Novel method for simultaneous quantification of phenotypic resistance to maturation, protease, reverse transcriptase, and integrase HIV inhibitors based on 3′Gag(p2/p7/p1/p6)/PR/RT/INT-recombinant viruses: A useful tool in the multitarget era of antiretroviral therapy

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 8, 2011, Pages 3729-3742

  Weber, Jan ^a   Vazquez, Ana C ^a   Winner, Dane ^a   Rose, Justine D ^a   Wylie, Doug ^a   Rhea, Ariel M ^a   Henry, Kenneth ^b   Pappas, Jennifer ^a   Wright, Alison ^a   Mohamed, Nizar ^a   Gibson, Richard ^b   Rodriguez, Benigno ^c   Soriano, Vicente ^d   King, Kevin ^a   Arts, Eric J ^b   Olivo, Paul D ^a   Quiñones Mateu, Miguel E ^a  

^a Quidel Corporation   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HOSPITAL UNIVERSITARIO LA PAZ   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ABACAVIR; AMPRENAVIR; ATAZANAVIR; DARUNAVIR; DELAVIRDINE; DIDANOSINE; EFAVIRENZ; EMTRICITABINE; ETRAVIRINE; GAG PROTEIN; INDINAVIR; INTEGRASE INHIBITOR; LAMIVUDINE; LOPINAVIR; NELFINAVIR; NEVIRAPINE; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; POL PROTEIN; PROTEINASE INHIBITOR; RITONAVIR; RNA DIRECTED DNA POLYMERASE INHIBITOR; SAQUINAVIR; STAVUDINE; TENOFOVIR; TIPRANAVIR; URACIL; VIRUS ENZYME; ZIDOVUDINE;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DRUG SENSITIVITY; DRUG TARGETING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN TISSUE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SENSITIVITY ANALYSIS; VIRAL GENETICS; VIRUS RECOMBINANT;

ANTI-HIV AGENTS; BASE SEQUENCE; DRUG RESISTANCE, MULTIPLE, VIRAL; GENES, POL; HEK293 CELLS; HIV INFECTIONS; HIV INTEGRASE INHIBITORS; HIV PROTEASE INHIBITORS; HIV REVERSE TRANSCRIPTASE; HIV-1; HUMANS; PHENOTYPE; REVERSE TRANSCRIPTASE INHIBITORS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASE H; SEQUENCE ANALYSIS, RNA;

EID: 79960330731     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00396-11     Document Type: Article

References (87)

