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription. Mol Cell 2005, 19:523-534. 10.1016/j.molcel.2005.06.027, 16109376.
8. Yang Z, Yik JH, Chen R, He N, Jang MK, Ozato K, Zhou Q. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 2005, 19:535-545. 10.1016/j.molcel.2005.06.029, 16109377.
9. Hargreaves DC, Horng T, Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 2009, 138:129-145. 10.1016/j.cell.2009.05.047, 2828818, 19596240.
10. Barboric M, Nissen RM, Kanazawa S, Jabrane-Ferrat N, Peterlin BM. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol Cell 2001, 8:327-337. 10.1016/S1097-2765(01)00314-8, 11545735.
11. Eberhardy SR, Farnham PJ. Myc recruits P-TEFb to mediate the final step in the transcriptional activation of the cad promoter. J Biol Chem 2002, 277:40156-40162. 10.1074/jbc.M207441200, 12177005.
12. Nojima M, Huang Y, Tyagi M, Kao HY, Fujinaga K. The positive transcription elongation factor b is an essential cofactor for the activation of transcription by myocyte enhancer factor 2. J Mol Biol 2008, 382:275-287. 10.1016/j.jmb.2008.07.017, 18662700.
13. Smith E, Lin C, Shilatifard A. The super elongation complex (SEC) and MLL in development and disease. Genes Dev 2011, 25:661-672. 10.1101/gad.2015411, 3070929, 21460034.
14. Dow EC, Liu H, Rice AP. T-loop phosphorylated Cdk9 localizes to nuclear speckle domains which may serve as sites of active P-TEFb function and exchange between the Brd4 and 7SK/HEXIM1 regulatory complexes. J Cell Physiol 2010, 224:84-93. 2888102, 20201073.
15. Yik JH, Chen R, Nishimura R, Jennings JL, Link AJ, Zhou Q. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell 2003, 12:971-982. 10.1016/S1097-2765(03)00388-5, 14580347.
16. Tahirov TH, Babayeva ND, Varzavand K, Cooper JJ, Sedore SC, Price DH. Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature 2010, 465:747-751. 10.1038/nature09131, 2885016, 20535204.
17. Bisgrove DA, Mahmoudi T, Henklein P, Verdin E. Conserved P-TEFb-interacting domain of BRD4 inhibits HIV transcription. Proc Natl Acad Sci USA 2007, 104:13690-13695. 10.1073/pnas.0705053104, 1959443, 17690245.
18. Schulte A, Czudnochowski N, Barboric M, Schonichen A, Blazek D, Peterlin BM, Geyer M. Identification of a cyclin T-binding domain in Hexim1 and biochemical analysis of its binding competition with HIV-1 Tat. J Biol Chem 2005, 280:24968-24977. 10.1074/jbc.M501431200, 15855166.
19. Barboric M, Yik JH, Czudnochowski N, Yang Z, Chen R, Contreras X, Geyer M, Matija PB, Zhou Q. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res 2007, 35:2003-12. 10.1093/nar/gkm063, 1874611, 17341462.
20. Sedore SC, Byers SA, Biglione S, Price JP, Maury WJ, Price DH. 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. 10.1093/nar/gkm443, 1935001, 17576689.
21. He N, Liu M, Hsu J, Xue Y, Chou S, Burlingame A, Krogan NJ, Alber T, Zhou Q. HIV-1 Tat and host AFF4 recruit two transcription elongation factors into a bifunctional complex for coordinated activation of HIV-1 transcription. Mol Cell 2010, 38:428-438. 10.1016/j.molcel.2010.04.013, 3085314, 20471948.
22. 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. 10.1016/j.molcel.2010.04.012, 20471949.
23. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998, 92:291-294. 10.1016/S0092-8674(00)80922-8, 9476889.
24. O'Malley BW, Qin J, Lanz RB. Cracking the coregulator codes. Curr Opin Cell Biol 2008, 20:310-315. 10.1016/j.ceb.2008.04.005, 18499426.
25. Malovannaya A, Lanz RB, Jung SY, Bulynko Y, Le NT, Chan DW, Ding C, Shi Y, Yucer N, Krenciute G, et al. Analysis of the human endogenous coregulator complexome. Cell 2011, 145:787-799. 10.1016/j.cell.2011.05.006, 3131083, 21620140.
