HMGA1 directly interacts with TAR to modulate basal and Tat-dependent HIV transcription

RNA Biology

Volumn 10, Issue 3, 2013, Pages 436-444

  Eilebrecht, Sebastian ^a,b   Wilhelm, Emmanuelle ^c   Benecke, Bernd Joachim ^d   Bell, Brendan ^c   Benecke, Arndt G ^a,b  

^a CNRS   (France)

^b INSERM U955   (France)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

HIV LTR; HIV transcription; HIV 1 TAR; HMGA1; Tat transactivation

Indexed keywords

HIGH MOBILITY GROUP A1A PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION ELONGATION FACTOR; TRANSCRIPTION FACTOR SP1;

ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ELECTROPHORETIC MOBILITY; FEMALE; GENE EXPRESSION; GENE SILENCING; HOUSEKEEPING GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MODULATION; NONHUMAN; POINT MUTATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSACTIVATION; TRANSCRIPTION INITIATION SITE; VIRUS TRANSCRIPTION; WESTERN BLOTTING; WILD TYPE;

7SK SNRNA; ELONGATION; HIV-1; HMGA1; P-TEFB; TAR; TAT; TRANSCRIPTION;

BINDING SITES; GENE EXPRESSION REGULATION, VIRAL; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HELA CELLS; HIV INFECTIONS; HIV LONG TERMINAL REPEAT; HIV-1; HMGA1A PROTEIN; HUMANS; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROMOTER REGIONS, GENETIC; RNA, VIRAL; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TRANSCRIPTION, GENETIC;

EID: 84874959786     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.23686     Document Type: Article

References (60)

