X-ray crystal structures of human immunodeficiency virus type 1 protease mutants complexed with atazanavir

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9525-9535

  Klei, Herbert E ^a   Kish, Kevin ^a   Lin, Pin Fang M ^a   Guo, Qi ^a   Friborg, Jacques ^a   Rose, Ronald E ^a   Zhang, Yaqun ^a   Goldfarb, Valentina ^a   Langley, David R ^a   Wittekind, Michael ^a,b   Sheriff, Steven ^a  

^a BRISTOL MYERS SQUIBB   (United States)

^b AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPRENAVIR; ATAZANAVIR; ENZYME VARIANT; INDINAVIR; LOPINAVIR; MUTANT PROTEIN; NELFINAVIR; PROTEINASE; RITONAVIR; SAQUINAVIR;

ARTICLE; AUTOLYSIS; COMPLEX FORMATION; CRYSTAL STRUCTURE; DRUG STRUCTURE; ENZYME CONFORMATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN ISOLATION; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DRUG RESISTANCE, VIRAL; HIV PROTEASE; HIV PROTEASE INHIBITORS; MODELS, MOLECULAR; MUTATION; OLIGOPEPTIDES; PROTEIN STRUCTURE, TERTIARY; PYRIDINES;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34548168260     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02503-05     Document Type: Article

References (67)

