HIV-1 Tat binding to PCAF bromodomain: Structural determinants from computational methods

Biology

Volumn 1, Issue 2, 2012, Pages 277-296

  Quy, Vo Cam ^a   Pantano, Sergio ^b   Rossetti, Giulia ^a,c   Giacca, Mauro ^d   Carloni, Paolo ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

^c BARCELONA SUPERCOMPUTING CENTER   (Spain)

^d INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

Docking; HIV 1; PCAF BRD; Protein protein interaction; Tat

Indexed keywords

EID: 84901347444     PISSN: None     EISSN: 20797737     Source Type: Journal    
DOI: 10.3390/biology1020277     Document Type: Article

References (89)

1. Flexner, C. HIV drug development: The next 25 years. Nat. Rev. Drug Discov. 2007, 6, 959-966.
2. Wainberg, M.A.; Zaharatos, G.J.; Brenner, B.G. Development of antiretroviral drug resistance. N. Engl. J. Med. 2011, 365, 637-646.
3. Detels, R. The search for protection against HIV infection. Ann. Epidemiol. 2009, 19, 250-252.
4. Al-Mawsawi, L.Q.; Al-Safi, R.I.; Neamati, N. Anti-infectives: Clinical progress of HIV-1 integrase inhibitors. Expert. Opin. Emerg. Drugs 2008, 13, 213-225.
5. Menendez-Arias, L. Molecular basis of human immunodeficiency virus drug resistance: An update. Antivir. Res. 2010, 85, 210-231.
6. Menendez-Arias, L. Targeting HIV: Antiretroviral therapy and development of drug resistance. Trends Pharmacol. Sci. 2002, 23, 381-388.
7. Al-Mawsawi, L.Q.; Neamati, N. Blocking interactions between HIV-1 integrase and cellular cofactors: An emerging anti-retroviral strategy. Trends Pharmacol. Sci. 2007, 28, 526-535.
8. Adamson, C.S.; Freed, E.O. Novel approaches to inhibiting HIV-1 replication. Antivir. Res. 2010, 85, 119-141.
9. Ensoli, B.; Fiorelli, V.; Ensoli, F.; Cafaro, A.; Titti, F.; Butto, S.; Monini, P.; Magnani, M.; Caputo, A.; Garaci, E. Candidate HIV-1 Tat vaccine development: From basic science to clinical trials. AIDS 2006, 20, 2245-2261.
10. Gatignol, A. Transcription of HIV: Tat and cellular chromatin. Adv. Pharmacol. 2007, 55, 137-159.
11. Johri, M.K.; Mishra, R.; Chhatbar, C.; Unni, S.K.; Singh, S.K. Tits and bits of HIV Tat protein. Expert. Opin. Biol. Ther. 2011, 11, 269-283.
12. Pantano, S.; Carloni, P. Comparative analysis of HIV-1 Tat variants. Proteins 2005, 58, 638-643.
13. Peloponese, J.M., Jr.; Gregoire, C.; Opi, S.; Esquieu, D.; Sturgis, J.; Lebrun, E.; Meurs, E.; Collette, Y.; Olive, D.; Aubertin, A.M.; et al. 1H-13C nuclear magnetic resonance assignment and structural characterization of HIV-1 Tat protein. C. R. Acad. Sci. III 2000, 323, 883-894.
14. Gregoire, C.; Peloponese, J.M., Jr.; Esquieu, D.; Opi, S.; Campbell, G.; Solomiac, M.; Lebrun, E.; Lebreton, J.; Loret, E.P. Homonuclear (1)H-NMR assignment and structural characterization of human immunodeficiency virus type 1 Tat Mal protein. Biopolymers 2001, 62, 324-335.
15. Bayer, P.; Kraft, M.; Ejchart, A.; Westendorp, M.; Frank, R.; Rosch, P. Structural studies of HIV-1 Tat protein. J. Mol. Biol. 1995, 247, 529-535.