26. Michels AA, Bensaude O. RNA-driven cyclin-dependent kinase regulation: when CDK9/cyclin T subunits of P-TEFb meet their ribonucleoprotein partners. Biotechnol J 2008, 3:1022-1032. 10.1002/biot.200800104, 18655042.
27. Benedikt A, Baltruschat S, Scholz B, Bursen A, Arrey TN, Meyer B, Varagnolo L, Muller AM, Karas M, Dingermann T, et al. The leukemogenic AF4-MLL fusion protein causes P-TEFb kinase activation and altered epigenetic signatures. Leukemia 2011, 25:135-144. 10.1038/leu.2010.249, 21030982.
28. Bushman FD, Malani N, Fernandes J, D'Orso I, Cagney G, Diamond TL, Zhou H, Hazuda DJ, Espeseth AS, Konig R, et al. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog 2009, 5:e1000437. 10.1371/journal.ppat.1000437, 2682202, 19478882.
29. Duan S, Cermak L, Pagan JK, Rossi M, Martinengo C, di Celle PF, Chapuy B, Shipp M, Chiarle R, Pagano M. FBXO11 targets BCL6 for degradation and is inactivated in diffuse large B-cell lymphomas. Nature 2012, 481:90-93. 3344385, 22113614.
30. Abida WM, Nikolaev A, Zhao W, Zhang W, Gu W. FBXO11 promotes the Neddylation of p53 and inhibits its transcriptional activity. J Biol Chem 2007, 282:1797-1804.
31. Landsverk HB, Mora-Bermudez F, Landsverk OJ, Hasvold G, Naderi S, Bakke O, Ellenberg J, Collas P, Syljuasen RG, Kuntziger T. The protein phosphatase 1 regulator PNUTS is a new component of the DNA damage response. EMBO Rep 2010, 11:868-875. 10.1038/embor.2010.134, 2966950, 20890310.
32. Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A. Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol 2008, 28:7337-7344. 10.1128/MCB.00976-08, 2593441, 18838538.
33. Dittmer S, Kovacs Z, Yuan SH, Siszler G, Kogl M, Summer H, Geerts A, Golz S, Shioda T, Methner A. TOX3 is a neuronal survival factor that induces transcription depending on the presence of CITED1 or phosphorylated CREB in the transcriptionally active complex. J Cell Sci 2011, 124:252-260. 10.1242/jcs.068759, 21172805.
34. Frosst P, Guan T, Subauste C, Hahn K, Gerace L. Tpr is localized within the nuclear basket of the pore complex and has a role in nuclear protein export. J Cell Biol 2002, 156:617-630. 10.1083/jcb.200106046, 2174070, 11839768.
35. Liu M, Xie Z, Price DH. A human RNA polymerase II transcription termination factor is a SWI2/SNF2 family member. J Biol Chem 1998, 273:25541-25544. 10.1074/jbc.273.40.25541, 9748214.
36. Jiang Y, Liu M, Spencer CA, Price DH. Involvement of transcription termination factor 2 in mitotic repression of transcription elongation. Mol Cell 2004, 14:375-385. 10.1016/S1097-2765(04)00234-5, 15125840.
37. Kanamori M, Seki M, Yoshimura A, Tsurimoto T, Tada S, Enomoto T. Werner interacting protein 1 promotes binding of Werner protein to template-primer DNA. Biol Pharm Bull 2011, 34:1314-1318. 10.1248/bpb.34.1314, 21804224.
38. Balajee AS, Machwe A, May A, Gray MD, Oshima J, Martin GM, Nehlin JO, Brosh R, Orren DK, Bohr VA. The Werner syndrome protein is involved in RNA polymerase II transcription. Mol Biol Cell 1999, 10:2655-2668. 25497, 10436020.
39. Comai L, Li B. The Werner syndrome protein at the crossroads of DNA repair and apoptosis. Mech Ageing Dev 2004, 125:521-528. 10.1016/j.mad.2004.06.004, 15336909.
40. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 1998, 72:2855-2864. 109730, 9525605.
41. Rice AP, Carlotti F. Mutational analysis of the conserved cysteine-rich region of the human immunodeficiency virus type 1 Tat protein. J Virol 1990, 64:1864-1868. 249332, 2181156.
