7SK RNA, a non-coding RNA regulating P-TEFb, a general transcription factor

RNA Biology

Volumn 6, Issue 2, 2009, Pages 122-128

  Diribarne, Gaelle ^a   Bensaude, Olivier ^a,b  

^a CNRS   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

7SK RNA; CDK9; Cyclin T1; HEXIM; LARP7; MePCE; P TEFb; Transcription

Indexed keywords

7SK RNA; CYCLIN T1; DNA DIRECTED RNA POLYMERASE III; NUCLEAR RNA; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN LARP7; PROTEIN SUBUNIT; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ADENYLATION; GENE CONTROL; GENE FUNCTION; GENE MAPPING; GENETIC CONSERVATION; GENETIC TRAIT; GENETIC TRANSCRIPTION; HEART VENTRICLE HYPERTROPHY; HUMAN; METHYLATION; PROTEIN FOLDING; REVIEW; RNA BINDING; RNA SYNTHESIS;

ANNELIDA; HEXAPODA; MOLLUSCA; VERTEBRATA;

EID: 66449089824     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.6.2.8115     Document Type: Review

References (93)

1. Zieve G, Penman S. Small RNA species of the HeLa cell: metabolism and subcellular localization. Cell 1976; 8:17-19
2. Reddy R, Henning D, Subrahmanyam CS, Busch H. Primary and secondary structure of 7-3 (K) RNA of Novikoff hepatoma. J Biol Chem 1984; 259:12265-12270 (Pubitemid 14019767)
3. Ullu E, Melli M. Cloning and characterization of cDNA copies of the 7S RNAs of HeLa cells. Nucleic Acids Res 1982; 10:2209-2223
4. Gurney TJ, Eliceiri GL. Intracellular distribution of low molecular weight RNA species in HeLa cells. J Cell Biol 1980; 87:398-403. (Pubitemid 11204334)
5. Matera AG, Ward DC. Nucleoplasmic organization of small nuclear ribonucleoproteins in cultured human cells. J Cell Biol 1993; 121:715-727 (Pubitemid 23143534)
6. Robb GB, Brown KM, Khurana J, Rana TM. Specific and potent RNAi in the nucleus of human cells. Nat Struct Mol Biol 2005; 12:133-137
7. Nguyen VT, Kiss T, Michels AA, Bensaude O. 7SK snRNA binds to and inhibits the activity of Cdk9/cyclin T complexes. Nature 2001; 414:322-325 (Pubitemid 33097810)
8. Yang Z, Zhu Q, Luo K, Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 2001; 414:317-322 (Pubitemid 33097809)
9. 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 (Pubitemid 37352789)
10. Michels AA, Nguyen VT, Fraldi A, Labas V, Edwards M, Bonnet F, et al. MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription- dependent manner. Mol Cell Biol 2003; 23:4859-4869 (Pubitemid 36793332)
11. Michels AA, Fraldi A, Li Q, Adamson TE, Bonnet F, Nguyen VT, et al. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J 2004; 23:2608-2619 (Pubitemid 38988232)
12. Peterlin BM, Price DH. Controlling the Elongation Phase of Transcription with P-TEFb. Mol Cell 2006; 23:297-305. (Pubitemid 44128850)
13. Chapman RD, Heidemann M, Hintermair C, DE. Molecular evolution of the RNA polymerase II CTD. Trends Genet 2008; 24:289-296
14. Egloff S, Murphy S. Cracking the RNA polymerase II CTD code. Trends Genet 2008; 24:630-642
15. Kulkarni PA, Sano M, Schneider MD. Phosphorylation of RNA polymerase II in cardiac hypertrophy: cell enlargement signals converge on cyclin T/Cdk9. Recent Prog Horm Res 2004; 59:125-139 (Pubitemid 41327149)
16. Biglione S, Byers SA, Price JP, Nguyen VT, Bensaude O, Price DH, et al. Inhibition of HIV-1 replication by P-TEFb inhibitors DRB, seliciclib and flavopiridol correlates with release of free P-TEFb from the large, inactive form of the complex. Retrovirology 2007; 4:47. (Pubitemid 47277974)