16. Foucault, M.; Mayol, K.; Receveur-Brechot, V.; Bussat, M.C.; Klinguer-Hamour, C.; Verrier, B.; Beck, A.; Haser, R.; Gouet, P.; Guillon, C. UV and X-ray structural studies of a 101-residue long Tat protein from a HIV-1 primary isolate and of its mutated, detoxified, vaccine candidate. Proteins 2010, 78, 1441-1456.
17. Tahirov, T.H.; Babayeva, N.D.; Varzavand, K.; Cooper, J.J.; Sedore, S.C.; Price, D.H. Crystal structure of HIV-1 Tat complexed with human P-TEFb. Nature 2010, 465, 747-751.
18. Mujtaba, S.; He, Y.; Zeng, L.; Farooq, A.; Carlson, J.E.; Ott, M.; Verdin, E.; Zhou, M.M. Structural basis of lysine-acetylated HIV-1 Tat recognition by PCAF bromodomain. Mol. Cell 2002, 9, 575-586.
19. Opi, S.; Peloponese, J.M., Jr.; Esquieu, D.; Campbell, G.; de Mareuil, J.; Walburger, A.; Solomiac, M.; Gregoire, C.; Bouveret, E.; Yirrell, D.L.; et al. Tat HIV-1 primary and tertiary structures critical to immune response against non-homologous variants. J. Biol. Chem. 2002, 277, 35915-35919.
20. Ott, M.; Schnolzer, M.; Garnica, J.; Fischle, W.; Emiliani, S.; Rackwitz, H.R.; Verdin, E. Acetylation of the HIV-1 Tat protein by p300 is important for its transcriptional activity. Curr. Biol. 1999, 9, 1489-1492.
21. Kiernan, R.E.; Vanhulle, C.; Schiltz, L.; Adam, E.; Xiao, H.; Maudoux, F.; Calomme, C.; Burny, A.; Nakatani, Y.; Jeang, K.T.; et al. HIV-1 tat transcriptional activity is regulated by acetylation. EMBO J. 1999, 18, 6106-6118.
22. Nakatani, Y. HIV-1 transcription: Activation mediated by acetylation of Tat. Structure 2002, 10, 443-444.
23. Dhalluin, C.; Carlson, J.E.; Zeng, L.; He, C.; Aggarwal, A.K.; Zhou, M.M. Structure and ligand of a histone acetyltransferase bromodomain. Nature 1999, 399, 491-496.
24. Shikama, N.; Chan, H.M.; Krstic-Demonacos, M.; Smith, L.; Lee, C.W.; Cairns, W.; La Thangue, N.B. Functional interaction between nucleosome assembly proteins and p300/CREB-binding protein family coactivators. Mol. Cell. Biol. 2000, 20, 8933-8943.
25. Teufel, D.P.; Freund, S.M.; Bycroft, M.; Fersht, A.R. Four domains of p300 each bind tightly to a sequence spanning both transactivation subdomains of p53. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 7009-7014.
26. Deng, L.; de la Fuente, C.; Fu, P.; Wang, L.; Donnelly, R.; Wade, J.D.; Lambert, P.; Li, H.; Lee, C.G.; Kashanchi, F. Acetylation of HIV-1 Tat by CBP/P300 increases transcription of integrated HIV-1 genome and enhances binding to core histones. Virology 2000, 277, 278-295.
27. Benkirane, M.; Chun, R.F.; Xiao, H.; Ogryzko, V.V.; Howard, B.H.; Nakatani, Y.; Jeang, K.T. Activation of integrated provirus requires histone acetyltransferase. p300 and P/CAF are coactivators for HIV-1 Tat. J. Biol. Chem. 1998, 273, 24898-24905.
28. Deng, L.; Wang, D.; de la Fuente, C.; Wang, L.; Li, H.; Lee, C.G.; Donnelly, R.; Wade, J.D.; Lambert, P.; Kashanchi, F. Enhancement of the p300 HAT activity by HIV-1 Tat on chromatin DNA. Virology 2001, 289, 312-326.
