In vitro selection and characterization of human immunodeficiency virus type 1 variants with increased resistance to ABT-378, a novel protease inhibitor

Journal of Virology

Volumn 72, Issue 9, 1998, Pages 7532-7541

  Carrillo, Alejandro ^a   Stewart, Kent D ^a   Sham, Hing L ^a   Norbeck, Daniel W ^a   Kohlbrenner, William E ^a   Leonard, John M ^a   Kempf, Dale J ^a   Molla, Akhteruzzaman ^a  

^a ABBOTT LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; LOPINAVIR; PROTEINASE INHIBITOR; RITONAVIR; SAQUINAVIR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; DRUG POTENCY; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEINASE INHIBITION; STRAIN DIFFERENCE; VIRUS MUTATION; VIRUS RESISTANCE;

EID: 0031849665     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.9.7532-7541.1998     Document Type: Article

References (40)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Barrie, K. A., E. E. Perez, S. L. Lamers, W. G. Farmerie, B. M. Dunn, J. W. Sleasman, and M. M. Goodenow. 1996. Natural variation in HIV-1 protease, Gag p7 and p6, and protease cleavage sites within gag/pol polyproteins: amino acid substitutions in the absence of protease inhibitors in mothers and children infected by human immunodeficiency virus type 1. Virology 219: 407-416.
3. Carrillo, A., and A. Molla. Unpublished data.
4. Chen, Z., Y. Li, H. B. Schock, D. Hall, E. Chen, and L. C. Kuo. 1995. Three-dimensional structure of a mutant HIV-1 protease displaying cross-resistance to all protease inhibitors in clinical trials. J. Biol. Chem. 270: 21433-21436.
5. Collins, J. R., S. K. Burl, and J. W. Erickson. 1995. Activated dynamics of flap opening in HIV-1 protease. Adv. Exp. Med. Biol. 362:455-460.
6. Condra, J. H., D. J. Holder, W. A. Schleif, O. M. Blahy, R. M. Danovich, L. J. Gabryelski, D. J. Graham, D. Laird, J. C. Quintero, A. Rhodes, H. L. Robbins, E. Roth, M. Shivaprakash, T. Yang, J. A. Chodakewitz, P. J. Deutsch, R. Y. Leavitt, F. E. Massari, J. W. Mellors, K. E. Squires, R. T. Steigbigel, H. Teppler, and E. A. Emini. 1996. Genetic correlates of in vivo viral resistance to indinavir, a human immunodeficiency virus type 1 protease inhibitor. J. Virol. 70:8270-8276.
7. Condra, J. H., W. A. Schleif, O. M. Blahy, L. J. Gabryelski, D. J. Graham, J. C. Quintero, A. Rhodes, H. L. Robbins, E. Roth, M. Shivaprakash, et al. 1995. In vivo emergence of HIV-1 variants resistant to multiple protease inhibitors. Nature 374:569-571.
8. Croteau, G., L. Doyon, D. Thibeault, G. McKercher, L. Pilote, and D. Lamarre. 1997. Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors. J. Virol. 71:1089-1096.
9. Darke, P. L., R. F. Nutt, S. F. Brady, V. M. Garsky, T. M. Ciccarone, C. T. Leu, P. K. Lumma, R. M. Freidinger, D. F. Veber, and I. S. Sigal. 1988. HIV-1 protease specificity of peptide cleavage is sufficient for processing of gag and pol polyproteins. Biochem. Biophys. Res. Commun. 156:297-303.
10. Debouck, C. 1992. The HIV-1 protease as a therapeutic target for AIDS. AIDS Res. Hum. Retroviruses 8:153-164.
11. Doyon, L., G. Croteau, D. Thibeault, F. Poulin, L. Pilote, and D. Lamarre. 1996. Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors, J. Virol. 70:3763-3769.
12. Erickson, J., D. J. Neidhart, J. VanDrie, D. J. Kempf, X. C. Wang, D. W. Norbeck, J. J. Plattner, J. W. Rittenhouse, M. Turon, N. Wideburg, et al. 1990. Design, activity, and 2.8 A crystal structure of a C2 symmetric inhibitor complexed to HIV-1 protease. Science 249:527-533.
13. 2-symmetric protease inhibitor. J. Virol. 68:2016-2020.
