Structure and dynamics of a stabilized coiled-coil domain in the P-TEFb regulator Hexim1

Journal of Molecular Biology

Volumn 414, Issue 5, 2011, Pages 639-653

  Bigalke, Janna M ^a   Dames, Sonja A ^b,c   Blankenfeldt, Wulf ^a   Grzesiek, Stephan ^b   Geyer, Matthias ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

coiled coil; crystal structure; Hexim1; P TEFb; transcription elongation

Indexed keywords

CYCLIN DEPENDENT KINASE 9; CYCLIN T; HEXAMETHYLENE BISACETAMIDE INDUCIBLE PROTEIN 1; LYSINE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN SUBUNIT; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; DELETION MUTANT; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; TRANSCRIPTION INITIATION;

EUKARYOTA;

EID: 82555170200     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.10.022     Document Type: Article

References (61)

1. Fuda N.J., Ardehali M.B., and Lis J.T. Defining mechanisms that regulate RNA polymerase II transcription in vivo Nature 461 2009 186 192
2. Akhtar M.S., Heidemann M., Tietjen J.R., Zhang D.W., Chapman R.D., Eick D., and Ansari A.Z. TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II Mol. Cell 34 2009 387 393
3. Meinhart A., Kamenski T., Hoeppner S., Baumli S., and Cramer P. A structural perspective of CTD function Genes Dev. 19 2005 1401 1415 (Pubitemid 41003005)
4. Peterlin B.M., and Price D.H. Controlling the elongation phase of transcription with P-TEFb Mol. Cell 23 2006 297 305 (Pubitemid 44128850)
5. Bartkowiak B., Liu P.D., Phatnani H.P., Fuda N.J., Cooper J.J., and Price D.H. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1 Genes Dev. 24 2010 2303 2316
6. Zhou Q., and Yik J.H. 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. 70 2006 646 659 (Pubitemid 44484688)
7. He N., Jahchan N.S., Hong E., Li Q., Bayfield M.A., and Maraia R.J. A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb- dependent transcriptional elongation and tumorigenesis Mol. Cell 29 2008 588 599
8. Krueger B.J., Jeronimo C., Roy B.B., Bouchard A., Barrandon C., and Byers S.A. LARP7 is a stable component of the 7SK snRNP while P-TEFb, HEXIM1 and hnRNP A1 are reversibly associated Nucleic Acids Res. 36 2008 2219 2229 (Pubitemid 351566996)
9. Jeronimo C., Forget D., Bouchard A., Li Q., Chua G., and Poitras C. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme Mol. Cell 27 2007 262 274 (Pubitemid 47058308)
10. Xue Y., Yang Z., Chen R., and Zhou Q. A capping-independent function of MePCE in stabilizing 7SK snRNA and facilitating the assembly of 7SK snRNP Nucleic Acids Res. 38 2010 360 369
11. Michels A.A., Fraldi A., Li Q., Adamson T.E., Bonnet F., and Nguyen V.T. Binding of the 7SK snRNA turns the HEXIM1 protein into a P-TEFb (CDK9/cyclin T) inhibitor EMBO J. 23 2004 2608 2619 (Pubitemid 38988232)
12. Yik J.H., Chen R., Nishimura R., Jennings J.L., Link A.J., and 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 12 2003 971 982 (Pubitemid 37352789)
13. Jang M.K., Mochizuki K., Zhou M., Jeong H.S., Brady J.N., and Ozato K. The bromodomain protein Brd4 is a positive regulatory component of P-TEFb and stimulates RNA polymerase II-dependent transcription Mol. Cell 19 2005 523 534 (Pubitemid 41140009)
14. Yang Z., Yik J.H., Chen R., He N., Jang M.K., Ozato K., and Zhou Q. Recruitment of P-TEFb for stimulation of transcriptional elongation by the bromodomain protein Brd4 Mol. Cell 19 2005 535 545 (Pubitemid 41140010)
15. Bisgrove D.A., Mahmoudi T., Henklein P., and Verdin E. Conserved P-TEFb- interacting domain of BRD4 inhibits HIV transcription Proc. Natl Acad. Sci. USA 104 2007 13690 13695 (Pubitemid 350003382)
16. Jones K.A., and Peterlin B.M. Control of RNA initiation and elongation at the HIV-1 promoter Annu. Rev. Biochem. 63 1994 717 743 (Pubitemid 24218647)
17. Schulte A., Czudnochowski N., Barboric M., Schonichen A., Blazek D., Peterlin B.M., and 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. 280 2005 24968 24977 (Pubitemid 40934589)