29. Lusic, M.; Marcello, A.; Cereseto, A.; Giacca, M. Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. EMBO J. 2003, 22, 6550-6561.
30. Zeng, L.; Zhou, M.M. Bromodomain: An acetyl-lysine binding domain. FEBS Lett. 2002, 513, 124-128.
31. Filippakopoulos, P.; Picaud, S.; Mangos, M.; Keates, T.; Lambert, J.P.; Barsyte-Lovejoy, D.; Felletar, I.; Volkmer, R.; Muller, S.; Pawson, T.; et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012, 149, 214-231.
32. Zeng, L.; Zhang, Q.; Gerona-Navarro, G.; Moshkina, N.; Zhou, M.M. Structural basis of sitespecific histone recognition by the bromodomains of human coactivators PCAF and CBP/p300. Structure 2008, 16, 643-652.
33. Tompa, P. Intrinsically unstructured proteins. Trends Biochem. Sci. 2002, 27, 527-533.
34. Wright, P.E.; Dyson, H.J. Intrinsically unstructured proteins: Re-assessing the protein structurefunction paradigm. J. Mol. Biol. 1999, 293, 321-331.
35. Struhl, K. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev. 1998, 12, 599-606.
36. Kuppuswamy, M.; Subramanian, T.; Srinivasan, A.; Chinnadurai, G. Multiple functional domains of Tat, the trans-activator of HIV-1, defined by mutational analysis. Nucleic Acids Res. 1989, 17, 3551-3561.
37. Garcia, J.A.; Harrich, D.; Pearson, L.; Mitsuyasu, R.; Gaynor, R.B. Functional domains required for tat-induced transcriptional activation of the HIV-1 long terminal repeat. EMBO J. 1988, 7, 3143-3147.
38. Jeang, K.T.; Xiao, H.; Rich, E.A. Multifaceted activities of the HIV-1 transactivator of transcription, Tat. J. Biol. Chem. 1999, 274, 28837-28840.
39. Dorn, P.; DaSilva, L.; Martarano, L.; Derse, D. Equine infectious anemia virus tat: Insights into the structure, function, and evolution of lentivirus trans-activator proteins. J. Virol. 1990, 64, 1616-1624.
40. Noiman, S.; Yaniv, A.; Tsach, T.; Miki, T.; Tronick, S.R.; Gazit, A. The Tat protein of equine infectious anemia virus is encoded by at least three types of transcripts. Virology 1991, 184, 521-530.
41. Roy, S.; Katze, M.G.; Parkin, N.T.; Edery, I.; Hovanessian, A.G.; Sonenberg, N. Control of the interferon-induced 68-kilodalton protein kinase by the HIV-1 tat gene product. Science 1990, 247, 1216-1219.
42. Churcher, M.J.; Lamont, C.; Hamy, F.; Dingwall, C.; Green, S.M.; Lowe, A.D.; Butler, J.G.; Gait, M.J.; Karn, J. High affinity binding of TAR RNA by the human immunodeficiency virus type-1 tat protein requires base-pairs in the RNA stem and amino acid residues flanking the basic region. J. Mol. Biol. 1993, 230, 90-110.
43. Dingwall, C.; Ernberg, I.; Gait, M.J.; Green, S.M.; Heaphy, S.; Karn, J.; Lowe, A.D.; Singh, M.; Skinner, M.A.; Valerio, R. Human immunodeficiency virus 1 tat protein binds trans-activationresponsive region (TAR) RNA in vitro. Proc. Natl. Acad. Sci. U. S. A. 1989, 86, 6925-6929.
44. Weeks, K.M.; Crothers, D.M. RNA recognition by Tat-derived peptides: Interaction in the major groove? Cell 1991, 66, 577-588.
45. Chang, Y.N.; Jeang, K.T. The basic RNA-binding domain of HIV-2 Tat contributes to preferential trans-activation of a TAR2-containing LTR. Nucleic Acids Res. 1992, 20, 5465-5472.