1. + T cell counts associated with low viral pol replication capacity among treatment-naive adults in early HIV-1 infection. J. Infect. Dis. 190:251-256.
2. Bates, M., T. Wrin, W. Huang, C. Petropoulos, and N. Hellmann. 2003. Practical applications of viral fitness in clinical practice. Curr. Opin. Infect. Dis. 16:11-18.
3. Bona, R., et al. 2006. Development of a human immunodeficiency virus vector-based, single-cycle assay for evaluation of anti-integrase compounds. Antimicrob. Agents Chemother. 50:3407-3417.
4. Boucher, C. A., et al. 1996. Human immunodeficiency virus type 1 drug susceptibility determination by using recombinant viruses generated from patient sera tested in a cell-killing assay. Antimicrob. Agents Chemother. 40:2404-2409.
5. Brehm, J. H., et al. 2007. Selection of mutations in the connection and RNase H domains of human immunodeficiency virus type 1 reverse transcriptase that increase resistance to 3′-azido-3′-dideoxythymidine. J. Virol. 81:7852-7859. (Pubitemid 47101471)
6. Buchacz, K., R. K. Baker, B. Young, and J. T. Brooks. 2010. Changes in the use of HIV antiretroviral resistance testing in a large cohort of U.S. patients, 1999 to 2006. J. Acquir. Immune. Defic. Syndr. 53:625-632.
7. Choi, J. Y., O. K. Kwon, S. Y. Choi, Y. K. Park, and S. S. Kim. 2011. Drug susceptibility of human immunodeficiency virus type 1-derived pseudoviruses from treatment-experienced patients to protease inhibitors and reverse transcriptase inhibitors, using a modified single-round assay. J. Clin. Virol. 50:19-25.
8. Church, J. D., et al. 2009. Comparison of laboratory methods for analysis of non-nucleoside reverse transcriptase inhibitor resistance in Ugandan infants. AIDS Res. Hum. Retroviruses 25:657-663.
9. Covens, K., et al. 2009. Novel recombinant virus assay for measuring susceptibility of human immunodeficiency virus type 1 group M subtypes to clinically approved drugs. J. Clin. Microbiol. 47:2232-2242.
10. Dam, E., et al. 2009. Gag mutations strongly contribute to HIV-1 resistance to protease inhibitors in highly drug-experienced patients besides compensating for fitness loss. PLoS Pathog. 5:e1000345.
11. Debyser, Z., et al. 1991. An antiviral target on reverse transcriptase of human immunodeficiency virus type 1 revealed by tetrahydroimidazo-[4,5,1-jk] [1,4]benzodiazepin-2 (1H)-one and -thione derivatives. Proc. Natl. Acad. Sci. U. S. A. 88:1451-1455.
12. Deeks, S. G. 2003. Treatment of antiretroviral-drug-resistant HIV-1 infection. Lancet 362:2002-2011. (Pubitemid 37548427)
13. Deeks, S. G., et al. 2003. Persistence of drug-resistant HIV-1 after a structured treatment interruption and its impact on treatment response. AIDS 17:361-370. (Pubitemid 36223261)
14. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
15. Dudley, D. M., et al. 2009. A novel yeast-based recombination method to clone and propagate diverse HIV-1 isolates. Biotechniques 46:458-467.
16. Dunne, A. L., et al. 2001. Comparison of genotyping and phenotyping methods for determining susceptibility of HIV-1 to antiretroviral drugs. AIDS 15:1471-1475. (Pubitemid 32744593)
17. Dykes, C., H. Wu, M. Sims, J. Holden-Wiltse, and L. M. Demeter. 2010. Human immunodeficiency virus type 1 protease inhibitor drug-resistant mutants give discordant results when compared in single-cycle and multiplecycle fitness assays. J. Clin. Microbiol. 48:4035-4043.
18. Ehteshami, M., et al. 2008. Connection domain mutations N348I and A360V in HIV-1 reverse transcriptase enhance resistance to 3′-azido-3′- deoxythymidine through both RNase H-dependent and -independent mechanisms. J. Biol. Chem. 283:22222-22232.
19. Ehteshami, M., and M. Gotte. 2008. Effects of mutations in the connection and RNase H domains of HIV-1 reverse transcriptase on drug susceptibility. AIDS Rev. 10:224-235.
20. Gallego, O., L. Martin-Carbonero, J. Aguero, M. C. de, A. Corral, and V. Soriano. 2004. Correlation between rules-based interpretation and virtual phenotype interpretation of HIV-1 genotypes for predicting drug resistance in HIV-infected individuals. J. Virol. Methods 121:115-118. (Pubitemid 39180033)
21. Garcia-Perez, J., S. Sanchez-Palomino, M. Perez-Olmeda, B. Fernandez, and J. Alcami. 2007. A new strategy based on recombinant viruses as a tool for assessing drug susceptibility of human immunodeficiency virus type 1. J. Med. Virol. 79:127-137.
22. Geretti, A. M. 2007. Epidemiology of antiretroviral drug resistance in drugnaive persons. Curr. Opin. Infect. Dis. 20:22-32.