1. Ala, P. J., E. E. Huston, R. M. Klabe, D. D. McCabe, J. L. Duke, C. J. Rizzo, B. D. Korant, R. J. DeLoskey, P. Y. S. Lam, C. N. Hodge, and C.-H. Chang. 1997. Molecular basis of HIV-1 protease drug resistance: structural analysis of mutant proteases complexed with cyclic urea inhibitors. Biochemistry 36:1573-1580.
2. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. Protein data bank. Nucleic Acids Res. 28:235-242.
3. Brünger, A. T., P. D. Adams, G. M. Clore, W. L. DeLano, P. Gros, R. W. Grosse-Kunstleve, J.-S. Jiang, J. Kuszewski, M. Nilges, N. S. Pannu, R. J. Read, L. M. Rice, T. Simonson, and G. L. Warren. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54:905-921.
4. Carson, M. 1997. RIBBONS. Methods Enzymol. 277:493-505.
5. Clemente, J. C., R. M. Coman, M. M. Thiaville, L. K. Janka, J. A. Jeung, S. Nukoolkarn, L. Govindasamy, M. Agbandje-McKenna, R. McKenna, W. Leelamanit, M. M. Goodenow, and B. M. Dunn. 2006. Analysis of HIV-1 CRF_01 A/E protease inhibitor resistance: structural determinants for maintaining sensitivity and developing resistance to atazanavir. Biochemistry 45:5468-5477.
6. Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50:760-763.
7. Colonno, R. J., A. Thiry, K. Limoli, and N. Parkin. 2003. Activities of atazanavir (BMS-232632) against a large panel of human immunodeficiency virus type 1 clinical isolates resistant to one or more approved protease inhibitors. Antimicrob. Agents Chemother. 47:1324-1333.
8. Colonno, R., R. Rose, C. McLaren, A. Thiry, N. Parkin, and J. Friborg. 2004. Identification of I50L as the signature atazanavir (ATV)-resistance mutation in treatment-naive HIV-1-infected patients receiving ATV-containing regimens. J. Infect. Dis. 189:1802-1810.
9. Dawson, R. M. C., D. C. Elliott, W. H. Elliot, and K. M. Jones. 1986. Data for biochemical research, 3rd ed. Clarendon Press, Oxford, United Kingdom.
10. De Clercq, E. 2002. New developments in anti-HIV chemotherapy. Biochim. Biophys. Acta 1587:258-275.
11. Devereux, J., P. Haeberli, and O. Smithies. 1984. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12:387-395.
12. 2 symmetric inhibitor complexed to HIV-1 protease. Science 249:527-533.
13. Erickson, J. W. 1993. Design and structure of symmetry-based inhibitors of HIV-1 protease, p. 109-128. In P. S. Anderson, G. L. Kenyon, and G. R. Marshall (ed.), Perspectives in drug discovery and design. ESCOM Science, Leiden, The Netherlands.
14. Ermolieff, J., X. Lin, and J. Tang. 1997. Kinetic properties of saquinavir-resistant mutants of human immunodeficiency virus type 1 protease and their implications in drug resistance in vivo. Biochemistry 36:12364-12370.
15. Flexner, C. 1998. HIV-protease inhibitors. N. Engl. J. Med. 338:1281-1292.
16. French, S., and K. Wilson. 1978. On the treatment of negative intensity observations. Acta. Crystallogr. A 34:517-525.
17. Gong, Y.-F., B. S. Robinson, R. E. Rose, C. Deminie, T. P. Spicer, D. Stock, R. J. Colonno, and P.-F. Lin. 2000. In vitro resistance profile of the human immnunodeficiency virus type 1 protease inhibitor BMS-232632. Antimicrob. Agents Chemother. 44:2319-2326.
18. Gulick, R. M. 1997. Current antiretroviral therapy: an overview. Quality Life Res. 6:471-474.
19. Hertogs, K., S. Bloor, S. D. Kemp, C. V. den Eynde, T. M. Alcorn, R. Pauwels, M. V. Houtte, S. Staszewski, V. Miller, and B. A. Larder. 2000. Phenotypic and genotypic analysis of clinical HIV-1 isolates reveals extensive protease inhibitor cross-resistance: a survey of over 6000 samples. AIDS 14:1203-1210.
20. Hong, L., X. C. Zhang, J. A. Hartsuck, and J. Tang. 2000. Crystal structure of an in vivo HIV-1 protease mutant in complex with saquinavir: insights into the mechanisms of drug resistance. Protein Sci. 9:1898-1904.
21. Ido, E., H.-P. Han, F. J. Kezdy, and J. Tang. 1991. Kinetic studies of human immunodeficiency virus type 1 protease and its active-site hydrogen bond mutant A28S. J. Biol. Chem. 266:24359-24366.
22. Kagan, R. M., M. D. Shenderovich, P. N. R. Heseltine, and K. Ramnarayan. 2005. Structural analysis of an HIV-1 protease I47A mutant resistant to the protease inhibitor lopinavir. Protein Sci. 14:1870-1878.
23. Klabe, R. M., L. T. Bacheler, P. J. Ala, S. Erickson-Viitanen, and J. L. Meek. 1998. Resistance to HIV protease inhibitors: a comparison of enzyme inhibition and antiviral potency. Biochemistry 37:8735-8742.