1. Kao SY, Calman A F, Luciw PA, Peterlin BM. Anti-termination of transcription within the long terminal repeat of HIV-1 by tat gene product. Nature 1987; 330:489-93; PMID:2825027; http://dx.doi.org/10.1038/330489a0.
2. Herrmann CH, Gold MO, Rice A P. Viral transac-tivators specifically target distinct cellular protein kinases that phosphorylate the RNA polymerase II C-terminal domain. Nucleic Acids Res 1996; 24:501-8; PMID:8602364; http://dx.doi.org/10.1093/nar/24.3.501.
3. Herrmann CH, Rice A P. Lentivirus Tat proteins specifically associate with a cellular protein kinase, TAK, that hyperphosphorylates the carboxyl-terminal domain of the large subunit of RNA polymerase II: candidate for a Tat cofactor. J Virol 1995; 69:1612-20; PMID:7853496.
4. Marshall N F, Peng J, Xie Z, Price DH. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem 1996; 271:27176-83; PMID:8900211; http://dx.doi.org/10.1074/jbc.271.43.27176.
5. Marshall N F, Price DH. Purification of P-TEFb, a transcription factor required for the transition into productive elongation. J Biol Chem 1995; 270:12335-8; PMID:7759473; http://dx.doi.org/10.1074/jbc.270.21.12335.
6. Zhu Y, Pe'ery T, Peng J, Ramanathan Y, Marshall N, Marshall T, et al. Transcription elongation factor P-TEFb is required for HIV-1 tat transactivation in vitro. Genes Dev 1997; 11:2622-32; PMID:9334325; http://dx.doi.org/10.1101/ gad.11.20.2622.
7. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006; 23:297-305; PMID:16885020; http://dx.doi.org/10. 1016/j.molcel.2006.06.014.
8. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA. 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; 92:451-62; PMID:9491887; http://dx.doi.org/10.1016/S0092-8674(00)80939-3.
9. 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; 70:646-59; PMID:16959964; http://dx.doi.org/10.1128/MMBR.00011-06.
10. Chao SH, Price DH. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J Biol Chem 2001; 276:31793-9; PMID:11431468; http://dx.doi.org/10.1074/jbc.M102306200.
11. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, et al. c-Myc regulates transcriptional pause release. Cell 2010; 141:432-45; PMID:20434984; http://dx.doi.org/10.1016/j.cell.2010.03.030.
12. Eilebrecht S, Benecke BJ, Benecke A. 7SK snRNA-mediated, gene-specific cooperativity of HMGA1 and P-TEFb. RNA Biol 2011; 8:1084-93; PMID:21957495; http://dx.doi.org/10.4161/rna.8.6.17015.
13. 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; 414:322-5; PMID:11713533; http://dx.doi.org/10.1038/35104581.
14. Yang Z, Zhu Q, Luo K, Zhou Q. The 7SK small nuclear RNA inhibits the CDK9/cyclin T1 kinase to control transcription. Nature 2001; 414:317-22; PMID:11713532; http://dx.doi.org/10.1038/35104575.
15. 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; 19:523-34; PMID:16109376; http://dx.doi.org/10.1016/j.molcel.2005.06.027.
16. Yang Z, Yik JH, Chen R, He N, Jang MK, Ozato K, et al. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4. Mol Cell 2005; 19:535-45; PMID:16109377; http://dx.doi.org/10.1016/j. molcel.2005.06.029.
17. D'Orso I, Frankel AD. RNA-mediated displacement of an inhibitory snRNP complex activates transcription elongation. Nat Struct Mol Biol 2010; 17:815-21; PMID:20562857; http://dx.doi.org/10.1038/nsmb.1827.
18. He N, Liu M, Hsu J, Xue Y, Chou S, Burlingame A, et al. 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; 38:428-38; PMID:20471948; http://dx.doi.org/10.1016/j.molcel.2010.04.013.
19. Sobhian B, Laguette N, Yatim A, Nakamura M, Levy Y, Kiernan R, et al. HIV-1 Ta t assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP. Mol Cell 2010; 38:439-51; PMID:20471949; http://dx.doi.org/10.1016/j.mol-cel.2010.04.012.
20. Pereira LA, Bentley K, Peeters A, Churchill MJ, Deacon NJ. A compilation of cellular transcription factor interactions with the HIV-1 LTR promoter. Nucleic Acids Res 2000; 28:663-8; PMID:10637316; http://dx.doi.org/10.1093/nar/ 28.3.663.
21. Gaynor R. Cellular transcription factors involved in the regulation of HIV-1 gene expression. AIDS 1992; 6:347-63; PMID:1616633; http://dx.doi.org/10. 1097/00002030-199204000-00001.
22. Gatignol A, Buckler-White A, Berkhout B, Jeang KT. Characterization of a human TAR RNA-binding protein that activates the HIV-1 LTR. Science 1991; 251:1597-600; PMID:2011739; http://dx.doi.org/10.1126/science.2011739.