42. Pearson R, Kim YK, Hokello J, Lassen K, Friedman J, Tyagi M, Karn J. Epigenetic silencing of human immunodeficiency virus (HIV) transcription by formation of restrictive chromatin structures at the viral long terminal repeat drives the progressive entry of HIV into latency. J Virol 2008, 82:12291-12303. 10.1128/JVI.01383-08, 2593349, 18829756.
43. Kornblihtt AR, De la MM, Fededa JP, Munoz MJ, Nogues G. Multiple links between transcription and splicing. RNA 2004, 10:1489-1498. 10.1261/rna.7100104, 1370635, 15383674.
44. Han J, Xiong J, Wang D, Fu XD. Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol 2011, 21:336-343. 10.1016/j.tcb.2011.03.003, 21514162.
45. Dehart JL, Andersen JL, Zimmerman ES, Ardon O, An DS, Blackett J, Kim B, Planelles V. The ataxia telangiectasia-mutated and Rad3-related protein is dispensable for retroviral integration. J Virol 2005, 79:1389-1396. 10.1128/JVI.79.3.1389-1396.2005, 544104, 15650165.
46. Mahmoudi T, Parra M, Vries RG, Kauder SE, Verrijzer CP, Ott M, Verdin E. The SWI/SNF Chromatin-remodeling Complex Is a Cofactor for Tat Transactivation of the HIV Promoter. J Biol Chem 2006, 281:19960-19968. 10.1074/jbc.M603336200, 16687403.
47. Agbottah E, Deng L, Dannenberg LO, Pumfery A, Kashanchi F. Effect of SWI/SNF chromatin remodeling complex on HIV-1 Tat activated transcription. Retrovirology 2006, 3:48. 10.1186/1742-4690-3-48, 1570494, 16893449.
48. Lee JH, You J, Dobrota E, Skalnik DG. Identification and characterization of a novel human PP1 phosphatase complex. J Biol Chem 2010, 285:24466-24476. 10.1074/jbc.M110.109801, 2915683, 20516061.
49. Brannan K, Kim H, Erickson B, Glover-Cutter K, Kim S, Fong N, Kiemele L, Hansen K, Davis R, Lykke-Andersen J, et al. mRNA decapping factors and the exonuclease Xrn2 function in widespread premature termination of RNA polymerase II transcription. Mol Cell 2012, 46:311-324. 10.1016/j.molcel.2012.03.006, 22483619.
50. Coyle JH, Bor YC, Rekosh D, Hammarskjold ML. The Tpr protein regulates export of mRNAs with retained introns that traffic through the Nxf1 pathway. RNA 2011, 17:1344-1356. 10.1261/rna.2616111, 3138570, 21613532.
51. Peng J, Zhu Y, Milton JT, Price DH. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev 1998, 12:755-762. 10.1101/gad.12.5.755, 316581, 9499409.
52. Shore SM, Byers SA, Maury W, Price DH. Identification of a novel isoform of Cdk9. Gene 2003, 307:175-182.
53. Kohoutek J, Li Q, Blazek D, Luo Z, Jiang H, Peterlin BM. Cyclin T2 is essential for mouse embryogenesis. Mol Cell Biol 2009, 29:3280-3285. 10.1128/MCB.00172-09, 2698739, 19364821.
54. Ramakrishnan R, Yu W, Rice AP. Limited redundancy in genes regulated by Cyclin T2 and Cyclin T1. BMC Res Notes 2011, 4:260. 10.1186/1756-0500-4-260, 3160394, 21791050.
55. Shore SM, Byers SA, Dent P, Price DH. Characterization of Cdk9(55) and differential regulation of two Cdk9 isoforms. Gene 2005, 350:51-58. 10.1016/j.gene.2005.01.015, 15780980.
56. Liu H, Herrmann CH. Differential localization and expression of the Cdk9 42k and 55k isoforms. J Cell Physiol 2005, 203:251-260. 10.1002/jcp.20224, 15452830.
57. Rice AP, Herrmann CH. Regulation of TAK/P-TEFb in CD4+ T lymphocytes and macrophages. Curr HIV Res 2003, 1:395-404. 10.2174/1570162033485159, 15049426.
58. Tyagi M, Pearson RJ, Karn J. Establishment of HIV latency in primary CD4+ cells is due to epigenetic transcriptional silencing and P-TEFb restriction. J Virol 2010, 84:6425-6437. 10.1128/JVI.01519-09, 2903277, 20410271.