23. Grant, P. M., and A. R. Zolopa. 2009. The use of resistance testing in the management of HIV-1-infected patients. Curr. Opin. HIV AIDS 4:474-480.
24. Gupta, S., et al. 2010. Combinations of mutations in the connection domain of human immunodeficiency virus type 1 reverse transcriptase: assessing the impact on nucleoside and nonnucleoside reverse transcriptase inhibitor resistance. Antimicrob. Agents Chemother. 54:1973-1980.
25. Hales, G., et al. 2006. A randomised trial comparing genotypic and virtual phenotypic interpretation of HIV drug resistance: the CREST study. PLoS Clin. Trials 1:e18.
26. Harrigan, P. R., et al. 2001. World-wide variation in HIV-1 phenotypic susceptibility in untreated individuals: biologically relevant values for resistance testing. AIDS 15:1671-1677. (Pubitemid 32918121)
27. Harrigan, P. R., et al. 2002. A mutation in the 3′ region of the human immunodeficiency virus type 1 reverse transcriptase (Y318F) associated with nonnucleoside reverse transcriptase inhibitor resistance. J. Virol. 76:6836-6840. (Pubitemid 34633550)
28. Hertogs, K., et al. 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.
29. Hirsch, M. S., et al. 2008. Antiretroviral drug resistance testing in adult HIV-1 infection: 2008 recommendations of an International AIDS Society-USA panel. Clin. Infect. Dis. 47:266-285.
30. Japour, A. J., et al. 1993. Standardized peripheral blood mononuclear cell culture assay for determination of drug susceptibilities of clinical human immunodeficiency virus type 1 isolates. Antimicrob. Agents Chemother. 37:1095-1101.
31. Jarmy, G., M. Heinkelein, B. Weissbrich, C. Jassoy, and A. Rethwilm. 2001. Phenotypic analysis of the sensitivity of HIV-1 to inhibitors of the reverse transcriptase, protease, and integrase using a self-inactivating virus vector system. J. Med. Virol. 64:223-231.
32. Johnson, V. A., et al. 2010. Update of the drug resistance mutations in HIV-1: December 2010. Top. HIV Med. 18:156-163.
33. Kellam, P., and B. A. Larder. 1994. Recombinant virus assay: a rapid, phenotypic assay for assessment of drug susceptibility of human immunodeficiency virus type 1 isolates. Antimicrob. Agents Chemother. 38:23-30.
34. Kusumi, K., et al. 1992. Human immunodeficiency virus type 1 envelope gene structure and diversity in vivo and after cocultivation in vitro. J. Virol. 66:875-885.
35. Lambert-Niclot, S., et al. 2008. Impact of gag mutations on selection of darunavir resistance mutations in HIV-1 protease. J. Antimicrob. Chemother. 62:905-908.
36. Larrouy, L., et al. 2010. Gag mutations can impact virological response to dual-boosted protease inhibitor combinations in antiretroviral-naive HIVinfected patients. Antimicrob. Agents Chemother. 54:2910-2919.
37. Larrouy, L., et al. 2011. Positive impact of HIV-1 gag cleavage site mutations on virological response to darunavir boosted with ritonavir. Antimicrob. Agents Chemother. 55:1754-1757.
38. Li, F., et al. 2003. PA-457: a potent HIV inhibitor that disrupts core condensation by targeting a late step in Gag processing. Proc. Natl. Acad. Sci. U. S. A. 100:13555-13560.
39. MacArthur, R. D. 2009. Understanding HIV phenotypic resistance testing: usefulness in managing treatment-experienced patients. AIDS Rev. 11:223-230.
40. Maguire, M. F., et al. 2002. Changes in human immunodeficiency virus type 1 Gag at positions L449 and P453 are linked to I50V protease mutants in vivo and cause reduction of sensitivity to amprenavir and improved viral fitness in vitro. J. Virol. 76:7398-7406. (Pubitemid 34760962)
41. Marchand, C., et al. 2008. Madurahydroxylactone derivatives as dual inhibitors of human immunodeficiency virus type 1 integrase and RNase H. Antimicrob. Agents Chemother. 52:361-364.
42. Martinez-Picado, J., L. Sutton, M. P. De Pasquale, A. V. Savara, and R. T. D'Aquila. 1999. Human immunodeficiency virus type 1 cloning vectors for antiretroviral resistance testing. J. Clin. Microbiol. 37:2943-2951.
43. McCormick, A. L., et al. 2011. The impact of the N348I mutation in HIV-1 reverse transcriptase, on non-nucleoside reverse transcriptase inhibitor resistance in non subtype B HIV-1. Antimicrob. Agents Chemother. 55:1806-1809.
44. Meyerhans, A., et al. 1989. Temporal fluctuations in HIV quasispecies in vivo are not reflected by sequential HIV isolations. Cell 58:901-910.
45. Mo, H., L. Lu, R. Pithawalla, D. J. Kempf, and A. Molla. 2004. Complementation in cells cotransfected with a mixture of wild-type and mutant human immunodeficiency virus (HIV) influences the replication capacities and phenotypes of mutant variants in a single-cycle HIV resistance assay. J. Clin. Microbiol. 42:4169-4174.
