HIV-1 protease mutations and protease inhibitor cross-resistance

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 10, 2010, Pages 4253-4261

  Rhee, Soo Yon ^a   Taylor, Jonathan ^b   Fessel, W Jeffrey ^c   Kaufman, David ^d   Towner, William ^e   Troia, Paolo ^f   Ruane, Peter ^g   Hellinger, James ^h   Shirvani, Vivian ⁱ   Zolopa, Andrew ^a   Shafer, Robert W ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c KAISER PERMANENTE   (United States)

^d ST VINCENT S HOSPITAL   (United States)

^e University of California Davis Medical Center ^*  (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Light Source Medical   (United States)

^h TUFTS MEDICAL CENTER   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATAZANAVIR; DARUNAVIR; FOSAMPRENAVIR; INDINAVIR; LOPINAVIR; NELFINAVIR; SAQUINAVIR; TIPRANAVIR;

ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CLINICAL EVALUATION; CONTROLLED STUDY; CROSS RESISTANCE; GENE MUTATION; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; PRIORITY JOURNAL; VIRAL GENETICS; VIRUS MUTATION;

CARBAMATES; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; INDINAVIR; LEAST-SQUARES ANALYSIS; MUTATION; NELFINAVIR; OLIGOPEPTIDES; PHOSPHORIC ACID ESTERS; POLYMORPHISM, GENETIC; PYRIDINES; PYRIMIDINONES; PYRONES; SAQUINAVIR; SULFONAMIDES;

EID: 77957351212     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00574-10     Document Type: Article

References (51)