17. Zhou Q, Yik JH. The Yin and Yang of P-TEFb regulation: implications for human immunodeficiency virus gene expression and global control of cell growth and differentiation. Microbiol Mol Biol Rev 2006; 70:646-659 (Pubitemid 44484688)
18. Barrandon C, Spiluttini B, Bensaude O. Non-coding RNAs regulating the transcriptional machinery. Biol Cell 2008; 100:83-95.
19. 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
20. Murphy S, Altruda F, Ullu E, Tripodi M, Silengo L, Melli M. DNA sequences complementary to human 7 SK RNA show structural similarities to the short mobile elements of the mammalian genome. J Mol Biol 1984; 177:575-590 (Pubitemid 16218905)
21. Humphries P, Russell SE, McWilliam P, McQuaid S, Pearson C, Humphries MM. Observations on the structure of two human 7SK pseudogenes and on homologous transcripts in vertebrate species. Biochem J 1987; 245:281-284
22. Suh D, Yuan Y, Henning D, Reddy R. Secondary structure of 7SK and 7-2 small RNAs. Possible origin of some 7SK pseudogenes from cDNA formed through self-priming by 7SK RNA. Eur J Biochem 1989; 186:221-226 (Pubitemid 20015147)
23. Murphy S, Tripodi M, Melli M. A sequence upstream from the coding region is required for the transcription of the 7SK RNA genes. Nucleic Acids Res 1986; 14:9243-9260 (Pubitemid 17220800)
24. Kleinert H, Bredow S, Benecke BJ. Expression of a human 7S K RNA gene in vivo requires a novel pol III upstream element. EMBO J 1990; 9:711-718 (Pubitemid 20080603)
25. Boyd DC, Turner PC, Watkins NJ, Gerster T, Murphy S. Functional Redundancy of Promoter Elements Ensures Efficient Transcription of the Human 7SK Gene in vivo. J Mol Biol 1995; 253:677-690
26. Murphy S, Pierani A, Scheidereit C, Melli M, Roeder RG. Purified octamer binding transcription factors stimulate RNA polymerase III-mediated transcription of the 7SK RNA gene. Cell 1989; 59:1071-1080 (Pubitemid 20024618)
27. Schaub M, Myslinski E, Schuster C, Krol A, Carbon P. Staf, a promiscuous activator for enhanced transcription by RNA polymerases II and III. EMBO J 1997; 16:173-181 (Pubitemid 27032860)
28. Yoon JB, Murphy S, Bai L, Wang Z, Roeder RG. Proximal sequence element-binding transcription factor (PTF) is a multisubunit complex required for transcription of both RNA polymerase II- and RNA polymerase III-dependent small nuclear RNA genes. Mol Cell Biol 1995; 15:2019-2027
29. Koper-Emde D, Herrmann L, Sandrock B, Benecke BJ. RNA interference by small hairpin RNAs synthesised under control of the human 7S K RNA promoter. Biol Chem 2004; 385:791-794 (Pubitemid 39335301)
30. Bannister SC, Wise TG, Cahill DM, Doran TJ. Comparison of chicken 7SK and U6 RNA polymerase III promoters for short hairpin RNA expression. BMC Biotechnol 2007; 19:7-79.
31. ter Brake O, 't Hooft K, Liu YP, Centlivre M, von Eije KJ, BB. Lentiviral vector design for multiple shRNA expression and durable HIV-1 inhibition. Mol Ther 2008; 16:557-564
32. Gupta S, Busch RK, Singh R, Reddy R. Characterization of U6 small nuclear RNA cap-specific antibodies. Identification of gamma-monomethyl-GTP cap structure in 7SK and several other human small RNAs. J Biol Chem 1990; 265:19137-19142 (Pubitemid 20378582)
33. Shumyatsky GP, Tillib SV, Kramerov DA. B2 RNA and 7SK RNA, RNA polymerase III transcripts, have a cap-like structure at their 5′ end. Nucleic Acids Res 1990; 18:6347-6351 (Pubitemid 20379185)
