Insights into a mutation-assisted lateral drug escape mechanism from the HIV-1 protease active site

Biochemistry

Volumn 46, Issue 51, 2007, Pages 14865-14877

  Sadiq, S Kashif ^a   Wan, Shunzhou ^a   Coveney, Peter V ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; COMPUTER SIMULATION; ENZYMES; HYDROGEN BONDS; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR DYNAMICS;

FLAP-INHIBITOR MOTION; HYDROPHOBIC INTERACTIONS; LATERAL DRUG EXPULSION; MUTATION;

DRUG THERAPY;

GLYCINE; LEUCINE; METHIONINE; SAQUINAVIR; SOLVENT; VALINE;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISSOCIATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME KINETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; STEREOCHEMISTRY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, VIRAL; HIV PROTEASE; HIV-1; MODELS, MOLECULAR; MUTATION; PROTEASE INHIBITORS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 37349127373     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700864p     Document Type: Article

References (50)

1. Wlodawer, A., and Erickson, J. W. (1993) Structure-based inhibitors of HIV-1 protease, Annu. Rev. Biochem. 62, 543-585.
2. Wlodawer, A., and Vondrasek, J. (1998) Inhibitors of HIV-1 Protease: A Major Success of Structure-Assissted Drug Design, Annu. Rev. Biophys. Biomol Struct. 27, 249-284.
3. Hoffman, N. G., Schiffer, C. A., and Swanstrom, R. (2003) Covariation of amino acid positions in HIV-1 protease, Virology 314, 536-548.
4. Svicher, V., Ceccherini-Silberstein, F., Erba, F., Santoro, M., Gori, C., Bellochi, M. C., Giannella, S., Trotta, M. P., d'Arminio Monforte, A., Antinori, A., and Perno, C. F. (2005) Novel human immunodeficiency virus type 1 protease mutations potentially involved in resistance to protease inhibitors, Antimicrob. Agents Chemother. 49, 2015-2025.
5. Wu, T. D., Schiffer, C. A., Gonzales, M., Taylor, J., Kantor, R., Chou, S., Israelski, D., Zolopa, A. R., Fessel, W. J., and Shafer, R. W. (2003) Mutation Patterns and Structural Correlates in Human Immunodeficiency Virus Type 1 Protease following Different Protease Inhibitor Treatments, J. Virol. 77, 4836-4847.
6. Yahi, N., Tamalet, C., Tourres, C., Tivoli, N., Ariasi, F., Volot, F., Gastaut, J.-A., Gallais, H., Moreau, J., and Fantini, J. (1999) Mutation patterns of the reverse transcriptase and protease genes in human immunodeficiency virus type 1-infected patients undergoing combination therapy: Survey of 787 sequences, J. Clin. Microbiol. 37, 4099-4106.
7. Maschera, B., Darby, G., Palu, G., Wright, L. L., Tisdale, M., Myers, R., Blair, E. D., and Furfine, E. S. (1996) Human Immunodeficiency Virus: Mutations in the viral protease that confer resistance to saquinavir increase the dissociation rate constant of the protease-saquinavir complex, J. Biol. Chem. 271, 33231-33235.
8. Ohtaka, H., Schon, A., and Freire, E. (2003) Multidrug resistance to HIV-1 protease inhibition requires cooperative coupling between distal mutations, Biochemistry 42, 13659-13666.
9. Todd, M. J., Luque, I., Velazquez-Campoy, A., and Freire, E. (2000) Thermodynamic Basis of Resistance to HIV-1 Protease Inhibition: Calorimetric Analysis of the V82F/I84V Active Site Resistant Mutant, Biochemistry 39, 11876-11883.
10. Lepsik, M., Kriz, Z., and Havlas, Z. (2004) Efficiency of a Second-Generation HIV-1 Protease Inhibitor Studied by Molecular Dynamics and Absolute Binding Free Energy Calculations, Proteins: Struct. Funct. Bioinf. 57, 279-293.
11. Wang, W., and Kollman, P. A. (2001) Computational study of protein specificity: The molecular basis of HIV-1 protease drug resistance, Proc. Natl. Acad. Sci. U.S.A. 98, 14937-14942.