18. Fraldi A., Varrone F., Napolitano G., Michels A.A., Majello B., Bensaude O., and Lania L. Inhibition of Tat activity by the HEXIM1 protein Retrovirology 2 2005 42
19. Barboric M., Yik J.H., Czudnochowski N., Yang Z., Chen R., and Contreras X. Tat competes with HEXIM1 to increase the active pool of P-TEFb for HIV-1 transcription Nucleic Acids Res. 35 2007 2003 2012 (Pubitemid 47061666)
20. Michels A.A., Nguyen V.T., Fraldi A., Labas V., Edwards M., and Bonnet F. MAQ1 and 7SK RNA interact with CDK9/cyclin T complexes in a transcription-dependent manner Mol. Cell. Biol. 23 2003 4859 4869 (Pubitemid 36793332)
21. Ghatpande S., Goswami S., Mascareno E., and Siddiqui M.A.Q. Signal transduction and transcriptional adaptation in embryonic heart development and during myocardial hypertrophy Mol. Cell. Biochem. 196 1999 93 97 (Pubitemid 29338783)
22. Huang F.C., Wagner M., and Siddiqui M.A.Q. Structure, expression, and functional characterization of the mouse CLP-1 gene Gene 292 2002 245 259 (Pubitemid 34762008)
23. Sano M., Abdellatif M., Oh H., Xie M., Bagella L., and Giordano A. Activation and function of cyclin T-Cdk9 (positive transcription elongation factor-b) in cardiac muscle-cell hypertrophy Nat. Med. 8 2002 1310 1317 (Pubitemid 35373565)
24. Galatioto J., Mascareno E., and Siddiqui M.A.Q. CLP-1 associates with MyoD and HDAC to restore skeletal muscle cell regeneration J. Cell Sci. 123 2010 3789 3795
25. Wittmann B.M., Fujinaga K., Deng H., Ogba N., and Montano M.M. The breast cell growth inhibitor, estrogen down regulated gene 1, modulates a novel functional interaction between estrogen receptor alpha and transcriptional elongation factor cyclin T1 Oncogene 24 2005 5576 5588 (Pubitemid 43119352)
26. Ogba N., Doughman Y.Q., Chaplin L.J., Hu Y., Gargesha M., Watanabe M., and Montano M.M. HEXIM1 modulates vascular endothelial growth factor expression and function in breast epithelial cells and mammary gland Oncogene 29 2010 3639 3649
27. He N., Liu M., Hsu J., Xue Y., Chou S., and Burlingame A. HIV-1 Tat and host AFF4 recruit two transcription elongation factors into a bifunctional complex for coordinated activation of HIV-1 transcription Mol. Cell 38 2010 428 438
28. Sobhian B., Laguette N., Yatim A., Nakamura M., Levy Y., Kiernan R., and Benkirane M. HIV-1 Tat assembles a multifunctional transcription elongation complex and stably associates with the 7SK snRNP Mol. Cell 38 2010 439 451
29. Ouchida R., Kusuhara M., Shimizu N., Hisada T., Makino Y., and Morimoto C. Suppression of NF-kappaB-dependent gene expression by a hexamethylene bisacetamide-inducible protein HEXIM1 in human vascular smooth muscle cells Genes Cells 8 2003 95 107 (Pubitemid 36519090)
30. Baumli S., Lolli G., Lowe E.D., Troiani S., Rusconi L., and Bullock A.N. The structure of P-TEFb (CDK9/cyclin T1), its complex with flavopiridol and regulation by phosphorylation EMBO J. 27 2008 1907 1918
31. Baumli S., Endicott J.A., and Johnson L.N. Halogen bonds form the basis for selective P-TEFb inhibition by DRB Chem. Biol. 17 2010 931 936
32. Anand K., Schulte A., Vogel-Bachmayr K., Scheffzek K., and Geyer M. Structural insights into the cyclin T1-Tat-TAR RNA transcription activation complex from EIAV Nat. Struct. Mol. Biol. 15 2008 1287 1292
33. Tahirov T.H., Babayeva N.D., Varzavand K., Cooper J.J., Sedore S.C., and Price D.H. Crystal structure of HIV-1 Tat complexed with human P-TEFb Nature 465 2010 747 751
34. Vollmuth F., Blankenfeldt W., and Geyer M. Structures of the dual bromodomains of the P-TEFb activating protein Brd4 at atomic resolution J. Biol. Chem. 284 2009 36547 36556
35. Cho S., Schroeder S., Kaehlcke K., Kwon H.S., Pedal A., and Herker E. Acetylation of cyclin T1 regulates the equilibrium between active and inactive P-TEFb in cells EMBO J. 28 2009 1407 1417
36. Vollmuth F., and Geyer M. Interaction of propionylated and butyrylated histone H3 lysine marks with Brd4 bromodomains Angew. Chem., Int. Ed. Engl. 49 2010 6768 6772