34. Shumyatsky G, Wright D, RR. Methylphosphate cap structure increases the stability of 7SK, B2 and U6 small RNAs in Xenopus oocytes. Nucleic Acids Res 1993; 21:4756-4761
35. Chen Y, Perumal K, Reddy R. Inhibition of translation of mRNAs containing gammamonomethylphosphate cap structure in frog oocytes and in mammalian cells. Gene Expr 2000; 9:133-143 (Pubitemid 32180167)
36. 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; 27:262-274 (Pubitemid 47058308)
37. Sinha KM, Gu J, Chen Y, Reddy R. Adenylation of small RNAs in human cells. J Biol Chem 1998; 273:6853-6859
38. Chen Y, Sinha K, Perumal K, Reddy R. Effect of 3′ terminal adenylic acid residue on the uridylation of human small RNAs in vitro and in frog oocytes. RNA 2000; 6:1277-1288
39. Wassarman DA, Steitz JA. Structural analyses of the 7SK ribonucleoprotein (RNP), the most abundant human small RNP of unknown function. Mol Cell Biol 1991; 11:3432-3445 (Pubitemid 21895730)
40. Gürsoy HC, Koper D, Benecke B-J. The vertebrate 7S K RNA separates hagfish (Myxine glutinosa) and lamprey (Lampetra fluviatilis). J Mol Evol 2000; 50:456-464 (Pubitemid 30429960)
41. Egloff S, Van Herreweghe E, Kiss T. Regulation of polymerase II transcription by 7SK snRNA: two distinct RNA elements direct P-TEFb and HEXIM1 binding. Mol Cell Biol 2006; 26:630-642 (Pubitemid 43089774)
42. Gruber AR, Koper-Emde D, Marz M, Tafer H, Bernhart S, Obernosterer G, et al. Invertebrate 7SK snRNAs. J Mol Evol 2008; 66:107-115
43. Gruber AR, Kilgus C, Mosig A, Hofacker IL, Hennig W, Stadler PF. Arthropod 7SK RNA. Mol Biol Evol 2008; 25:1923-1930
44. 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; 26:3570-3580 (Pubitemid 47236869)
45. He N, Jahchan NS, Hong E, Li Q, Bayfield MA, Maraia RJ, et al. A La-Related Protein Modulates 7SK snRNP Integrity to Suppress P-TEFb-Dependent Transcriptional Elongation and Tumorigenesis. Mol Cell 2008; 29:1-12.
46. Stefano JE. Purified Lupus antigen La Recognizesan Oligouridylate Stretch Common to the 3′ Termini of RNA polymerase III Transcripts. Cell 1984; 36:145-154
47. Maraia RJ, Bayfield MA. The La protein-RNA complex surfaces. Mol Cell 2006; 21:75-85. (Pubitemid 43099931)
48. Bhattacharya R, Perumal K, Sinha K, Maraia R, Reddy R. Methylphosphate cap structure in small RNAs reduces the affinity of RNAs to La protein. Gene Expr 2002; 10:243-253 (Pubitemid 35315386)
49. Chambers JC, Kurilia MG, Keene JD. Association between the 7 S RNA and the lupus La protein varies among cell types. J Biol Chem 1983:11438-11441
50. Kiss T. Biogenesis of small nuclear RNPs. J Cell Science 2006; 117:5949-5951 (Pubitemid 40123960)
51. 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; 36:2219-2229
52. 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 Reports 2008; 9:569-575
53. Mori Y, Sato F, Selaru FM, Olaru A, Perry K, Kimos MC, et al. Instabilotyping reveals unique mutational spectra in microsatellite-unstable gastric cancers. Cancer Res 2002; 62:3641-3645 (Pubitemid 34728839)
54. Santamaría P, Randsholt NB. Characterization of a region of the X chromosome of Drosophila including multi sex combs (mxc), a Polycomb group gene which also functions as a tumour suppressor. Mol Gen Genet 1995; 246:282-290
55. Cassé C, Giannoni F, Nguyen VT, Dubois M-F, Bensaude O. The transcriptional inhibitors, actinomycin D and a-amanitin, activate the HIV-1 promoter and favor phosphorylation of the RNA polymerase II C-terminal domain. J Biol Chem 1999; 274:16097-16106 (Pubitemid 129526355)