1. Ait-Khaled, M., A. Rakik, P. Griffin, C. Stone, N. Richards, D. Thomas, J. Falloon, and M. Tisdale. 2003. HIV-1 reverse transcriptase and protease resistance mutations selected during 16-72 weeks of therapy in isolates from antiretroviral therapy-experienced patients receiving abacavir/efavirenz/ amprenavir in the CNA2007 study. Antivir. Ther. 8:111-120.
2. Atkinson, B., J. Isaacson, M. Knowles, E. Mazabel, and A. K. Patick. 2000. Correlation between human immunodeficiency virus genotypic resistance and virologic response in patients receiving nelfinavir monotherapy or nelfi- navir with lamivudine and zidovudine. J. Infect. Dis. 182:420-427.
3. Baxter, J. D., J. M. Schapiro, C. A. Boucher, V. M. Kohlbrenner, D. B. Hall, J. R. Scherer, and D. L. Mayers. 2006. Genotypic changes in human immunodeficiency virus type 1 protease associated with reduced susceptibility and virologic response to the protease inhibitor tipranavir. J. Virol. 80:10794-10801.
4. Bennett, D. E., R. J. Camacho, D. Otelea, D. R. Kuritzkes, H. Fleury, M. Kiuchi, W. Heneine, R. Kantor, M. R. Jordan, J. M. Schapiro, A. M. Vandamme, P. Sandstrom, C. A. Boucher, D. van de Vijver, S. Y. Rhee, T. F. Liu, D. Pillay, and R. W. Shafer. 2009. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS One 4:e4724.
5. Bristol-Myers Squibb Company. 2009. Reyetaz prescribing information. Bristol-Myers Squibb Company, New York, NY. http://www.bms.com.
6. 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.
7. 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.
8. Cote, H. C., Z. L. Brumme, and P. R. Harrigan. 2001. Human immunodeficiency virus type 1 protease cleavage site mutations associated with protease inhibitor cross-resistance selected by indinavir, ritonavir, and/or saquinavir. J. Virol. 75:589-594.
9. Craig, C., E. Race, J. Sheldon, L. Whittaker, S. Gilbert, A. Moffatt, J. Rose, S. Dissanayeke, G. W. Chirn, I. B. Duncan, and N. Cammack. 1998. HIV protease genotype and viral sensitivity to HIV protease inhibitors following saquinavir therapy. AIDS 12:1611-1618. (Pubitemid 28418330)
10. De Meyer, S., H. Azijn, D. Surleraux, D. Jochmans, A. Tahri, R. Pauwels, P. Wigerinck, and M. P. de Bethune. 2005. TMC114, a novel human immunodeficiency virus type 1 protease inhibitor active against protease inhibitorresistant viruses, including a broad range of clinical isolates. Antimicrob. Agents Chemother. 49:2314-2321.
11. De Meyer, S., I. Dierynck, E. Lathouwers, B. Baalen, T. Vangeneugden, S. Spinosa-Guzman, G. Picchio, and M. P. de Bethune. 2008. Identification of mutations predictive of a diminished response to darunavir/ritonavir: analysis of data from treatment-experienced patients in POWER 1, 2, 3, and DUET-1 and DUET-2, abstr. 54. Sixth European HIV Drug Resistance Workshop, Budapest, Hungary.
12. De Meyer, S., I. Dierynck, E. Lathouwers, B. Van Baelen, T. Vangeneugden, S. Spinosa-Guzman, M. Peeters, G. Picchio, and M. de Bethune. 2008. Phenotypic and genotypic determinants of resistance to darunavir: analysis of data from treatment experienced patients in POWER 1, 2, 3 and DUET-1 and 2 [abstract 33]. Antivir. Ther. 13(Suppl. 3):A33.
13. De Meyer, S., A. Hill, G. Picchio, R. DeMasi, E. De Paepe, and M. P. de Bethune. 2008. Influence of baseline protease inhibitor resistance on the efficacy of darunavir/ritonavir or lopinavir/ritonavir in the TITAN trial. J. Acquir. Immune Defic. Syndr. 49:563-564.
14. De Meyer, S., E. Lathouwers, I. Dierynck, E. De Paepe, B. Van Baelen, T. Vangeneugden, S. Spinosa-Guzman, E. Lefebvre, G. Picchio, and M. P. de Bethune. 2009. Characterization of virologic failure patients on darunavir/ritonavir in treatment-experienced patients. AIDS 23:1829-1840.
15. Doyon, L., S. Tremblay, L. Bourgon, E. Wardrop, and M. G. Cordingley. 2005. Selection and characterization of HIV-1 showing reduced susceptibility to the non-peptidic protease inhibitor tipranavir. Antiviral Res. 68:27-35.
16. Efron, B., T. Hastie, I. Johnstone, and R. Tibshirani. 2004. Least angle regression. Ann. Stat. 32:407-499.
17. Ghosn, J., P. Flandre, I. Cohen-Codar, P. M. Girard, M. L. Chaix, F. Raffi, P. Dellamonica, P. Ngovan, M. Norton, and J. F. Delfraissy. 2010. Long-term (96-week) follow-up of antiretroviral-naive HIV-infected patients treated with first-line lopinavir/ritonavir monotherapy in the MONARK trial. HIV Med. 11:137-142.
18. 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 immunodeficiency virus type 1 protease inhibitor BMS-232632. Antimicrob. Agents Chemother. 44:2319-2326.