14. Jacobsen, H., M. Haenggi, M. Ott, I. B. Duncan, M. Andreoni, S. Vella, and J. Mous. 1996. Reduced sensitivity to saquinavir: an update on genotyping from phase I/I1 trials. Antiviral Res. 29:95-97.
15. Jacobsen, H., M. Hanggi, M. Ott, I. B. Duncan, S. Owen, M. Andreoni, S. Vella, and J. Mous. 1996. In vivo resistance to a human immunodeficiency virus type 1 proteinase inhibitor: mutations, kinetics, and frequencies. J. Infect. Dis. 173:1379-1387.
16. Jacobsen, H., K. Yasargil, D. L. Winslow, J. C. Craig, A. Krohn, I. B. Duncan, and J. Mous. 1995. Characterization of human immunodeficiency virus type 1 mutants with decreased sensitivity to proteinase inhibitor Ro 31-8959. Virology 206:527-534.
17. Kaplan, A. H., S. F. Michael, R. S. Wehbie, M. F. Knigge, D. A. Paul, L. Everitt, D. J. Kempf, D. W. Norbeck, J. W. Erickson, and R. Swanstrom. 1994. Selection of multiple human immunodeficiency virus type 1 variants that encode viral proteases with decreased sensitivity to an inhibitor of the viral protease. Proc. Natl. Acad. Sci. USA 91:5597-5601.
18. Kaplan, A. H., J. A. Zack, M. Knigge, D. A. Paul, D. J. Kempf, D. W. Norbeck, and R. Swanstrom. 1993. Partial inhibition of the human immunodeficiency virus type 1 protease results in aberrant virus assembly and the formation of noninfectious particles. J. Virol. 67:4050-4055.
19. Kempf, D. J., K. C. Marsh, J. F. Denissen, E. McDonald, S. Vasavanonda, C. A. Flentge, B. E. Green, L. Fino, C. H. Park, X. P. Kong, et al. 1995. ABT-538 is a potent inhibitor of human immunodeficiency virus protease and has high oral bioavailability in humans. Proc. Natl. Acad. Sci. USA 92:2484-2488.
20. King, R. W., S. Garber, D. L. Winslow, C. Reid, L. T. Bacheler, E. Anton, and M. J. Otto. 1995. Multiple mutations in the human immunodeficiency virus protease gene are responsible for decreased susceptibility to protease inhibitors. Antiviral Chem. Chemother. 6:80-88.
21. Kohl, N. E., E. A. Emini, W. A. Schleif, L. J. Davis, J. C. Heimbach, R. A. Dixon, E. M. Scolnick, and I. S. Sigal. 1988. Active human immunodeficiency virus protease is required for viral infectivity. Proc. Natl. Acad. Sci. USA 85:4686-4690.
22. Markowitz, M., H. Mo, D. J. Kempf, D. W. Norbeck, T. N. Bhat, J. W. Erickson, and D. D. Ho. 1995. Selection and analysis of human immunodeficiency virus type 1 variants with increased resistance to ABT-538, a novel protease inhibitor. J. Virol. 69:701-706.
23. Mo, H., M. Markowitz, P. Majer, S. K. Burt, S. V. Gulnik, L. I. Suvorov, J. W. Erickson, and D. D. Ho. 1996. Design, synthesis, and resistance patterns of MP-134 and MP-167, two novel inhibitors of HIV type 1 protease. AIDS Res. Hum. Retroviruses 12:55-61.
24. Molla, A., M. Korneyeva, Q. Gao, S. Vasavanonda, P. J. Schipper, H. M. Mo, M. Markowitz, T. Chernyavskiy, P. Niu, N. Lyons, A. Hsu, G. R. Granneman, D. D. Ho, C. A. Boucher, J. M. Leonard, D. W. Norbeck, and D. J. Kempf. 1996. Ordered accumulation of mutations in HIV protease confers resistance to ritonavir. Nat. Med. 2:760-766.
25. Partaledis, J. A., K. Yamaguchi, M. Tisdale, E. E. Blair, C. Falcione, B. Maschera, R. E. Myers, S. Pazhanisamy, O. Futer, A. B. Cullinan, C. M. Stuver, R. A. Byrn, and D. J. Livingston. 1995. In vitro selection and characterization of human immunodeficiency virus type 1 (HIV-1) isolates with reduced sensitivity to hydroxyethylamino sulfonamide inhibitors of HIV-1 aspartyl protease. J. Virol. 69:5228-5235.
26. Patick, A. K., R. Rose, J. Greytok, C. M. Bechtold, M. A. Hermsmeier, P. T. Chen, J. C. Barrish, R. Zahler, R. J. Colonno, and P.-F. Lin. 1995. Characterization of a human immunodeficiency virus type 1 variant with reduced sensitivity to an aminodiol protease inhibitor. J. Virol. 69:2148-2152.