23. Gatignol A, Duarte M, Daviet L, Chang YN, Jeang K T. Sequential steps in Tat trans-activation of HIV-1 mediated through cellular DNA, RNA, and protein binding factors. Gene Expr 1996; 5:217-28; PMID:8723388.
24. Ansari SA, Safak M, Gallia GL, Sawaya BE, Amini S, Khalili K. Interaction of YB-1 with human immunodeficiency virus type 1 Tat and TAR RNA modulates viral promoter activity. J Gen Virol 1999; 80:2629-38; PMID:10573156.
25. Chepenik LG, Tretiakova A P, Krachmarov C P, Johnson EM, Khalili K. The single-stranded DNA binding protein, Pur-alpha, binds HIV-1 TAR RNA and activates HIV-1 transcription. Gene 1998; 210:37-44; PMID:9524214; http://dx.doi.org/10.1016/S0378-1119(98)00033-X.
26. Fujii R, Okamoto M, Aratani S, Oishi T, Ohshima T, Taira K, et al. A Role of RNA Helicase A in cis-Acting Transactivation Response Element-mediated Transcriptional Regulation of Human Immunodeficiency Virus Type 1. J Biol Chem 2001; 276:5445-51; PMID:11096080; http://dx.doi.org/10.1074/jbc.M006892200.
27. Eilebrecht S, Brysbaert G, Wegert T, Urlaub H, Benecke BJ, Benecke A. 7SK small nuclear RNA directly affects HMGA1 function in transcription regulation. Nucleic Acids Res 2011; 39:2057-72; PMID:21087998; http://dx.doi.org/10.1093/ nar/gkq1153.
28. Reeves R, Nissen MS. The A.T-DNA-binding domain of mammalian high mobility group I chromosomal proteins. A novel peptide motif for recognizing DNA structure. J Biol Chem 1990; 265:8573-82; PMID:1692833.
29. Farnet CM, Bushman FD. HIV-1 cDNA integration: requirement of HMG I(Y) protein for function of pre-integration complexes in vitro. Cell 1997; 88:483-92; PMID:9038339; http://dx.doi.org/10.1016/S0092-8674(00)81888-7.
30. Gao K, Gorelick RJ, Johnson DG, Bushman F. Cofactors for human immunodeficiency virus type 1 cDNA integration in vitro. J Virol 2003; 77:1598-603; PMID:12502875; http://dx.doi.org/10.1128/JVI.77.2.1598-1603.2003.
31. Van Maele B, Busschots K, Vandekerckhove L, Christ F, Debyser Z. Cellular co-factors of HIV-1 integration. Trends Biochem Sci 2006; 31:98-105; PMID:16403635; http://dx.doi.org/10.1016/j.tibs.2005.12.002.
32. Tsuruno C, Ohe K, Kuramitsu M, Kohma T, Takahama Y, Hamaguchi Y, et al. HMGA1a is involved in specific splice site regulation of human immunodeficiency virus type 1. Biochem Biophys Res Commun 2011; 406:512-7; PMID:21329653; http://dx.doi.org/10.1016/j.bbrc.2011.02.059.
33. Henderson A, Holloway A, Reeves R, Tremethick DJ. Recruitment of SWI/SNF to the human immunodeficiency virus type 1 promoter. Mol Cell Biol 2004; 24:389-97; PMID:14673171; http://dx.doi.org/10.1128/MCB.24.1.389-397.2004.
34. Henderson A, Bunce M, Siddon N, Reeves R, Tremethick DJ. High-mobility-group protein I can modulate binding of transcription factors to the U5 region of the human immunodeficiency virus type 1 proviral promoter. J Virol 2000; 74:10523-34; PMID:11044097; http://dx.doi.org/10.1128/JVI.74.22. 10523-10534.2000.
35. Chi YH, Semmes OJ, Jeang KT. A proteomic study of TAR-RNA binding protein (TRBP)-associated factors. Cell Biosci 2011; 1:9; PMID:21711701; http://dx.doi.org/10.1186/2045-3701-1-9.
36. Foti D, Iuliano R, Chiefari E, Brunetti A. A nucleo-protein complex containing Sp1, C/EBP beta, and HMGI-Y controls human insulin receptor gene transcription. Mol Cell Biol 2003; 23:2720-32; PMID:12665574; http://dx.doi.org/10.1128/MCB.23.8.2720-2732.2003.
37. Harrer M, Lührs H, Bustin M, Scheer U, Hock R. Dynamic interaction of HMGA1a proteins with chro-matin. J Cell Sci 2004; 117:3459-71; PMID:15213251; http://dx.doi.org/10.1242/jcs.01160.
38. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA. 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; 92:451-62; PMID:9491887; http://dx.doi.org/10.1016/S0092-8674(00)80939-3.
39. Berkhout B, Jeang KT. trans activation of human immunodeficiency virus type 1 is sequence specific for both the single-stranded bulge and loop of the trans-acting-responsive hairpin: a quantitative analysis. J Virol 1989; 63:5501-4; PMID:2479775.
40. Huthoff H, Girard F, Wijmenga SS, Berkhout B. Evidence for a base triple in the free HIV-1 TAR RNA. RNA 2004; 10:412-23; PMID:14970387; http://dx.doi.org/10.1261/rna.5161304.
41. Jossinet F, Ludwig TE, Westhof E. Assemble: an interactive graphical tool to analyze and build RNA architectures at the 2D and 3D levels. Bioinformatics 2010; 26:2057-9; PMID:20562414; http://dx.doi.org/10.1093/bioinformatics/btq321.