56. Yik JH, Chen R, Pezda AC, Zhou Q. Compensatory contributions of HEXIM1 and HEXIM2 in maintaining the balance of active and inactive P-TEFb complexes for control of transcription. J Biol Chem 2005; 280:16368-16376 (Pubitemid 40616766)
57. Byers SA, Price JP, Cooper JJ, Li Q, Price DH. HEXIM2, A HEXIM1 related protein, regulates P-TEFb through association with 7SK. J Biol Chem 2005; 280:16360-16367
58. Dulac C, AAM, Fraldi A, Bonnet F, Nguyen VT, Napolitano G, et al. Transcription-dependent association of multiple P-TEFb units to a HEXIM multimer. J Biol Chem 2005; 280:30619-30629
59. Li Q, Price JP, Byers SA, Cheng D, Peng J, Price DH. 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 (Pubitemid 41105784)
60. Yik JH, Chen R, Pezda AC, Samford CS, Zhou Q. A human immunodeficiency virus type 1 Tat-like arginine-rich RNA-binding domain is essential for HEXIM1 to inhibit RNA polymerase II transcription through 7SK snRNA-mediated inactivation of P-TEFb. Mol Cell Biol 2004; 24:5094-5105 (Pubitemid 38738148)
61. Schulte A, Czudnochowski N, Barboric M, Schonichen A, Blazek D, Peterlin BM, et al. 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 (Pubitemid 40934589)
62. Barboric M, Kohoutek J, Price JP, Blazek D, Price DH, Peterlin BM. Interplay between 7SK snRNA and oppositely charged regions in HEXIM1 direct the inhibition of P-TEFb. EMBO J 2005; 24:4291-4303 (Pubitemid 41828904)
63. Li Q, Cooper JJ, Altwerger GH, Feldkamp MD, Shea MA, Price DH. HEXIM1 is a promiscuous double-stranded RNA-binding protein and interacts with RNAs in addition to 7SK in cultured cells. Nucleic Acids Res 2007; 35:2503-2512 (Pubitemid 47073665)
64. Dames SA, Schonichen A, Schulte A, Barboric M, Peterlin BM, Grzesiek S, et al. Structure of the Cyclin T binding domain of Hexim1 and molecular basis for its recognition of P-TEFb. Proc Natl Acad Sci USA 2007; 104:14312-14317 (Pubitemid 350003259)
65. Jeffrey PD, Tong L, Pavletich NP. Structural basis of inhibition of CDK-cyclin complexes by INK4 inhibitors. Genes Dev 2000; 14:3115-3125 (Pubitemid 32015130)
66. Hogg JR, Collins K. RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA 2007; 13:868-880 (Pubitemid 46799821)
67. 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; 27:6996-7006. (Pubitemid 47549739)
68. Mili S, Steitz JA. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 2004; 10:1692-1694 (Pubitemid 39426366)
69. Valverde R, Edwards L, Regan L. Structure and function of KH domains. FEBS Letters 2008; 275:2712-2726
70. Ghatpande S, Goswami S, Mathew S, Rong G, LC, Shafiq S, et al. Identification of a novel cardiac lineage-associated protein(cCLP-1): A candidate regulator of cardiogenesis. Dev Biol 1999; 208:210-221 (Pubitemid 29149459)
71. Huang F, Wagner M, Siddiqui MA. Structure, expression and functional characterization of the mouse CLP-1 gene. Gene 2002; 292:245-259 (Pubitemid 34762008)
72. Huang F, Wagner M, Siddiqui MA. Ablation of the CLP-1 gene leads to downregulation of the HAND1 gene and abnormality of the left ventricle of the heart and fetal death. Mech Dev 2004; 121:559-572 (Pubitemid 38681211)
73. Montano MM, Doughman YQ, Deng H, Chaplin L, Yang J, Wang N, et al. Mutation of the HEXIM1 Gene Results in Defects During Heart and Vascular Development Partly Through Downregulation of Vascular Endothelial Growth Factor. Circ Res 2008; 102:415-422