12. Zoete, V., Michielin, O., and Karplus, M. (2003) Protein-ligand binding free energy estimation using molecular mechanics and continuum electrostatics: Application to HIV-1 protease inhibitors, J. Comput.-Aided Mol. Des. 17, 861-880.
13. Collins, J. R., Burt, S. K., and Erickson, J. W. (1995) Flap opening in HIV-1 protease simulated by 'activated' molecular dynamics, Nat. Struct. Biol. 2, 334-338.
14. Piana, S., Carloni, P., and Rothlisberger, U. (2002) Drug resistance in HIV-1 protease: Flexibility-assisted mechanism of compensatory mutations, Protein Sci. 11, 2393-2402.
15. Johnson, V. A., Brun-Vezinet, F., Clotet, B., Conway, B., Kuritzkes, D. R., Pillay, D., Schapiro, J., Telenti, A., and Richman, D. (2005) Update of the Drug Resistance Mutations in HIV-1: 2005, Int. AIDS Soc. - U.S.A. 13, 51-57.
16. Furfine, E. S., D'Souza, E., Ingold, K. J., Leban, J. J., Spector, T., and Porter, D. J. T. (1992) Two-step binding mechanism for HIV protease inhibitors, Biochemistry 31, 7886-7891.
17. Zoete, V., Michielin, O., and Karplus, M. (2002) Relation between Sequence and Structure of HIV-1 Protease Inhibitor Complexes: A Model System for the Analysis of Protein Flexibility, J. Mol. Biol. 315, 21-52.
18. Kumar, M., and Hosur, M. V. (2003) Adaptability and flexibility of HIV-1 protease, Eur. J. Biochem. 270, 1231-1239.
19. Scott, W. R. P., and Schiffer, C. A. (2000) Curling of Flap Tips in HIV-1 Protease as a Mechanism for Substrate Entry and Tolerance of Drug Resistance, Structure 8, 1259-1265.
20. Wang, W., and Kollman, P. A. (2000) Free energy calculations on dimer stability of the hiv protease using molecular dynamics and a continuum solvent model, J. Mol. Biol. 303, 567-582
21. Hornak, V., Okur, A., Rizzo, R. C., and Simmerling, C. (2006b) HIV-1 protease flaps spontaneously open and reclose in molecular dynamics simulations, Proc. Natl. Acad. Sci. U.S.A. 103, 915-920.
22. Freedberg, D. I., Ishima, R., Jacob, J., Wang, Y.-X., Kustanovich, I., Louis, J. M., and Torchia, D. A. (2002) Rapid structural fluctuations of the free HIV protease flaps in solution: Relationship to crystal structures and comparison with predictions of dynamics calculations, Protein Sci. 11, 221-232.
23. Ishima, R., Freedberg, D. I., Wang, Y. X., Louis, J. M., and Torchia, D. A. (1999) Flap opening and dimer-interface flexibility in the free and inhibitor-bound HIV protease, and their implications for function, Struct. Fold. Des. 7, 1047-1055.
24. Rose, J. R., Babe, L. M., and Craik, C. S. (2006) The Open Structure of a Multi-Drug-Resistant HIV-1 Protease is Stabilized by Crystal Packing Contacts, J. Am. Chem. Soc. 128, 13360-13361.
25. Toth, G., and Borics, A. (2006a) Closing of the Flaps of HIV-1 Protease Induced by Substrate Binding: A Model of a Flap Closing Mechanism in Retroviral Aspartic Proteases, Biochemistry 45, 6606-6614.
26. Toth, G., and Borics, A. (2006b) Flap opening mechanism of HIV-1 protease, J. Mol. Graphics Modell. 24, 465-474.
27. Perryman, A. L., Lin, J., and McCammon, J. A. (2004) HIV-1 protease molecular dynamics of a wild-type and of the V82F/I84V mutant: Possible contributions to drug resistance and a potential new target site for drugs, Protein Sci. 13, 1108-1123.
28. Chang, C.-E., Shen, T., Trylska, J., Tozzini, V., and McCammon, J. A. (2006) Gated binding of ligands to HIV-1 protease: Brownian dynamics simulations in a coarse-grained model, Biophys. J. 90, 3880-3885.
29. Balsera, M. A., Wriggers, W., Oono, Y., and Schulten, K. (1996) Principal component analysis and long time protein dynamics, J. Phys. Chem. 100, 2567-2572.