42. Desfosses Y, Solis M, Sun Q, Grandvaux N, Van Lint C, Burny A, et al. Regulation of human immunodeficiency virus type 1 gene expression by clade-specific Tat proteins. J Virol 2005; 79:9180-91; PMID:15994812; http://dx.doi.org/10.1128/JVI.79.14.9180-9191.2005.
43. Muniz L, Egloff S, Ughy B, Jády BE, Kiss T. Controlling cellular P-TEFb activity by the HIV-1 transcriptional transactivator Tat. PLoS Pathog 2010; 6:e1001152; PMID:20976203; http://dx.doi.org/10.1371/journal.ppat.1001152.
44. Eilebrecht S, Pellay FX, Odenwälder P, Brysbaert G, Benecke BJ, Benecke A. EBER2 RNA-induced transcriptome changes identify cellular processes likely targeted during Epstein Barr Virus infection. BMC Res Notes 2008; 1:100; PMID:18957101; http://dx.doi.org/10.1186/1756-0500-1-100.
45. Reeves R, Leonard WJ, Nissen MS. Binding of HMG-I(Y) imparts architectural specificity to a positioned nucleosome on the promoter of the human interleukin-2 receptor alpha gene. Mol Cell Biol 2000; 20:4666-79; PMID:10848593; http://dx.doi.org/10.1128/MCB.20.13.4666-4679.2000.
46. John S, Reeves RB, Lin JX, Child R, Leiden JM, Thompson CB, et al. Regulation of cell-type-specific interleukin-2 receptor alpha-chain gene expression: potential role of physical interactions between Elf-1, HMG-I(Y), and NF-kappa B family proteins. Mol Cell Biol 1995; 15:1786-96; PMID:7862168.
47. Zhang XM, Verdine GL. A small region in HMG I(Y) is critical for cooperation with NF-kappaB on DNA. J Biol Chem 1999; 274:20235-43; PMID:10400641; http://dx.doi.org/10.1074/jbc.274.29.20235.
48. Kretzschmar M, Meisterernst M, Scheidereit C, Li G, Roeder RG. Transcriptional regulation of the HIV-1 promoter by NF-kappa B in vitro. Genes Dev 1992; 6:761-74; PMID:1577271; http://dx.doi.org/10.1101/gad.6.5.761.
49. Harrich D, Garcia J, Wu F, Mitsuyasu R, Gonazalez J, Gaynor R. Role of SP1-binding domains in in vivo transcriptional regulation of the human immunodeficiency virus type 1 long terminal repeat. J Virol 1989; 63:2585-91; PMID:2657100.
50. Sedore SC, Byers SA, Biglione S, Price J P, 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; 35:4347-58; PMID:17576689; http://dx.doi.org/10.1093/nar/gkm443.
51. Mashima T, Udagawa S, Tsuruo T. Involvement of transcriptional repressor ATF3 in acceleration of cas-pase protease activation during DNA damaging agent-induced apoptosis. J Cell Physiol 2001; 188:352-8; PMID:11473362; http://dx.doi.org/10.1002/jcp.1130.
52. Mancebo HS, Lee G, Flygare J, Tomassini J, Luu P, Zhu Y, et al. P-TEFb kinase is required for HIV Tat transcriptional activation in vivo and in vitro. Genes Dev 1997; 11:2633-44; PMID:9334326; http://dx.doi.org/10.1101/gad.11.20. 2633.
53. Sanghvi VR, Steel L F. The cellular TAR RNA binding protein, TRBP, promotes HIV-1 replication primarily by inhibiting the activation of double-stranded RNA-dependent kinase PKR. J Virol 2011; 85:12614-21; PMID:21937648; http://dx.doi.org/10.1128/JVI.05240-11.
54. Dorin D, Bonnet MC, Bannwarth S, Gatignol A, Meurs EF, Vaquero C. The TAR RNA-binding protein, TRBP, stimulates the expression of TAR-containing RNAs in vitro and in vivo independently of its ability to inhibit the dsRNA-dependent kinase PKR. J Biol Chem 2003; 278:4440-8; PMID:12475984; http://dx.doi.org/10. 1074/jbc.M208954200.
55. Wagschal A, Rousset E, Basavarajaiah P, Contreras X, Harwig A, Laurent-Chabalier S, et al. Microprocessor, Setx, Xrn2, and Rrp6 co-operate to induce premature termination of transcription by RNAPII. Cell 2012; 150:1147-57; PMID:22980978; http://dx.doi.org/10.1016/j.cell.2012.08.004.
56. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-5; PMID:5432063; http://dx.doi.org/10.1038/227680a0.
57. Wienken CJ, Baaske P, Rothbauer U, Braun D, Duhr S. Protein-binding assays in biological liquids using microscale thermophoresis. Nat Commun 2010; 1:100; PMID:20981028; http://dx.doi.org/10.1038/ncomms1093.
58. Wienken CJ, Baaske P, Duhr S, Braun D. Thermophoretic melting curves quantify the conformation and stability of RNA and DNA. Nucleic Acids Res 2011; 39:e52; PMID:21297115; http://dx.doi.org/10.1093/nar/gkr035.
59. Zuker M. Computer prediction of RNA structure. Methods Enzymol 1989; 180:262-88; PMID:2482418; http://dx.doi.org/10.1016/0076-6879(89)80106-5.
60. Wilhelm E, Doyle MC, Nzaramba I, Magdzinski A, Dumais N, Bell B. CTGC motifs within the HIV core promoter specify Tat-responsive pre-initiation complexes. Retrovirology 2012; 9:62; PMID:22834489; http://dx.doi.org/10.1186/ 1742-4690-9-62.