How does darunavir prevent HIV-1 protease dimerization?

Journal of Chemical Theory and Computation

Volumn 8, Issue 5, 2012, Pages 1786-1794

  Huang, Danzhi ^a   Caflisch, Amedeo ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84860733278     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct300032r     Document Type: Article

References (46)

1. Kohl, N. E.; Emini, E. A.; Schleif, W. A.; Davis, L. J.; Heimbach, J. C.; Dixon, R. A.; Scolnick, E. M.; Sigal, I. S. Active human immunodeficiency virus protease is required for viral infectivity Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 4686-4690
2. Rang, H. P.; Dale, M. M.; Ritter, J. M.; Flower, R. J. Rang and Dale's Pharmacology, 6 th ed.; Churchill Livingstone Elsevier: Philadelphia, PA, 2007.
3. Watkins, T.; Resch, W.; Irlbeck, D.; Swanstrom, R. Selection of high-level resistance to human immunodeficiency virus type 1 protease inhibitors Antimicrob. Agents Chemother. 2003, 47, 759-769 (Pubitemid 36158112)
4. Ferrer, E.; Podzamczer, D.; Arnedo, M.; Fumero, E.; McKenna, P.; Rinehart, A.; Prez, J. L.; Barber, M. J.; Pumarola, T.; Gatell, J. M.; Team, C. S. Genotype and phenotype at baseline and at failure in human immunodeficiency virus,infected antiretroviral-naive patients in a randomized trial comparing zidovudine and lamivudine plus nelfinavir or nevirapine J. Infect. Dis. 2003, 187, 687-690 (Pubitemid 36250035)
5. MacArthur, R. D. Darunavir: promising initial results Lancet 2007, 369, 1143-1144 (Pubitemid 46533997)
6. Ghosh, A. K.; Dawson, Z. L.; Mitsuya, H. Darunavir, a conceptually new HIV-1 protease inhibitor for the treatment of drug-resistant HIV Bioorg. Med. Chem. 2007, 15, 7576-7580 (Pubitemid 47575929)
7. Madruga, J. V.; Berger, D.; McMurchie, M.; Suter, F.; Banhegyi, D.; Ruxrungtham, K.; Norris, D.; Lefebvre, E.; de Bthune, M.-P.; Tomaka, F.; Pauw, M. D.; Vangeneugden, T.; Spinosa-Guzman, S. Efficacy and safety of darunavir-ritonavir compared with that of lopinavir-ritonavir at 48 weeks in treatment-experienced, HIV-infected patients in titan: a randomised controlled phase III trial Lancet 2007, 370, 49-58 (Pubitemid 47023100)
8. Koh, Y.; Matsumi, S.; Das, D.; Amano, M.; Davis, D.; Li, J.; Leschenko, S.; Baldridge, A.; Shioda, T.; Yarchoan, R. Potent inhibition of HIV-1 replication by novel non-peptidyl small molecule inhibitors of protease dimerization J. Biol. Chem. 2007, 282, 28709
9. Koh, Y.; Aoki, M.; Danish, M.; Aoki-Ogata, H.; Amano, M.; Das, D.; Shafer, R.; Ghosh, A.; Mitsuya, H. Loss of protease dimerization inhibition activity of darunavir is associated with the acquisition of resistance to darunavir by HIV-1 J. Virol. 2011, 85, 10079-10089
10. Levy, Y.; Caflisch, A. Flexibility of monomeric and dimeric HIV-1 protease J. Phys. Chem. B 2003, 107, 3068-3079
11. Levy, Y.; Caflisch, A.; Onuchic, J. N.; Wolynes, P. G. The folding and dimerization of HIV-1 protease: Evidence for a stable monomer from simulations J. Mol. Biol. 2004, 340, 67-79 (Pubitemid 38739438)
12. Broglia, R.; Levy, Y.; Tiana, G. HIV-1 protease folding and the design of drugs which do not create resistance Curr. Opin. Struct. Biol. 2008, 18, 60-66