59. Chiang K, Sung TL, Rice AP. Regulation of Cyclin T1 and HIV-1 Replication by MicroRNAs in Resting CD4+ T Lymphocytes. J Virol 2012, 86:3244-3252. 10.1128/JVI.05065-11, 3302325, 22205749.
60. Herrmann CH, Carroll RG, Wei P, Jones KA, Rice AP. Tat-associated kinase, TAK, activity is regulated by distinct mechanisms in peripheral blood lymphocytes and promonocytic cell lines. J Virol 1998, 72:9881-9888. 110500, 9811724.
61. Garriga J, Peng J, Parreno M, Price DH, Henderson EE, Grana X. Upregulation of cyclin T1/CDK9 complexes during T cell activation. Oncogene 1998, 17:3093-3102. 10.1038/sj.onc.1202548, 9872325.
62. Marshall RM, Salerno D, Garriga J, Grana X. Cyclin T1 expression is regulated by multiple signaling pathways and mechanisms during activation of human peripheral blood lymphocytes. J Immunol 2005, 175:6402-6411.
63. Ghose R, Liou LY, Herrmann CH, Rice AP. Induction of TAK (cyclin T1/P-TEFb) in purified resting CD4(+) T lymphocytes by combination of cytokines. J Virol 2001, 75:11336-11343. 10.1128/JVI.75.23.11336-11343.2001, 114719, 11689614.
64. Ramakrishnan R, Dow EC, Rice AP. Characterization of Cdk9 T-loop phosphorylation in resting and activated CD4(+) T lymphocytes. J Leukoc Biol 2009, 86:1345-1350. 10.1189/jlb.0509309, 2780919, 19741158.
65. Haaland RE, Herrmann CH, Rice AP. Increased association of 7SK snRNA with Tat cofactor P-TEFb following activation of peripheral blood lymphocytes. AIDS 2003, 17:2429-2436. 10.1097/00002030-200311210-00004, 14600513.
66. Haaland RE, Herrmann CH, Rice AP. siRNA depletion of 7SK snRNA induces apoptosis but does not affect expression of the HIV-1 LTR or P-TEFb-dependent cellular genes. J Cell Physiol 2005, 205:463-470. 10.1002/jcp.20528, 16152622.
67. Sung TL, Rice AP. miR-198 inhibits HIV-1 gene expression and replication in monocytes and its mechanism of action appears to involve repression of cyclin T1. PLoS Pathog 2009, 5:e1000263. 10.1371/journal.ppat.1000263, 2607557, 19148268.
68. Dong C, Kwas C, Wu L. Transcriptional restriction of human immunodeficiency virus type 1 gene expression in undifferentiated primary monocytes. J Virol 2009, 83:3518-3527. 10.1128/JVI.02665-08, 2663290, 19211771.
69. Liou LY, Herrmann CH, Rice AP. Transient induction of cyclin T1 during human macrophage differentiation regulates human immunodeficiency virus type 1 Tat transactivation function. J Virol 2002, 76:10579-10587. 10.1128/JVI.76.21.10579-10587.2002, 136632, 12368300.
70. Liou LY, Herrmann CH, Rice AP. Human immunodeficiency virus type 1 infection induces cyclin T1 expression in macrophages. J Virol 2004, 78:8114-8119. 10.1128/JVI.78.15.8114-8119.2004, 446126, 15254183.
71. Liou LY, Haaland RE, Herrmann CH, Rice AP. Cyclin T1 but not cyclin T2a is induced by a post-transcriptional mechanism in PAMP-activated monocyte-derived macrophages. J Leukoc Biol 2006, 79:388-396.
72. Roshal M, Kim B, Zhu Y, Nghiem P, Planelles V. Activation of the ATR-mediated DNA damage response by the HIV-1 viral protein R. J Biol Chem 2003, 278:25879-25886. 10.1074/jbc.M303948200, 12738771.
73. Abramoff MD, Magalhaes PJ, Ram SJ. Image Processing with ImageJ. Biophotonics International 2004, 11:36-42.
74. Budhiraja S, Ramakrishnan R, Rice AP. Phosphatase PPM1A negatively regulates P-TEFb function in resting CD4T+ T cells and inhibits HIV-1 gene expression. Retrovirology 2012, 9:52. 10.1186/1742-4690-9-52, 3406988, 22727189.