37. Dames S.A., Schonichen A., Schulte A., Barboric M., Peterlin B.M., Grzesiek S., and Geyer M. Structure of the Cyclin T binding domain of Hexim1 and molecular basis for its recognition of P-TEFb Proc. Natl Acad. Sci. USA 104 2007 14312 14317 (Pubitemid 350003259)
38. Mason J.M., and Arndt K.M. Coiled coil domains: stability, specificity, and biological implications Chembiochem 5 2004 170 176 (Pubitemid 39256232)
39. Brown J.H., Cohen C., and Parry D.A.D. Heptad breaks in alpha-helical coiled coils: Stutters and stammers Proteins 26 1996 134 145 (Pubitemid 26365307)
40. Schönichen A., Bigalke J.M., Urbanke C., Grzesiek S., Dames S.A., and Geyer M. A flexible bipartite coiled coil structure is required for the interaction of Hexim1 with the P-TEFB subunit cyclin T1 Biochemistry 49 2010 3083 3091
41. Lupas A.N., and Gruber M. The structure of alpha-helical coiled coils Adv. Protein Chem. 70 2005 37 78
42. Oshea E.K., Klemm J.D., Kim P.S., and Alber T. X-Ray structure of the Gcn4 leucine zipper, a 2-stranded, parallel coiled coil Science 254 1991 539 544 (Pubitemid 21917367)
43. Glover J.N.M., and Harrison S.C. Crystal-structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA Nature 373 1995 257 261
44. Strelkov S.V., and Burkhard P. Analysis of alpha-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation J. Struct. Biol. 137 2002 54 64 (Pubitemid 35430421)
45. Mandel A.M., Akke M., and Palmer A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme J. Mol. Biol. 246 1995 144 163
46. Dosset P., Hus J.C., Blackledge M., and Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data J. Biomol. NMR 16 2000 23 28 (Pubitemid 30114721)
47. Czudnochowski N., Vollmuth F., Baumann S., Vogel-Bachmayr K., and Geyer M. Specificity of Hexim1 and Hexim2 complex formation with cyclin T1/T2, importin alpha and 7SK snRNA J. Mol. Biol. 395 2010 28 41
48. Lebars I., Martinez-Zapien D., Durand A., Coutant J., Kieffer B., and Dock-Bregeon A.C. HEXIM1 targets a repeated GAUC motif in the riboregulator of transcription 7SK and promotes base pair rearrangements Nucleic Acids Res. 38 2010 7749 7763
49. Belanger F., Baigude H., and Rana T.M. U30 of 7SK RNA forms a specific photo-cross-link with Hexim1 in the context of both a minimal RNA-binding site and a fully reconstituted 7SK/Hexim1/P-TEFb ribonucleoprotein complex J. Mol. Biol. 386 2009 1094 1107
50. Kim Y.K., Mbonye U., Hokello J., and 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. 410 2011 896 916
51. Anand K., Schulte A., Fujinaga K., Scheffzek K., and Geyer M. Cyclin box structure of the P-TEFb subunit cyclin T1 derived from a fusion complex with EIAV Tat J. Mol. Biol. 370 2007 826 836 (Pubitemid 46901131)
52. Kabsch W. Xds Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 125 132
53. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 2002 1772 1779 (Pubitemid 35169744)
54. Emsley P., Lohkamp B., Scott W.G., and Cowtan K. Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
55. Murshudov G.N., Skubák P., Lebedev A.A., Pannu N.S., Steiner R.A., and Nicholls R.A. REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 355 367
56. Krissinel E., and Henrick K. Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797 (Pubitemid 47321791)
57. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6 1995 277 293
58. Johnson B.A. Using NMRView to visualize and analyze the NMR spectra of macromolecules Methods Mol. Biol. 278 2004 313 352
59. Dames S.A., Schonichen A., Grzesiek S., and Geyer M. NMR assignment of the Cyclin T-binding domain of human Hexim1 J. Biomol. NMR 36 2006 39 (Pubitemid 46909595)
60. Grzesiek S., Bax A., Hu J.S., Kaufman J., Palmer I., and Stahl S.J. Refined solution structure and backbone dynamics of HIV-1 Nef Protein Sci. 6 1997 1248 1263 (Pubitemid 27260159)
61. Bigalke J.M., Czudnochowski N., Vollmuth F., Vogel-Bachmayr K., Anand K., and Geyer M. Formation of Tat-TAR containing ribonucleoprotein complexes for biochemical and structural analyses Methods 53 2011 78 84