19. Hertogs, K., M. P. de Bethune, V. Miller, T. Ivens, P. Schel, A. Van Cauwenberge, C. Van Den Eynde, V. Van Gerwen, H. Azijn, M. Van Houtte, F. Peeters, S. Staszewski, M. Conant, S. Bloor, S. Kemp, B. Larder, and R. Pauwels. 1998. A rapid method for simultaneous detection of phenotypic resistance to inhibitors of protease and reverse transcriptase in recombinant human immunodeficiency virus type 1 isolates from patients treated with antiretroviral drugs. Antimicrob. Agents Chemother. 42:269-276.
20. Johnson, V. A., F. Brun-Vezinet, B. Clotet, H. F. Gunthard, D. R. Kuritzkes, D. Pillay, J. M. Schapiro, and D. D. Richman. 2009. Update of the drug resistance mutations in HIV-1: December 2009. Top. HIV Med. 17:138-145.
21. Kagan, R. M., M. D. Shenderovich, P. N. 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.
22. Kempf, D. J., J. D. Isaacson, M. S. King, S. C. Brun, J. Sylte, B. Richards, B. Bernstein, R. Rode, and E. Sun. 2002. Analysis of the virological response with respect to baseline viral phenotype and genotype in protease inhibitor-experienced HIV-1-infected patients receiving lopinavir/ritonavir therapy. Antivir. Ther. 7:165-174.
23. Kempf, D. J., J. D. Isaacson, M. S. King, S. C. Brun, Y. Xu, K. Real, B. M. Bernstein, A. J. Japour, E. Sun, and R. A. Rode. 2001. Identification of genotypic changes in human immunodeficiency virus protease that correlate with reduced susceptibility to the protease inhibitor lopinavir among viral isolates from protease inhibitor-experienced patients. J. Virol. 75:7462-7469.
24. Kolli, M., S. Lastere, and C. A. Schiffer. 2006. Co-evolution of nelfinavirresistant HIV-1 protease and the p1-p6 substrate. Virology 347:405-409.
25. Llibre, J. M., J. M. Schapiro, and B. Clotet. 2010. Clinical implications of genotypic resistance to the newer antiretroviral drugs in HIV-1-infected patients with virological failure. Clin. Infect. Dis. 50:872-881.
26. Madruga, J. V., P. Cahn, B. Grinsztejn, R. Haubrich, J. Lalezari, A. Mills, G. Pialoux, T. Wilkin, M. Peeters, J. Vingerhoets, G. de Smedt, L. Leopold, R. Trefiglio, and B. Woodfall. 2007. Efficacy and safety of TMC125 (etravirine) in treatment-experienced HIV-1-infected patients in DUET-1: 24-week results from a randomised, double-blind, placebo-controlled trial. Lancet 370:29-38. (Pubitemid 47017466)
27. Maguire, M., D. Shortino, A. Klein, W. Harris, V. Manohitharajah, M. Tisdale, R. Elston, J. Yeo, S. Randall, F. Xu, H. Parker, J. May, and W. Snowden. 2002. Emergence of resistance to protease inhibitor amprenavir in human immunodeficiency virus type 1-infected patients: selection of four alternative viral protease genotypes and influence of viral susceptibility to coadministered reverse transcriptase nucleoside inhibitors. Antimicrob. Agents Chemother. 46:731-738.
28. Malan, D. R., E. Krantz, N. David, V. Wirtz, J. Hammond, and D. McGrath. 2008. Efficacy and safety of atazanavir, with or without ritonavir, as part of once-daily highly active antiretroviral therapy regimens in antiretroviral-naive patients. J. Acquir. Immune Defic. Syndr. 47:161-167.
29. Marcelin, A. G., D. Affolabi, C. Lamotte, H. A. Mohand, C. Delaugerre, M. Wirden, D. Voujon, P. Bossi, N. Ktorza, F. Bricaire, D. Costagliola, C. Katlama, G. Peytavin, and V. Calvez. 2004. Resistance profiles observed in virological failures after 24 weeks of amprenavir/ritonavir containing regimen in protease inhibitor experienced patients. J. Med. Virol. 74:16-20.
30. Margot, N. A., E. Isaacson, I. McGowan, A. K. Cheng, R. T. Schooley, and M. D. Miller. 2002. Genotypic and phenotypic analyses of HIV-1 in antiretroviral- experienced patients treated with tenofovir DF. AIDS 16:1227-1235.
31. Mo, H., N. Parkin, K. D. Stewart, L. Lu, T. Dekhtyar, D. J. Kempf, and A. Molla. 2007. Identification and structural characterization of I84C and I84A mutations that are associated with high-level resistance to human immunodeficiency virus protease inhibitors and impair viral replication. Antimicrob. Agents Chemother. 51:732-735.
32. Myers, R. E., C. V. Gale, A. Harrison, Y. Takeuchi, and P. Kellam. 2005. A statistical model for HIV-1 sequence classification using the subtype analyser (STAR). Bioinformatics 21:3535-3540.
33. Nijhuis, M., N. van Maarseveen, D. de Jong, P. Schipper, I. Goedegebuure, and C. Boucher. 2006. Substitutions within Gag but outside the cleavage sites can cause protease inhibitor resistance. Antivir. Ther. 11:S149.
