Capturing the reaction pathway in near-atomic-resolution crystal structures of HIV-1 protease

Biochemistry

Volumn 51, Issue 39, 2012, Pages 7726-7732

  Shen, Chen Hsiang ^a   Tie, Yunfeng ^a,b   Yu, Xiaxia ^a   Wang, Yuan Fang ^a   Kovalevsky, Andrey Y ^a,c   Harrison, Robert W ^a   Weber, Irene T ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL AGENTS; CARBONYL OXYGEN; DRUG RESISTANCE; GEOMETRIC DETAILS; HIV-1 PROTEASE; LIGAND-FREE; PRODUCT COMPLEX; PRODUCT RELEASE; PROTEOLYTIC REACTION; REACTION MECHANISM; REACTION PATHWAYS; STRUCTURAL DETAILS; TETRAHEDRAL INTERMEDIATES; TWO-PRODUCT; WATER MOLECULE; WILD TYPES;

AMIDES; ATOMS; CARBOXYLATION; HYDROGEN BONDS; MOLECULES; OXYGEN;

REACTION KINETICS;

AMIDE; ANTIVIRUS AGENT; ASPARAGINE; ASPARTIC ACID; CARBON; CARBONYL DERIVATIVE; ENZYME; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; PEPTIDE; WATER;

ARTICLE; BINDING SITE; CONFORMATION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME MECHANISM; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN BOND; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REACTION ANALYSIS; SUBSTITUTION REACTION; WILD TYPE;

AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HIV PROTEASE; HIV-1; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84867065402     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi3008092     Document Type: Article

References (32)