46. de Mareuil, J.; Carre, M.; Barbier, P.; Campbell, G.R.; Lancelot, S.; Opi, S.; Esquieu, D.; Watkins, J.D.; Prevot, C.; Braguer, D.; et al. HIV-1 Tat protein enhances microtubule polymerization. Retrovirology 2005, 2, 5.
47. Fiorelli, V.; Barillari, G.; Toschi, E.; Sgadari, C.; Monini, P.; Sturzl, M.; Ensoli, B. IFN-gamma induces endothelial cells to proliferate and to invade the extracellular matrix in response to the HIV-1 Tat protein: Implications for AIDS-Kaposi's sarcoma pathogenesis. J. Immunol. 1999, 162, 1165-1170.
48. Barillari, G.; Gendelman, R.; Gallo, R.C.; Ensoli, B. The Tat protein of human immunodeficiency virus type 1, a growth factor for AIDS Kaposi sarcoma and cytokine-activated vascular cells, induces adhesion of the same cell types by using integrin receptors recognizing the RGD amino acid sequence. Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 7941-7945.
49. Kaehlcke, K.; Dorr, A.; Hetzer-Egger, C.; Kiermer, V.; Henklein, P.; Schnoelzer, M.; Loret, E.; Cole, P.A.; Verdin, E.; Ott, M. Acetylation of Tat defines a cyclinT1-independent step in HIV transactivation. Mol. Cell 2003, 12, 167-176.
50. Bres, V.; Tagami, H.; Peloponese, J.M.; Loret, E.; Jeang, K.T.; Nakatani, Y.; Emiliani, S.; Benkirane, M.; Kiernan, R.E. Differential acetylation of Tat coordinates its interaction with the co-activators cyclin T1 and PCAF. EMBO J. 2002, 21, 6811-6819.
51. Dorr, A.; Kiermer, V.; Pedal, A.; Rackwitz, H.R.; Henklein, P.; Schubert, U.; Zhou, M.M.; Verdin, E.; Ott, M. Transcriptional synergy between Tat and PCAF is dependent on the binding of acetylated Tat to the PCAF bromodomain. EMBO J. 2002, 21, 2715-2723.
52. Pantano, S.; Marcello, A.; Ferrari, A.; Gaudiosi, D.; Sabo, A.; Pellegrini, V.; Beltram, F.; Giacca, M.; Carloni, P. Insights on HIV-1 Tat:P/CAF bromodomain molecular recognition from in vivo experiments and molecular dynamics simulations. Proteins 2006, 62, 1062-1073.
53. de Vries, S.J.; van Dijk, A.D.; Krzeminski, M.; van Dijk, M.; Thureau, A.; Hsu, V.; Wassenaar, T.; Bonvin, A.M. HADDOCK versus HADDOCK: New features and performance of HADDOCK2.0 on the CAPRI targets. Proteins 2007, 69, 726-733.
54. Dominguez, C.; Boelens, R.; Bonvin, A.M. HADDOCK: A protein-protein docking approach based on biochemical or biophysical information. J. Am. Chem. Soc. 2003, 125, 1731-1737.
55. Lowry, J.A.; Gamsjaeger, R.; Thong, S.Y.; Hung, W.; Kwan, A.H.; Broitman-Maduro, G.; Matthews, J.M.; Maduro, M.; Mackay, J.P. Structural analysis of MED-1 reveals unexpected diversity in the mechanism of DNA recognition by GATA-type zinc finger domains. J. Biol. Chem. 2009, 284, 5827-5835.
56. Gelis, I.; Bonvin, A.M.; Keramisanou, D.; Koukaki, M.; Gouridis, G.; Karamanou, S.; Economou, A.; Kalodimos, C.G. Structural basis for signal-sequence recognition by the translocase motor SecA as determined by NMR. Cell 2007, 131, 756-769.