74. Espinoza-Derout J, Wagner M, Shahmiri K, Mascareno E, Chaqour B, Siddiqui MA. Pivotal role of cardiac lineage protein-1 (CLP-1) in transcriptional elongation factor P-TEFb complex formation in cardiac hypertrophy. Cardiovasc Res 2007; 75:129-138 (Pubitemid 46873518)
75. Kusuhara M, Nagasaki K, Kimura K, Maass N, Manabe T, Ishikawa S, et al. Cloning of hexamethylene-bis-acetamide-inducible transcript, HEXIM1, in human vascular smooth muscle cells. Biomedical Research 1999; 20:273-279 (Pubitemid 30128957)
76. Turano M, Napolitano G, Dulac C, Majello B, Bensaude O, Lania L. Increased HEXIM1 expression during erythroleukemia and neuroblastoma cell differentiation. J Cell Physiol 2006; 206:603-610 (Pubitemid 43191034)
77. He N, Pezda AC, Zhou Q. Modulation of a P-TEFb functional equilibrium for the global control of cell growth and differentiation. Mol Cell Biol 2006; 26:7068-7076 (Pubitemid 44477686)
78. Contreras X, Barboric M, Lenasi T, Peterlin BM. HMBA Releases P-TEFb from HEXIM1 and 7SK snRNA via PI3K/Akt and Activates HIV Transcription. PLoS Pathog 2007; 3:146. (Pubitemid 350085610)
79. 2+ signaling. Genes Dev 2008; 22:1356-1368
80. Wang Y, Dow EC, Liang YY, Ramakrishnan R, Liu H, Sung TL, et al. Phosphatase PPM1A Regulates Phosphorylation of Thr-186 in the Cdk9 T-loop. J Biol Chem 2008; 283:33578-33584
81. Chen R, Yang Z, Zhou Q. Phosphorylated P-TEFb is tagged for inhibition through association with 7SK snRNA. J Biol Chem 2004; 279:4153-4160
82. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006; 20:3347-3365 (Pubitemid 44969154)
83. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 2006; 7:589-600. (Pubitemid 44325350)
84. Matunis EL, Matunis MJ, Dreyfuss G. Association of individual hnRNP proteins and snRNPs with nascent transcripts. J Cell Biol 1993; 121:219-228 (Pubitemid 23989095)
85. Berkhout B, Silverman RH, Jeang K-T. Tat trans-activates the human immunodefiency virus through a nascent RNA target. Cell 1989; 59:273-282 (Pubitemid 19264373)
86. Garber ME, Wei P, KewalRamani VN, Mayall TP, Herrmann CH, Rice AP, et al. The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes & Dev 1998; 12:3512-3527 (Pubitemid 28553243)
87. Peng J, Zhu Y, Milton JT, Price DH. Identification of multiple cyclin subunits of human P-TEFb. Genes Dev 1998; 12:755-762 (Pubitemid 28134306)
88. Bannwarth S, Gatignol A. HIV-1 TAR RNA: the target of molecular interactions between the virus and its host. Curr HIV Res 2005; 3:61-71. (Pubitemid 40081286)
89. Brady J, Kashanchi F. Tat gets the "green" light on transcription initiation. Retrovirology 2005; 2:69.
90. Zhou M, Halanski MA, Radonovich MF, Kashanchi F, Peng J, Price DH, et al. Tat modifies the activity of CDK9 to phosphorylate serine 5 of the RNA polymerase II carboxyl-terminal domain during human immunodeficiency virus type 1 transcription. Mol Cell Biol 2000; 20:5077-5086 (Pubitemid 30431561)
91. Barboric M, Yik JH, Czudnochowski N, Yang Z, Chen R, Contreras X, et al. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription. Nucleic Acids Res 2007; 35:2003-2012 (Pubitemid 47061666)
92. 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 (Pubitemid 47244588)
93. Guiguen A, Soutourina J, Dewez M, Tafforeau L, Dieu M, Raes M, et al. Recruitment of P-TEFb (Cdk9-Pch1) to chromatin by the cap-methyl transferase Pcm1 in fission yeast. EMBO J 2007; 21:1552-1559 (Pubitemid 46480946)