1. Weber, I. T., Kovalevsky, A. Y., and Harrison, R. W. (2007) Structures of HIV Protease Guide Inhibitor Design to Overcome Drug Resistance. Frontiers in Drug Design & Discovery, Vol. 3, pp 45-62, Bentham Science Publishers, Oak Park, IL.
2. Weber, I. and Agniswamy, J. (2009) HIV-1 Protease: Structural Perspectives on Drug Resistance Viruses 1, 1110-1136
3. Brik, A. and Wong, C. H. (2003) HIV-1 protease: Mechanism and drug discovery Org. Biomol. Chem. 1, 5-14
4. 18O isotope exchange Biochemistry 30, 8441-8453
5. Adachi, M., Ohhara, T., Kurihara, K., Tamada, T., Honjo, E., Okazaki, N., Arai, S., Shoyama, Y., Kimura, K., Matsumura, H., Sugiyama, S., Adachi, H., Takano, K., Mori, Y., Hidaka, K., Kimura, T., Hayashi, Y., Kiso, Y., and Kuroki, R. (2009) Structure of HIV-1 protease in complex with potent inhibitor KNI-272 determined by high-resolution X-ray and neutron crystallography Proc. Natl. Acad. Sci. U.S.A. 106, 4641-4646
6. Pearson, A. R. and Owen, R. L. (2009) Combining X-ray crystallography and single-crystal spectroscopy to probe enzyme mechanisms Biochem. Soc. Trans. 37, 378-381
7. Veerapandian, B., Cooper, J. B., Sali, A., Blundell, T. L., Rosati, R. L., Dominy, B. W., Damon, D. B., and Hoover, D. J. (1992) Direct observation by X-ray analysis of the tetrahedral "intermediate" of aspartic proteinases Protein Sci. 1, 322-328
8. Coates, L., Tuan, H. F., Tomanicek, S., Kovalevsky, A., Mustyakimov, M., Erskine, P., and Cooper, J. (2008) The catalytic mechanism of an aspartic proteinase explored with neutron and X-ray diffraction J. Am. Chem. Soc. 130, 7235-7237
9. Rose, R. B., Craik, C. S., Douglas, N. L., and Stroud, R. M. (1996) Three-dimensional structures of HIV-1 and SIV protease product complexes Biochemistry 35, 12933-12944
10. Kumar, M., Prashar, V., Mahale, S., and Hosur, M. V. (2005) Observation of a tetrahedral reaction intermediate in the HIV-1 protease-substrate complex Biochem. J. 389, 365-371
11. Das, A., Mahale, S., Prashar, V., Bihani, S., Ferrer, J. L., and Hosur, M. V. (2010) X-ray snapshot of HIV-1 protease in action: Observation of tetrahedral intermediate and short ionic hydrogen bond SIHB with catalytic aspartate J. Am. Chem. Soc. 132, 6366-6373
12. Kovalevsky, A. Y., Chumanevich, A. A., Liu, F., Louis, J. M., and Weber, I. T. (2007) Caught in the Act: The 1.5 Å resolution crystal structures of the HIV-1 protease and the I54V mutant reveal a tetrahedral reaction intermediate Biochemistry 46, 14854-14864
13. Johnson, V. A., Calvez, V., Gunthard, H. F., Paredes, R., Pillay, D., Shafer, R., Wensing, A. M., and Richman, D. D. (2011) 2011 update of the drug resistance mutations in HIV-1 Top. Antiviral Med. 19, 156-164
14. Wu, T. D., Schiffer, C. A., Gonzales, M. J., 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
15. Pazhanisamy, S., Stuver, C. M., Cullinan, A. B., Margolin, N., Rao, B. G., and Livingston, D. J. (1996) Kinetic characterization of human immunodeficiency virus type-1 protease-resistant variants J. Biol. Chem. 271, 17979-17985
16. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 267, 307-326
17. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C., and Read, R. J. (2005) Likelihood-enhanced fast translation functions Acta Crystallogr. D61, 458-464
18. Kovalevsky, A. Y., Tie, Y., Liu, F., Boross, P. I., Wang, Y. F., Leshchenko, S., Ghosh, A. K., Harrison, R. W., and Weber, I. T. (2006) Effectiveness of nonpeptide clinical inhibitor TMC-114 on HIV-1 protease with highly drug resistant mutations D30N, I50V, and L90M J. Med. Chem. 49, 1379-1387
19. Mahalingam, B., Louis, J. M., Hung, J., Harrison, R. W., and Weber, I. T. (2001) Structural implications of drug-resistant mutants of HIV-1 protease: High-resolution crystal structures of the mutant protease/substrate analogue complexes Proteins 43, 455-464
20. Sheldrick, G. M. and Schneider, T. R. (1997) SHELXL: High-resolution refinement Methods Enzymol. 277, 319-343
21. Emsley, P. and Cowtan, K. (2004) Coot: Model-Building Tools for Molecular Graphics Acta Crystallogr. D60, 2126-2132
22. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
23. Tie, Y. (2006) Crystallographic Analysis and Kinetic Studies of HIV-1 Protease and Drug-Resistant Mutants. In Biology, pp 131-141, Georgia State University, Atlanta.
24. Kovalevsky, A. Y., Liu, F., Leshchenko, S., Ghosh, A. K., Louis, J. M., Harrison, R. W., and Weber, I. T. (2006) Ultra-high resolution crystal structure of HIV-1 protease mutant reveals two binding sites for clinical inhibitor TMC114 J. Mol. Biol. 363, 161-173
25. Mildner, A. M., Rothrock, D. J., Leone, J. W., Bannow, C. A., Lull, J. M., Reardon, I. M., Sarcich, J. L., Howe, W. J., Tomich, C. S., and Smith, C. W. 1994, The HIV-1 protease as enzyme and substrate: Mutagenesis of autolysis sites and generation of a stable mutant with retained kinetic properties Biochemistry 33, 9405-9413
26. Shen, C. H., Wang, Y. F., Kovalevsky, A. Y., Harrison, R. W., and Weber, I. T. (2010) Amprenavir complexes with HIV-1 protease and its drug-resistant mutants altering hydrophobic clusters FEBS J. 277, 3699-3714
27. Rowley, R. L. and Pakkanen, T. (1999) Determination of a methane intermolecular potential model for use in molecular simulations from ab initio calculations J. Chem. Phys. 110, 3368-3377
28. Tie, Y., Boross, P. I., Wang, Y. F., Gaddis, L., Liu, F., Chen, X., Tozser, J., Harrison, R. W., and Weber, I. T. (2005) Molecular basis for substrate recognition and drug resistance from 1.1 to 1.6 angstroms resolution crystal structures of HIV-1 protease mutants with substrate analogs FEBS J. 272, 5265-5277
29. Weber, I. T., Agniswamy, J., Fu, G., Shen, C. H., and Harrison, R. W. (2012) Reaction intermediates discovered in crystal structures of enzymes Adv. Protein Chem. Struct. Biol. 87, 57-86
30. Kipp, D. R., Hirschi, J. S., Wakata, A., Goldstein, H., and Schramm, V. L. (2012) Transition states of native and drug-resistant HIV-1 protease are the same Proc. Natl. Acad. Sci. U.S.A. 109, 6543-6548
31. Heaslet, H., Rosenfeld, R., Giffin, M., Lin, Y. C., Tam, K., Torbett, B. E., Elder, J. H., McRee, D. E., and Stout, C. D. (2007) Conformational flexibility in the flap domains of ligand-free HIV protease Acta Crystallogr. D63, 866-875
32. Piana, S., Sebastiani, D., Carloni, P., and Parrinello, M. (2001) Ab initio molecular dynamics-based assignment of the protonation state of pepstatin A/HIV-1 protease cleavage site J. Am. Chem. Soc. 123, 8730-8737