30. Isralewitz, B., Gao, M., and Schulten, K. (2001) Steered molecular dynamics and mechanical functions of proteins, Curr. Opin. Struct. Biol. 11, 224-230.
31. Schuettelkopf, A. W., and van Aalten, D. M. F. (2004) PRODRG - a tool for high-throughput crystallography of protein-ligand complexes, Acta Crystallogr. D60, 1355-1363.
32. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robe, M. A., Cheeseman, J. R., Zakrzewski, V. G., Montgomery, J. A., Stratman, J., Burant, J. C., et al. (2002) Gaussian 98, Gaussian Inc., Pittsburgh, PA
33. Wang, J., Wolf, R. M., Case, D. A., and Kollman, P. A. (2004) Development and Testing of a General AMBER Force Field (GAFF), J. Comput. Chem. 25, 1157-1174.
34. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD - Visual Molecular Dynamics, J. Mol. Graphics 14, 33-38.
35. Wang, J. M., Cieplak, P., and Kollman, P. A. (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules, J. Comput. Chem. 21, 1049-1074.
36. Kovalskyy, D., Dubyna, V., Mark, A. E., and Korenelyuk, A. (2005) A molecular dynamics study of the structural stability of HIV-1 protease under physiological conditions: The role of Na+ ions in stabilizing the active site, Proteins: Struct. Funct. Bioinf. 58, 450-458.
37. Schafmeister, C. E. A. F., Ross, W. S., and Romanovski, V. (1995) LEaP, University of California, San Francisco, CA.
38. Case, D. A., Cheatham, T., Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerlang, C., Wang, B., and Woods, R. (2005) The Amber biomolecular simulations programs, J. Comput. Chem. 26, 1668-1688.
39. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water, J. Chem. Phys. 79, 926-935.
40. Kale, L., Skeel, R., Bhandarkar, M., Brunner, R., Gursoy, A., Krawetz, N., Phillips, J., Shinozaki, A., Varadarajan, K., and Schulten, K. (1999) NAMD2: Greater scalability for parallel molecular dynamics, J. Comput. Phys. 151, 283-312.
41. Essmann, U., Perera, L., Berkowitz, M. L., and Darden, T. (1995) A smooth particle mesh Ewald method, J. Chem. Phys. 103, 8577-9593.
42. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes, J. Comput. Phys. 23, 327-341.
43. Meagher, K. L., and Carlson, H. A. (2005) Solvation Influences Flap Collapse in HIV-1 Protease, Proteins: Struct. Funct. Bioinf. 58, 119-125.
44. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
45. Mongan, J. (2004) Interactive Essential Dynamics, J. Comput. - Aided Mol. Des. 18, 433-436.
46. Israilev, S., Stepaniants, S., Balsera, M., Oono, Y., and Schulten, K. (1997) Molecular dynamics study of unbinding of the avidin-biotin complex, Biophys. J. 72, 1568-1581.
47. Rose, R. B., Craik, C. S., and Stroud, R. M. (1998) Domain flexibility in retroviral proteases: Structural implications for drug resistance mutations, Biochemistry 37, 2607-2621.
48. Kurt, N., Scott, W. R. P., Schiffer, C. A., and Haliloglu, T. (2003) Cooperative Fluctuations of Unliganded and Substrate-Bound HIV-1 Protease: A Structure-Based Analysis on a Variety of Conformations From Crystallography and Molecular Dynamics Simulations, Proteins: Struct. Funct. Genet. 51, 409-422.
49. Wittayanarakul, K., Aruksakunwong, O., Saen-oon, S., Chantratita, W., Parasuk, V., Sompornpisut, P., and Hannongbua, S. (2005) Insights into saquinavir resistance in the G48V HIV-1 protease: Quantum calculations and molecular dynamic simulations, Biophys. J. 88, 867-879.
50. Wriggers, W., and Schulten, K. (1999) Investigating a Back Door Mechansim of Actin Phosphate Release by Steered Molecular Dynamics, Proteins: Struct. Funct. Genet. 35, 262-273.