24. Kunkel, T. A. 1985. Rapid and efficient site-specific mutagenesis without phenotype selection. Proc. Natl. Acad. Sci. USA 82:488-492.
25. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
26. Lin, Y., X. Lin, L. Hong, S. Foundling, R. L. Heinrikson, S. Thaisrivongs, W. Leelamanit, D. Raterman, M. Shah, B. M. Dunn, and J. Tang. 1995. Effect of point mutations on the kinetics and the inhibition of human immunodeficiency virus type 1 protease: relationship to drug resistance. Biochemistry 34:1143-1152.
27. Lovell, S. C., I. W. Davis, W. B. Arendall III, P. I. W. de Bakker, J. M. Word, M. G. Prisant, J. S. Richardson, and D. C. Richardson. 2003. Structure validation by Cα geometry: φ, ψ; and Cβ deviation. Proteins 50:437-450.
28. Mahalingam, B., Y.-F. Wang, P. I. Boross, J. Tozser, J. M. Louis, R. W. Harrison, and I. T. Weber. 2004. Crystal structures of HIV protease V82A and L90M mutants reveal changes in the indinavir-binding site. Eur. J. Biochem. 271:1516-1524.
29. McIlvaine, T. C. 1921. A buffer solution for colorimetric comparison. J. Biol. Chem. 49:183-186.
30. Mildner, A. M., D. J. Rothrock, J. W. Leone, C. A. Bannow, J. M. Lull, I. M. Reardon, J. L. Sarcich, W. J. Howe, C. C. Tomich, C. W. Smith, R. L. Heinrikson, and A. G. Tomasselli. 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.
31. Molla, A., G. R. Granneman, E. Sun, and D. J. Kempf. 1998. Recent developments in HIV protease inhibitor therapy. Antivir. Res. 39:1-23.
32. Navaza, J. 1994. AMoRe: an automated package for molecular replacement. Acta Crystallogr. A 50:157-163.
33. Nicholson, L. K., T. Yamazaki, D. A. Torchia, S. Grzesiek, A. Bax, S. J. Stahl, J. D. Kaufman, P. T. Wingfield, P. Y. S. Lam, P. K. Jadhav, C. N. Hodge, P. J. Domaille, and C.-H. Chang. 1995. Flexibility and function in HIV-1 protease. Struct. Biol. 2:274-280.
34. Ohtaka, H., A. Schon, and E. Freire. 2003. Multidrug resistance to HIV-1 protease inhibition requires cooperative coupling between distal mutations. Biochemistry 42:13659-13666.
35. Otwinowski, Z., and W. Minor. 1997. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:307-326.
36. Palella, F. J., K. M. Delaney, A. C. Moorman, M. O. Loveless, J. Fuhrer, G. A. Satten, D. J. Aschman, and S. D. Holmberg. 1998. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N. Engl. J. Med. 338:853-860.
37. Piliero, P., P. Cahn, G. Pantaleo, J. M. Gatell, K. Squires, L. Percival, I. Sanne, R. Wood, P. Phanuphak, S. Shelton, A. Lazzarin, A. Thiry, T. Kelleher, M. Giordano, and S. M. Schnittman. 2002. Atazanavir: a once-daily protease inhibitor with a superior lipid profile: results of clinical trials beyond week 48, abstr. 706-T. Abstr. 9th Conf. Retrovir. Opportun. Infect.
38. Pivazyan, A. D., D. S. Matteson, L. Fabry-Asztalos, R. P. Singh, P.-F. Lin, W. Blair, K. Guo, B. Robinson, and W. H. Prusoff. 2000. Inhibition of HIV-1 protease by a boron-modified polypeptide. Biochem. Pharmacol. 60:927-936.
39. Prabu-Jeyabalan, M., E. Nalivaika, and C. A. Schiffer. 2000. How does a symmetric dimer recognize an asymmetric substrate? A substrate complex of HIV-1 protease. J. Mol. Biol. 301:1207-1220.
40. Prabu-Jeyabalan, M., E. A. Nalivaika, N. M. King, and C. A. Schiffer. 2003. Viability of a drug-resistant human immunodeficiency virus type 1 protease variant: structural insights for better antiviral therapy. J. Virol. 77:1306-1315.
41. Rhee, S.-Y., M. J. Gonzales, R. Kantor, B. J. Betts, J. Ravela, and R. W. Shafer. 2003. HIV reverse transcriptase and sequence database. Nucleic Acids Res. 31:298-303.
42. Ridky, T., and J. Leis. 1995. Development of drug resistance to HIV-1 protease inhibitors. J. Biol. Chem. 270:29621-29623.
43. Robinson, B. S., K. A. Riccardi, Y.-F. Gong, Q. Guo, D. A. Stock, W. S. Blair, B. J. Terry, C. A. Deminie, F. Djang, R. J. Colonno, and P.-F. Lin. 2000. BMS-233632, a highly potent human immunodeficiency virus protease inhibitor that can be used in combination with other available antiretroviral agents. Antimicrob. Agents Chemother. 44:2093-2099.
44. Rosé, J. R., R. Salto, and C. S. Craik. 1993. Regulation of autoproteolysis of the HIV-1 and HIV-2 protease with engineered amino acid substitutions. J. Biol. Chem. 268:11939-11945.
45. Sack, J. S., and F. A. Quiocho. 1997. CHAIN-a crystallographic modeling program. Methods Enzymol. 277:158-173.
46. Reference deleted.
