A Cyclin T1 point mutation that abolishes positive transcription elongation factor (P-TEFb) binding to Hexim1 and HIV tat

Retrovirology

Volumn 11, Issue 1, 2014, Pages

  Verstraete, Nina ^a,b,c   Kuzmina, Alona ^d   Diribarne, Gaelle ^a,b,c   Nguyen, Van T ^a,b,c   Kobbi, Lydia ^a,b,c   Ludanyi, Monika ^a,b,c,e   Taube, Ran ^d   Bensaude, Olivier ^a,b,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^e Present Address CEA   (France)

Author keywords

7SK RNA; CDK inhibition; Cyclin T; Genetic mapping of protein protein interfaces; Hexim1; P TEFb

Indexed keywords

AMINO ACID; CELL PROTEIN; CYCLIN T1; HEXIM1 PROTEIN; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; CCNT1 PROTEIN, HUMAN; CYCLIN T; HEXIM1 PROTEIN, HUMAN; RNA BINDING PROTEIN; BINDING PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIMERIZATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS; MUTAGENESIS; NONHUMAN; POINT MUTATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; CHEMISTRY; HYDROGEN BOND; METABOLISM; PROTEIN FOLDING; STRUCTURE ACTIVITY RELATION; TWO HYBRID SYSTEM; BINDING AFFINITY; BINDING SITE; MOLECULAR DYNAMICS; NEMATODE; NUCLEAR MAGNETIC RESONANCE; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RESIDUE ANALYSIS; VIRUS IDENTIFICATION; X RAY CRYSTALLOGRAPHY;

CYCLIN T; HUMANS; HYDROGEN BONDING; POINT MUTATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; PROTEIN FOLDING; RNA-BINDING PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TWO-HYBRID SYSTEM TECHNIQUES;

HUMAN IMMUNODEFICIENCY VIRUS 1; NEMATODA;

EID: 84904600705     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-11-50     Document Type: Article

References (48)