13. Bonomi, M.; Barducci, A.; Gervasio, F. L.; Parrinello, M. Multiple routes and milestones in the folding of HIV-1 protease monomer PLoS ONE 2010, 5, e13208
14. Ishima, R.; Ghirlando, R.; Tözsér, J.; Gronenborn, A.; Torchia, D.; Louis, J. Folded monomer of HIV-1 protease J. Biol. Chem. 2001, 276, 49110
15. Louis, J.; Ishima, R.; Nesheiwat, I.; Pannell, L.; Lynch, S.; Torchia, D.; Gronenborn, A. Revisiting monomeric HIV-1 protease J. Biol. Chem. 2003, 278, 6085-6092
16. Ishima, R.; Torchia, D.; Lynch, S.; Gronenborn, A.; Louis, J. Solution structure of the mature HIV-1 protease monomer J. Biol. Chem. 2003, 278, 43311-43319
17. Louis, J.; Ishima, R.; Aniana, A.; Sayer, J. Revealing the dimer dissociation and existence of a folded monomer of the mature HIV-2 protease Protein Sci. 2009, 18, 2442-2453
18. Hartl, M.; Schweimer, K.; Reger, M.; Schwarzinger, S.; Bodem, J.; Rosch, P.; Wohrl, B. Formation of transient dimers by a retroviral protease Biochem. J. 2010, 427, 197-203
19. Kovalevsky, A.; Liu, F.; Leshchenko, S.; Ghosh, A.; Louis, J.; Harrison, R.; Weber, I. Ultra-high resolution crystal structure of HIV-1 protease mutant reveals two binding sites for clinical inhibitor TMC114 J. Mol. Biol. 2006, 363, 161-173 (Pubitemid 44437563)
20. Ghosh, A.; Dawson, Z.; Mitsuya, H. Darunavir, a conceptually new HIV-1 protease inhibitor for the treatment of drug-resistant HIV Bioorg. Med. Chem. 2007, 15, 7576-7580 (Pubitemid 47575929)
21. Dierynck, I.; De Wit, M.; Gustin, E.; Keuleers, I.; Vandersmissen, J.; Hallenberger, S.; Hertogs, K. Binding kinetics of darunavir to human immunodeficiency virus type 1 protease explain the potent antiviral activity and high genetic barrier J. Virol. 2007, 81, 13845
22. Kovalevsky, A.; Ghosh, A.; Weber, I. Solution kinetics measurements suggest HIV-1 protease has two binding sites for darunavir and amprenavir J. Med. Chem. 2008, 51, 6599-6603
23. Darke, P.; Jordan, S.; Hall, D.; Zugay, J.; Shafer, J.; Kuo, L. Dissociation and association of the HIV-1 protease dimer subunits: equilibria and rates Biochemistry 1994, 33, 98-105 (Pubitemid 24046501)
24. Berendsen, H.; van der Spoel, D.; Van Drunen, R. Gromacs: A message-passing parallel molecular dynamics implementation Comput. Phys. Commun. 1995, 91, 43-56
25. Hess, B.; Kutzner, C.; Van Der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 2008, 4, 435-447
26. MacKerell, A. D.; Bashford, D.; Bellott; Dunbrack, R. L.; Evanseck, J. D.; Field, M. J.; Fischer, S.; Gao, J.; Guo, H.; Ha, S.; Joseph-McCarthy, D.; Kuchnir, L.; Kuczera, K.; Lau, F. T. K.; Mattos, C.; Michnick, S.; Ngo, T.; Nguyen, D. T.; Prodhom, B.; Reiher, W. E.; Roux, B.; Schlenkrich, M.; Smith, J. C.; Stote, R.; Straub, J.; Watanabe, M.; Wirkiewicz-Kuczera, J.; Yin, D.; Karplus, M. All-atom empirical potential for molecular modeling and dynamics studies of proteins J. Phys. Chem. B 1998, 102, 3586-3616 (Pubitemid 128576688)
27. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J.; Impey, R. W.; Klein, M. L. Comparison of simple potential functions for simulating liquid water J. Chem. Phys. 1983, 79, 926-935
28. Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J.; Darian, E.; Guvench, O.; Lopes, P.; Vorobyov, I.; Mackerell, A. D. J. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 2010, 31, 671-690
29. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general amber force field J. Comput. Chem. 2004, 25, 1157-1174
30. Cai, Y.; Schiffer, C. A. Decomposing the energetic impact of drug resistant mutations in hiv-1 protease on binding drv J. Chem. Theory Comput. 2010, 6, 1358-1368
31. Darden, T.; York, D.; Pedersen, L. G. Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems J. Chem. Phys. 1993, 98, 10089
32. Bussi, G.; Donadio, D.; Parrinello, M. Canonical sampling through velocity rescaling J. Chem. Phys. 2007, 126, 014101
33. 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
34. Brooks, B. R.; Brooks, C. L., III; Mackerell, A. D. J.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: the biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-614
35. Seeber, M.; Cecchini, M.; Rao, F.; Settanni, G.; Caflisch, A. Wordom: a program for efficient analysis of molecular dynamics simulations Bioinformatics 2007, 23, 2625
36. Seeber, M.; Felline, A.; Raimondi, F.; Muff, S.; Friedman, R.; Rao, F.; Caflisch, A.; Fanelli, F. Wordom: A user-friendly program for the analysis of molecular structures, trajectories, and free energy surfaces J. Comput. Chem. 2011, 32, 1183-1194
37. Krivov, S.; Karplus, M. One-dimensional free-energy profiles of complex systems: Progress variables that preserve the barriers J. Phys. Chem. B 2006, 110, 12689-12698 (Pubitemid 44139460)
38. Krivov, S. V.; Muff, S.; Caflisch, A.; Karplus, M. One-dimensional barrier-preserving free-energy projections of a-sheet miniprotein: New insights into the folding process J. Phys. Chem. B 2008, 112, 8701-8714
39. Freedberg, D.; Ishima, R.; Jacob, J.; Wang, Y.; Kustanovich, I.; Louis, J.; Torchia, D. Rapid structural fluctuations of the free HIV protease flaps in solution: relationship to crystal structures and comparison with predictions of dynamics calculations Protein Sci. 2002, 11, 221-232 (Pubitemid 34075785)
40. Ishima, R.; Freedberg, D.; Wang, Y.; Louis, J.; Torchia, D. Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function Structure 1999, 7, 1047-1055 (Pubitemid 29436502)
41. Eyal, E.; Gerzon, S.; Potapov, V.; Edelman, M.; Sobolev, V. The limit of accuracy of protein modeling: influence of crystal packing on protein structure J. Mol. Biol. 2005, 351, 431-442 (Pubitemid 41007760)
42. Case, D. A.; Cheatham, T. E.; Darden, T.; Gohlke, H.; Luo, R.; Merz, K. M.; Onufriev, A.; Simmerling, C.; Wang, B.; Woods, R. J. The amber biomolecular simulation programs J. Comput. Chem. 2005, 26, 1668-1688 (Pubitemid 43076180)
43. Liu, F.; Kovalevsky, A.; Tie, Y.; Ghosh, A.; Harrison, R.; Weber, I. Effect of flap mutations on structure of HIV-1 protease and inhibition by saquinavir and darunavir J. Mol. Biol. 2008, 381, 102-115
44. Sayer, J.; Liu, F.; Ishima, R.; Weber, I.; Louis, J. Effect of the active site D25N mutation on the structure, stability, and ligand binding of the mature HIV-1 protease J. Biol. Chem. 2008, 283, 13459-13470
45. 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
46. DeLano, W. L. The PyMOL Molecular Graphics System; DeLano Scientific: San Carlos, CA, 2002; http://www.pymol.org.