47. Sanne, I., P. Piliero, K. Squires, A. Thiry, and S. Schnittman. 2003. Results of a phase 2 clinical trial at 48 weeks (A1424-007): a dose-ranging, safety, and efficacy comparative trial of atazanavir at three doses in combination with didanosine and stavudine in antiretroviral-naive subjects. J. Acquir. Immune. Defic. Syndr. 32:18-29.
48. Satow, Y., G. H. Cohen, E. A. Padlan, and D. R. Davies. 1986. Phosphocholine binding immunoglobulin Fab McPC603: an X-ray diffraction study at 2.7 Å. J. Mol. Biol. 190:593-604.
49. Schechter, I., and A. Berger. 1967. On the size of the active site in protease. Biochem. Biophys. Res. Commun. 27:157-162.
50. Schinazi, R. F., B. A. Larder, and J. W. Mellors. 1996. Mutations in retroviral genes associated with drug resistance. Int. Antiviral Newsl. 4:95-107.
51. Schnell, T., B. Schmidt, G. Moschik, C. Thein, C. Paatz, K. Korn, and H. Walter. 2003. Distinct cross-resistance profiles of the new protease inhibitors amprenavir, lopinavir, and atazanavir in a panel of clinical samples. AIDS 17:1324-1333.
52. Shenderovish, M. D., R. M. Kagan, P. N. R. Heseltine, and K. Ramnarayan. 2003. Structure-based phenotyping predicts HIV-1 protease inhibitor resistance. Protein Sci. 12:1706-1718.
53. Sheriff, S., and W. A. Hendrickson. 1987. Description of overall anisotropy in diffraction from macromolecular crystals. Acta Crystallogr. A 43:118-121.
54. Starcich, B. R., B. H. Hahn, G. M. Shaw, P. D. McNeely, S. Modrow, H. Wolf, E. S. Parks, W. P. Parks, S. F. Josephs, R. C. Gallo, and F. Wong-Staal. 1986. Identification and characterization of conserved and variable regions in the envelope gene of HTLV-III/LAV, the retrovirus of AIDS. Cell 45:637-648.
55. Todd, M. J., I. Luque, A. Velázquez-Campoy, and E. Freire. 2000. The thermodynamic basis of resistance to HIV-1 protease inhibition: calorimetric analysis of the V82F/I84V active site resistant mutant. Biochemistry 39:11876-11883.
56. Vacca, J. P., and J. H. Contra. 1997. Clinically effective HIV-1 protease inhibitors. Drug Discov. Today 2:261-272.
57. Vondrasek, J., C. P. van Buskirk, and A. Wlodawer. 1997. Database of three-dimensional structures of HIV proteinases. Nat. Struct. Biol. 4:8.
58. Vondrasek, J., and A. Wlodawer. 2002. HIVdb: a database of the structure of human immunodeficiency virus protease. Proteins 49:429-431.
59. Wallace, A. C., R. A. Laskowski, and J. M. Thornton. 1995. LIGPLOT. a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:127-134.
60. Wang, Y.-X., D. I. Freedberg, T. Yamazaki, P. T. Wingfield, S. J. Stahl, J. D. Kaufman, Y. Kiso, and D. A. Torchia. 1996. Solution NMR evidence that the HIV-1 protease catalytic aspartyl groups have different ionization states in the complex formed with the asymmetric drug KNI-272. Biochemistry 35:9945-9950.
61. Wang, Y.-X., D. I. Freedberg, S. Grzesiek, D. A. Torchia, P. T. Wingfield, J. D. Kaufman, S. J. Stahl, C.-H. Chang, and C. N. Hodge. 1996. Mapping hydration water molecules in the HIV-1 protease/DMP323 complex in solution by NMR spectroscopy. Biochemistry 35:12694-12704.
62. Weinheimer, S., L. Discotto, J. Friborg, H. Yang, and R. Colonno. 2005. Atazanavir signature I50L resistance substitution accounts for unique phenotype of increased susceptibility to other PIs in a variety of HIV-1 genetic backbones. Antimicrob. Agents Chemother. 49:3816-3824.
63. Wlodawer, A., and J. Vondrasek. 1998. Inhibitors of HIV-1 protease: a major success of structure-assisted drug design. Annu. Rev. Biophys. Biomol. Struct. 27:249-284.
64. Wlodawer, A. 2002. Rational approach to AIDS drug design through structural biology. Annu. Rev. Med. 53:595-614.
65. Yamazaki, T., L. K. Nicholson, D. A. Torchia, S. J. Stahl, J. D. Kaufman, P. T. Wingfield, P. J. Domaille, and S. Campbell-Burk. 1994. Secondary structure and signal assignments of human-immunodeficiency-virus-1 protease complexed to a novel, structure-based inhibitor. Eur. J. Biochem. 219:707-712.
66. Yamazaki, T., A. P. Hinck, Y.-X. Wang, L. K. Nicholson, D. A. Torchia, P. Wingfield, S. J. Stahl, J. D. Kaufman, C.-H. Chang, P. J. Domaille, and P. Y. S. Lam. 1996. Three-dimensional solution structure of the HIV-1 protease complexed with DMP323, a novel cyclic urea-type inhibitor, determined by nuclear magnetic resonance spectroscopy. Protein Sci. 5:495-506.
67. Yanchunas, J., D. R. Langley, L. Tao, R. E. Rose, J. Friborg, R. J. Colonno, and M. L. Doyle. 2005. Molecular basis for increased susceptibility of atazanavir-resistant substitution I50L to other protease inhibitors. Antimicrob. Agents Chemother. 49:3825-3832.