1. Peterlin BM, Price DH. Controlling the elongation phase of transcription with P-TEFb. Mol Cell 2006, 23:297-305.
2. Karn J. The molecular biology of HIV latency: breaking and restoring the Tat-dependent transcriptional circuit. Curr Opin HIV AIDS 2011, 6:4-11.
3. Perales R, Bentley D. " Cotranscriptionality" : the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 2009, 36:178-191.
4. 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.
5. 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.
6. Peterlin BM, Brogie JE, Price DH. 7SK snRNA: a noncoding RNA that plays a major role in regulating eukaryotic transcription. Wiley Interdiscip Rev RNA 2012, 3:92-103.
7. Michels AA, Nguyen VT, Fraldi A, Labas V, Edwards M, Bonnet F, Lania L, Bensaude O. MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner. Mol Cell Biol 2003, 23:4859-4869.
8. Michels AA, Fraldi A, Li Q, Adamson TE, Bonnet F, Nguyen VT, Sedore SC, Price JP, Price DH, Lania L, Bensaude O. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor. EMBO J 2004, 23:2608-2619.
9. 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.
10. 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.
11. Fraldi A, Varrone F, Napolitano G, Michels AA, Majello B, Bensaude O, Lania L. Inhibition of Tat activity by the HEXIM1 protein. Retrovirology 2005, 2:42.
12. Van Herreweghe E, Egloff S, Goiffon I, Jady BE, Froment C, Monsarrat B, Kiss T. Dynamic remodelling of human 7SK snRNP controls the nuclear level of active P-TEFb. EMBO J 2007, 26:3570-3580.
13. 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.
14. Hogg JR, Collins K. RNA-based affinity purification reveals 7SK RNPs with distinct composition and regulation. RNA (New York, NY) 2007, 13:868-880.
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, 19:523-534.
16. 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.
17. Schroder S, Cho S, Zeng L, Zhang Q, Kaehlcke K, Mak L, Lau J, Bisgrove D, Schnölzer M, Verdin E, Zhou MM, Ott M. Two-pronged binding with bromodomain-containing protein 4 liberates positive transcription elongation factor b from inactive ribonucleoprotein complexes. J Biol Chem 2012, 287:1090-1099.
18. Liu W, Ma Q, Wong K, Li W, Ohgi K, Zhang J, Aggarwal AK, Rosenfeld MG. Brd4 and JMJD6-associated anti-pause enhancers in regulation of transcriptional pause release. Cell 2013, 155:1581-1595.
19. McNamara RP, McCann JL, Gudipaty SA, D'Orso I. Transcription factors mediate the enzymatic disassembly of promoter-bound 7SK snRNP to locally recruit P-TEFb for transcription elongation. Cell Rep 2013, 5:1256-1268.
20. Lu H, Li Z, Xue Y, Schulze-Gahmen U, Johnson JR, Krogan NJ, Alber T, Zhou Q. AFF1 is a ubiquitous P-TEFb partner to enable Tat extraction of P-TEFb from 7SK snRNP and formation of SECs for HIV transactivation. Proc Natl Acad Sci U S A 2014, 111:E15-E24.
21. Baumli S, Lolli G, Lowe ED, Troiani S, Rusconi L, Bullock AN, Debreczeni JE, Knapp S, Johnson LN. The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation. EMBO J 2008, 27:1907-1918.
22. 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.
23. Dames SA, Schonichen A, Schulte A, Barboric M, Peterlin BM, Grzesiek S, Geyer M. Structure of the cyclin T binding domain of Hexim1 and molecular basis for its recognition of P-TEFb. Proc Natl Acad Sci U S A 2007, 104:14312-14317.
24. Lebars I, Martinez-Zapien D, Durand A, Coutant J, Kieffer B, Dock-Bregeon A. HEXIM1 targets a repeated GAUC motif in the riboregulator of transcription 7SK and promotes base pair rearrangements. Nucleic Acids Res 2010, 38:7749-7763.
25. Durney MA, D'Souza VM. Preformed protein-binding motifs in 7SK snRNA: structural and thermodynamic comparisons with retroviral TAR. J Mol Biol 2010, 404:555-567.
26. Dhayalan A, Jurkowski TP, Laser H, Reinhardt R, Jia D, Cheng X, Jeltsch A. Mapping of protein-protein interaction sites by the 'absence of interference' approach. J Mol Biol 2008, 376:1091-1099.
27. Vidal M, Brachmann RK, Fattaey A, Harlow E, Boeke JD. Reverse two-hybrid and one-hybrid systems to detect dissociation of protein-protein and DNA-protein interactions. Proc Natl Acad Sci U S A 1996, 93:10315-10320.
28. Echalier A, Endicott JA, Noble ME. Recent developments in cyclin-dependent kinase biochemical and structural studies. Biochim Biophys Acta 2010, 1804:511-519.
29. Nguyen D, Krueger BJ, Sedore SC, Brogie JE, Rogers JT, Rajendra TK, Saunders A, Matera AG, Lis JT, Uguen P, Price DH. The Drosophila 7SK snRNP and the essential role of dHEXIM in development. Nucleic Acids Res 2012, 40:5283-97.
30. Shim EY, Walker AK, Shi Y, Blackwell TK. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev 2002, 16:2135-2146.
31. Marz M, Donath A, Verstraete N, Nguyen VT, Stadler P-F, Bensaude O. Evolution of 7SK RNA and its protein partners in Metazoa. Mol Biol Evol 2009, 26:2821-2830.
32. Dulac C, Michels AA, Fraldi A, Bonnet F, Nguyen VT, Napolitano G, Lania L, Bensaude O. Transcription-dependent association of multiple P-TEFb units to a HEXIM multimer. J Biol Chem 2005, 280:30619-30629.
33. Majello B, De Luca P, Hagen G, Suske G, Lania L. Different members of the Sp1 multigene family exert opposite transcriptional regulation of the long terminal repeat of HIV-1. Nucleic Acids Res 1994, 22:4914-4921.
34. Taube R, Lin X, Irwin D, Fujinaga K, Peterlin BM. Interaction between P-TEFb and the C-terminal domain of RNA polymerase II activates transcriptional elongation from sites upstream or downstream of target genes. Mol Cell Biol 2002, 22:321-331.
35. Garber ME, Wei P, KewalRamani VN, Mayall TP, Herrmann CH, Rice AP, Littman DR, Jones KA. 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.
36. Zhang J, Tamilarasu N, Hwang S, Garber ME, Huq I, Jones KA, Rana TM. HIV-1 TAR RNA enhances the interaction between Tat and cyclin T1. J Biol Chem 2000, 275:34314-34319.
37. Muniz L, Egloff S, Ughy B, Jady B, Kiss T. Controlling cellular P-TEFb activity by the HIV-1 transcriptional transactivator Tat. PLoS Pathog 2010, 6:e1001152.
38. Kuzmina A, Hadad U, Fujinaga K, Taube R. Functional characterization of a human cyclin T1 mutant reveals a different binding surface for Tat and HEXIM1. Virology 2012, 426:152-161.
39. Otieno S, Grace CR, Kriwacki RW. The role of the LH subdomain in the function of the Cip/Kip cyclin-dependent kinase regulators. Biophys J 2011, 100:2486-2494.
40. Campbell GR, Loret EP. What does the structure-function relationship of the HIV-1 Tat protein teach us about developing an AIDS vaccine?. Retrovirology 2009, 6:50.
41. Wang Y, Fisher J, Mathew R, Ou L, Otieno S, Sublet J, Xiao L, Chen J, Roussel MF, Kriwacki RW. Intrinsic disorder mediates the diverse regulatory functions of the Cdk inhibitor p21. Nat Chem Biol 2011, 7:214-221.
42. Baumli S, Endicott JA, Johnson L. Halogen bonds form the basis for selective P-TEFb inhibition by DRB. Chem Biol 2010, 17:931-936.
43. Steiner T, Koellner G. Hydrogen bonds with Pi-acceptors in proteins: frequencies and role in stabilizing local 3D structures. J Mol Biol 2000, 305:535-557.
44. Schulze-Gahmen U, Upton H, Birnberg A, Bao K, Chou S, Krogan NJ, Zhou Q, Alber T. The AFF4 scaffold binds human P-TEFb adjacent to HIV Tat. Elife 2013, 2:e00327.
45. Gu J, Babayeva ND, Suwa Y, Baranovskiy AG, Price DH, Tahirov TH. Crystal structure of HIV-1 Tat complexed with human P-TEFb and AFF4. Cell Cycle 2014, 13:1788-1797.
46. Asamitsu K, Hibi Y, Imai K, Victoriano AF, Kurimoto E, Kato K, Okamoto T. Functional characterization of human cyclin T1 N-terminal region for human immunodeficiency virus-1 Tat transcriptional activation. J Mol Biol 2011, 410:887-895.
47. Cho RJ, Fromont-Racine M, Wodicka L, Feierbach B, Stearns T, Legrain P, Lockhart DJ, Davis RW. Parallel analysis of genetic selections using whole genome oligonucleotide arrays. Proc Natl Acad Sci U S A 1998, 95:3752-3757.
48. Yu D, Ellis HM, Lee EC, Jenkins NA, Copeland NG, Court DL. An efficient recombination system for chromosome engineering in Escherichia coli. Proc Natl Acad Sci U S A 2000, 97:5978-5983.