34. Nijhuis, M., A. M. Wensing, W. F. Bierman, D. de Jong, R. Kagan, A. Fun, C. A. Jaspers, K. A. Schurink, M. A. van Agtmael, and C. A. Boucher. 2009. Failure of treatment with first-line lopinavir boosted with ritonavir can be explained by novel resistance pathways with protease mutation 76V. J. Infect. Dis. 200:698-709.
35. Parkin, N. T., C. Chappey, and C. J. Petropoulos. 2003. Improving lopinavir genotype algorithm through phenotype correlations: novel mutation patterns and amprenavir cross-resistance. AIDS 17:955-961.
36. Partaledis, J. A., K. Yamaguchi, M. Tisdale, E. E. Blair, C. Falcione, B. Maschera, R. E. Myers, S. Pazhanisamy, O. Futer, A. B. Cullinan, et al. 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.
37. Patick, A. K., H. Mo, M. Markowitz, K. Appelt, B. Wu, L. Musick, V. Kalish, S. Kaldor, S. Reich, D. Ho, and S. Webber. 1996. Antiviral and resistance studies of AG1343, an orally bioavailable inhibitor of human immunodeficiency virus protease. Antimicrob. Agents Chemother. 40:292-297.
38. Petropoulos, C. J., N. T. Parkin, K. L. Limoli, Y. S. Lie, T. Wrin, W. Huang, H. Tian, D. Smith, G. A. Winslow, D. J. Capon, and J. M. Whitcomb. 2000. A novel phenotypic drug susceptibility assay for human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 44:920-928.
39. Rhee, S. Y., W. J. Fessel, A. R. Zolopa, L. Hurley, T. Liu, J. Taylor, D. P. Nguyen, S. Slome, D. Klein, M. Horberg, J. Flamm, S. Follansbee, J. M. Schapiro, and R. W. Shafer. 2005. HIV-1 protease and reverse-transcriptase mutations: correlations with antiretroviral therapy in subtype B isolates and implications for drug-resistance surveillance. J. Infect. Dis. 192:456-465.
40. Rhee, S. Y., M. J. Gonzales, R. Kantor, B. J. Betts, J. Ravela, and R. W. Shafer. 2003. Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res. 31:298-303.
41. Rhee, S. Y., J. Taylor, G. Wadhera, A. Ben-Hur, D. L. Brutlag, and R. W. Shafer. 2006. Genotypic predictors of human immunodeficiency virus type 1 drug resistance. Proc. Natl. Acad. Sci. U. S. A. 103:17355-17360.
42. Shahriar, R., S. Y. Rhee, T. F. Liu, W. J. Fessel, A. Scarsella, W. Towner, S. P. Holmes, A. R. Zolopa, and R. W. Shafer. 2009. Nonpolymorphic human immunodeficiency virus type 1 protease and reverse transcriptase treatmentselected mutations. Antimicrob. Agents Chemother. 53:4869-4878.
43. 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.
44. Van Marck, H., I. Dierynck, G. Kraus, S. Hallenberger, T. Pattery, G. Muyldermans, L. Geeraert, L. Borozdina, R. Bonesteel, C. Aston, E. Shaw, Q. Chen, C. Martinez, V. Koka, J. Lee, E. Chi, M. P. de Bethune, and K. Hertogs. 2009. The impact of individual human immunodeficiency virus type 1 protease mutations on drug susceptibility is highly influenced by complex interactions with the background protease sequence. J. Virol. 83:9512-9520.
45. Vergani, B., M. L. Cicero, O. Vigano, F. Sirianni, S. Ferramosca, P. Vitiello, P. Di Vincenzo, M. Pia De Pasquale, M. Galli, and S. Rusconi. 2008. Evolution of the HIV-1 protease region in heavily pretreated HIV-1 infected patients receiving Atazanavir. J. Clin. Virol. 41:154-159.
46. Vermeiren, H., E. Van Craenenbroeck, P. Alen, L. Bacheler, G. Picchio, and P. Lecocq. 2007. Prediction of HIV-1 drug susceptibility phenotype from the viral genotype using linear regression modeling. J. Virol. Methods 145:47-55. (Pubitemid 47247892)
47. Watkins, T., W. Resch, D. Irlbeck, and R. Swanstrom. 2003. Selection of high-level resistance to human immunodeficiency virus type 1 protease inhibitors. Antimicrob. Agents Chemother. 47:759-769.
48. 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 protease inhibitors in a variety of human immunodeficiency virus type 1 genetic backbones. Antimicrob. Agents Chemother. 49:3816-3824.
49. Winters, M. A., J. M. Schapiro, J. Lawrence, and T. C. Merigan. 1998. Human immunodeficiency virus type 1 protease genotypes and in vitro protease inhibitor susceptibilities of isolates from individuals who were switched to other protease inhibitors after long-term saquinavir treatment. J. Virol. 72:5303-5306.
50. Ziermann, R., K. Limoli, K. Das, E. Arnold, C. J. Petropoulos, and N. T. Parkin. 2000. A mutation in human immunodeficiency virus type 1 protease, N88S, that causes in vitro hypersensitivity to amprenavir. J. Virol. 74:4414-4419.
51. Zolopa, A., W. Towner, D. Butcher, S. Wang, J. Maa, and D. Seekins. 2007. Resistance profile after viral rebound on atazanavir-containing therapy: focus on protease inhibitor-naive subjects in the IMPACT study (BMS AI424-128) [abstract 77]. Antivir. Ther. 12:S86.