57. Wang, J.; Hu, W.; Cai, S.; Lee, B.; Song, J.; Chen, Y. The intrinsic affinity between E2 and the Cys domain of E1 in ubiquitin-like modifications. Mol. Cell. 2007, 27, 228-237.
58. Lowry, J.A.; Gamsjaeger, R.; Thong, S.Y.; Hung, W.; Kwan, A.H.; Broitman-Maduro, G.; Matthews, J.M.; Maduro, M.; Mackay, J.P. Structural analysis of MED-1 reveals unexpected diversity in the mechanism of DNA recognition by GATA-type zinc finger domains. J. Biol. Chem. 2009, 284, 5827-5835.
59. Haynes, S.R.; Dollard, C.; Winston, F.; Beck, S.; Trowsdale, J.; Dawid, I.B. The bromodomain: A conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Res. 1992, 20, 2603.
60. Tamkun, J.W. The role of brahma and related proteins in transcription and development. Curr. Opin. Genet. Dev. 1995, 5, 473-477.
61. Tamkun, J.W.; Deuring, R.; Scott, M.P.; Kissinger, M.; Pattatucci, A.M.; Kaufman, T.C.; Kennison, J.A. brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 1992, 68, 561-572.
62. Umehara, T.; Nakamura, Y.; Jang, M.K.; Nakano, K.; Tanaka, A.; Ozato, K.; Padmanabhan, B.; Yokoyama, S. Structural basis for acetylated histone H4 recognition by the human BRD2 bromodomain. J. Biol. Chem. 2010, 285, 7610-7618.
63. Hewings, D.S.; Wang, M.; Philpott, M.; Fedorov, O.; Uttarkar, S.; Filippakopoulos, P.; Picaud, S.; Vuppusetty, C.; Marsden, B.; Knapp, S.; et al. 3,5-dimethylisoxazoles act as acetyl-lysinemimetic bromodomain ligands. J. Med. Chem. 2011, 54, 6761-6770.
64. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual molecular dynamics. J. Mol. Graph. 1996, 14, 33-38, 27-28.
65. Case, D.A.; Darden, T.A.; Cheatham, T.E.; Simmerling, C.L.; Wang, J.; Duke, R.E.; Luo, R.; Walker, R.C.; Zhang, W.; Merz, K.M.; et al. Amber 11; University of California: San Francisco, CA, USA, 2010.
66. Machado, M.R.; Dans, P.D.; Pantano, S. Isoform-specific determinants in the HP1 binding to histone 3: Insights from molecular simulations. Amino Acids 2010, 38, 1571-1581.
67. De Mori, G.M.; Colombo, G.; Micheletti, C. Study of the Villin headpiece folding dynamics by combining coarse-grained Monte Carlo evolution and all-atom molecular dynamics. Proteins 2005, 58, 459-471.
68. HADDOCK, version 2.1 program; free of charge for non commercial users. Available online: http://www.nmr.chem.uu.nl/haddock/download.html (accessed on 31 July 2012).
69. van Dijk, A.D.; Bonvin, A.M. Solvated docking: Introducing water into the modelling of biomolecular complexes. Bioinformatics 2006, 22, 2340-2347.
70. Hornak, V.; Abel, R.; Okur, A.; Strockbine, B.; Roitberg, A.; Simmerling, C. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 2006, 65, 712-725.
71. Jorgensen, W.L.; Chandrasekhar, J.; Madura, J.D.; Impey, R.W.; Klein, M.L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 1983, 79, 926.
72. Makov, G.; Payne, M.C. Periodic boundary conditions in ab initio calculations. Phys. Rev. B Condens Matter 1995, 51, 4014-4022.
73. Darden, T.; York, D.; Pedersen, L. Particle mesh Ewald: An N [center-dot] log(N) method for Ewald sums in large systems. J. Chem. Phys. 1993, 98, 10089-10092.
74. Ryckaert, J.-P.; Ciccotti, G.; Berendsen, H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J. Comput. Phys. 1977, 23, 327-341.