27. Pauwels, R., J. Balzarini, M. Baba, R. Snoeck, D. Schols, P. Herdewijn, J. Desmyter, and E. De Clercq. 1988. Rapid and automated tetrazolium-based colorimetric assay for the detection of anti-HIV compounds. J. Virol. Methods 20:309-321.
28. Pazhanisamy. S., C. M. Stuver, A. B. Cullinan, N. Margolin, B. G. Rao, and D. J. Livingston. 1996. Kinetic characterization of human immunodeficiency virus type-1 protease-resistant variants. J. Biol. Chem. 271:17979-17985.
29. Peng, C., B. K. Ho, T. W. Chang, and N. T. Chang. 1989. Role of human immunodeficiency virus type 1-specific protease in core protein maturation and viral infectivity. J. Virol. 63:2550-2556.
30. Pettit, S. C., S. F. Michael, and R. Swanstrom. 1993. The specificity of the HIV-1 protease. Perspect. Drug Discov. Des. 1:69-83.
31. Pettit, S. C., J. Simsic, D. D. Loeb, L. Everitt, C. A. D. Hutchison, and R. Swanstrom. 1991. Analysis of retroviral protease cleavage sites reveals two types of cleavage sites and the structural requirements of the P1 amino acid. J. Biol. Chem. 266:14539-14547.
32. Roberts, N. A. 1995. Drug-resistance patterns of saquinavir and other HIV proteinase inhibitors. AIDS 9:S27-S32.
33. Sardana, V. V., A. J. Schlabach, P. Graham, B. L. Bush, J. H. Condra, J. C. Culberson, L. Gotlib, D. J. Graham, N. E. Kohl, R. L. LaFemina, C. L. Schneider, B. S. Wolanski, J. A. Wolfgang, and E. A. Emini. 1994. Human immunodeficiency virus type 1 protease inhibitors: evaluation of resistance engendered by amino acid substitutions in the enzyme's substrate binding site. Biochemistry 33:2004-2010.
34. Schock, H. B., V. M. Garsky, and L. C. Kuo. 1996. Mutational anatomy of an HIV-1 protease variant conferring cross-resistance to protease inhibitors in clinical trials. Compensatory modulations of binding and activity. J. Biol. Chem. 271:31957-31963.
35. Sham, H. L., D. J. Kempf, A. Molla, K. C. Marsh, G. N. Kumar, C.-M. Chen, W. Kati, K. Stewart, R. Lal, A. Hsu, D. Betebenner, M. Korneyeva, S, Vasavanonda, E. McDonald, A. Saldivar, N. Wideburg, X. Chen, P. Niu, C. Park, V. Jayanti, B. Grabowski, G. R. Granneman, E. Sun, A. J. Japour, J. M. Leonard, J. J. Plattner, and D. W. Norbeck. ABT-378, a potent second generation inhibitor of the human immunodeficiency virus protease. Submitted for publication.
36. Tisdale, M., R. E. Myers, B. Maschera, N. R. Parry, N. M. Oliver, and E. D. Blair. 1995. Cross-resistance analysis of human immunodeficiency virus type 1 variants individually selected for resistance to five different protease inhibitors. Antimicrob. Agents Chemother. 39:1704-1710.
37. Tozser, J., I. Blaha, T. D. Copeland, E. M. Wondrak, and S. Oroszlan. 1991. Comparison of the HIV-1 and HIV-2 proteinases using oligopeptide substrates representing cleavage sites in Gag and Gag-Pol polyproteins. FEBS Lett. 281:77-80.
38. Winslow, D. L., E. D. Anton, R. A. Horlick, R. J. Zagursky, R. J. Tritch, H. Scarnati, K. Ackerman, and L. T. Bacheler. 1994. Construction of infectious molecular clones of HIV-1 containing defined mutations in the protease gene. Biochem. Biophys. Res. Commun. 205:1651-1657.
39. Wondrak, E. M., J. M. Louis, H. de Rocquigny, J. C. Chermann, and B. P. Roques. 1993. The gag precursor contains a specific HIV-1 protease cleavage site between the NC (P7) and P1 proteins. FEBS Lett. 333:21-24.
40. Zhang, Y.-M., H. Imamichi, T. Imamichi, H. C. Lane, J. Falloon, M. B. Vasudevachari, and N. P. Salzman. 1997. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J. Virol. 71:6662-6670.