75. Berendsen, H.J.C.; Postma, J.P.M.; van Gunsteren, W.F.; DiNola, A.; Haak, J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684-3690.
76. Phillips, J.C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R.D.; Kale, L.; Schulten, K. Scalable molecular dynamics with NAMD. J. Comput. Chem. 2005, 26, 1781-1802.
77. Wallace, A.C.; Laskowski, R.A.; Thornton, J.M. LIGPLOT: A program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 1995, 8, 127-134.
78. Zeng, L.; Li, J.; Muller, M.; Yan, S.; Mujtaba, S.; Pan, C.; Wang, Z.; Zhou, M.M. Selective small molecules blocking HIV-1 Tat and coactivator PCAF association. J. Am. Chem. Soc. 2005, 127, 2376-2377.
79. Pan, C.; Mezei, M.; Mujtaba, S.; Muller, M.; Zeng, L.; Li, J.; Wang, Z.; Zhou, M.M. Structure-guided optimization of small molecules inhibiting human immunodeficiency virus 1 Tat association with the human coactivator p300/CREB binding protein-associated factor. J. Med. Chem. 2007, 50, 2285-2288.
80. Filippakopoulos, P.; Qi, J.; Picaud, S.; Shen, Y.; Smith, W.B.; Fedorov, O.; Morse, E.M.; Keates, T.; Hickman, T.T.; Felletar, I.; et al. Selective inhibition of BET bromodomains. Nature 2010, 468, 1067-1073.
81. Umehara, T.; Nakamura, Y.; Wakamori, M.; Ozato, K.; Yokoyama, S.; Padmanabhan, B. Structural implications for K5/K12-di-acetylated histone H4 recognition by the second bromodomain of BRD2. FEBS Lett. 2010, 584, 3901-3908.
82. Mujtaba, S.; He, Y.; Zeng, L.; Yan, S.; Plotnikova, O.; Sachchidanand; Sanchez, R.; Zeleznik-Le, N.J.; Ronai, Z.; Zhou, M.M. Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol. Cell 2004, 13, 251-263.
83. Chandy, M.; Gutierrez, J.L.; Prochasson, P.; Workman, J.L. SWI/SNF displaces SAGAacetylated nucleosomes. Eukaryot. Cell 2006, 5, 1738-1747.
84. Singh, M.; D'Silva, L.; Holak, T.A. DNA-binding properties of the recombinant high-mobilitygroup-like AT-hook-containing region from human BRG1 protein. Biol. Chem. 2006, 387, 1469-1478.
85. Huang, H.; Zhang, J.; Shen, W.; Wang, X.; Wu, J.; Shi, Y. Solution structure of the second bromodomain of Brd2 and its specific interaction with acetylated histone tails. BMC Struct. Biol. 2007, 7, 57.
86. Chung, C.W.; Coste, H.; White, J.H.; Mirguet, O.; Wilde, J.; Gosmini, R.L.; Delves, C.; Magny, S.M.; Woodward, R.; Hughes, S.A.; et al. Discovery and characterization of small molecule inhibitors of the BET family bromodomains. J. Med. Chem. 2011, 54, 3827-3838.
87. Chung, C.W.; Witherington, J. Progress in the discovery of small-molecule inhibitors of bromodomain-Histone interactions. J. Biomol. Screen 2011, 16, 1170-1185.
88. Chung, C.W.; Dean, A.W.; Woolven, J.M.; Bamborough, P. Fragment-based discovery of bromodomain inhibitors part 1: Inhibitor binding modes and implications for lead discovery. J. Med. Chem. 2012, 55, 576-586.
89. Filippakopoulos, P.; Picaud, S.; Fedorov, O.; Keller, M.; Wrobel, M.; Morgenstern, O.; Bracher, F.; Knapp, S. Benzodiazepines and benzotriazepines as protein interaction inhibitors targeting bromodomains of the BET family. Bioorg. Med. Chem. 2012, 20, 1878-1886.