46. Nikolenko, G. N., et al. 2007. Mutations in the connection domain of HIV-1 reverse transcriptase increase 3′-azido-3′-deoxythymidine resistance. Proc. Natl. Acad. Sci. U. S. A. 104:317-322.
47. Paolucci, S., F. Baldanti, M. Zavattoni, and G. Gerna. 2004. Novel recombinant phenotypic assay for clonal analysis of reverse transcriptase mutations conferring drug resistance to HIV-1 variants. J. Antimicrob. Chemother. 53:766-771.
48. Paredes, R., and B. Clotet. 2010. Clinical management of HIV-1 resistance. Antiviral Res. 85:245-265.
49. Parkin, N., et al. 2002. Phenotypic and genotypic HIV-1 drug resistance assays provide complementary information. J. Acquir. Immune. Defic. Syndr. 31:128-136.
50. Parkin, N. T., et al. 2004. Natural variation of drug susceptibility in wild-type human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 48:437-443.
51. Petropoulos, C. J., et al. 2000. A novel phenotypic drug susceptibility assay for human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 44:920-928.
52. Qari, S. H., et al. 2002. Comparative analysis of two commercial phenotypic assays for drug susceptibility testing of human immunodeficiency virus type 1. J. Clin. Microbiol. 40:31-35.
53. Quinones-Mateu, M. E., and E. J. Arts. 2001. HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution, p. 134-170. In C. Kuiken, et al. (ed.), HIV sequence compendium 2001. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM.
54. Quinones-Mateu, M. E., and E. J. Arts. 2002. Fitness of drug resistant HIV-1: methodology and clinical implications. Drug Resist. Updat. 5:224-233.
55. Quinones-Mateu, M. E., and E. J. Arts. 2006. Virus fitness: concept, quantification, and application to HIV population dynamics. Curr. Top. Microb. Immunol. 299:83-140.
56. Quinones-Mateu, M. E., et al. 2000. A dual infection/competition assay shows a correlation between ex vivo human immunodeficiency virus type 1 fitness and disease progression. J. Virol. 74:9222-9233.
57. Race, E., E. Dam, V. Obry, S. Paulous, and F. Clavel. 1999. Analysis of HIV cross-resistance to protease inhibitors using a rapid single-cycle recombinant virus assay for patients failing on combination therapies. AIDS 13:2061-2068. (Pubitemid 29509582)
58. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
59. Richman, D. D., et al. 2004. The prevalence of antiretroviral drug resistance in the United States. AIDS 18:1393-1401. (Pubitemid 38925131)
60. Robinson, B. F., and R. Bakeman. 1998. ComKappa: a Windows 95 program for calculating kappa and related statistics. Behav. Res. Methods Instruments Computers 30:731-732.
61. Robinson, L. H., C. V. Gale, and J. P. Kleim. 2002. Inclusion of full-length human immunodeficiency virus type 1 (HIV-1) gag sequences in viral recombinants applied to drug susceptibility phenotyping. J. Virol. Methods 104:147-160.
62. Roman, F., et al. 2006. A new recombinant virus system for the study of HIV-1 entry and inhibition. J. Virol. Methods 131:99-104. (Pubitemid 41772567)
63. Roquebert, B., and A. G. Marcelin. 2008. The involvement of HIV-1 RNAse H in resistance to nucleoside analogues. J. Antimicrob. Chemother. 61:973-975.
64. Ross, L., et al. 2005. A direct comparison of drug susceptibility to HIV type 1 from antiretroviral experienced subjects as assessed by the antivirogram and PhenoSense assays and by seven resistance algorithms. AIDS Res. Hum. Retroviruses 21:933-939.
65. Schuckmann, M. M., et al. 2010. The N348I mutation at the connection subdomain of HIV-1 reverse transcriptase decreases binding to nevirapine. J. Biol. Chem. 285:38700-38709.
66. Selhorst, P., et al. 2011. Human immunodeficiency virus type 1 resistance or cross-resistance to nonnucleoside reverse transcriptase inhibitors currently under development as microbicides. Antimicrob. Agents Chemother. 55:1403-1413.
67. Shi, C., and J. W. Mellors. 1997. A recombinant retroviral system for rapid in vivo analysis of human immunodeficiency virus type 1 susceptibility to reverse transcriptase inhibitors. Antimicrob. Agents Chemother. 41:2781-2785.
68. Sista, P., et al. 2009. Nine-year trends in clinically relevant reduced susceptibility of HIV-1 to antiretrovirals. J. Clin. Virol. 44:190-194.
69. Tang, J. W., and D. Pillay. 2004. Transmission of HIV-1 drug resistance. J. Clin. Virol. 30:1-10.
70. Thompson, M. A., et al. 2010. Antiretroviral treatment of adult HIV infection: 2010 recommendations of the International AIDS Society-USA panel. JAMA 304:321-333.
71. Van Baelen, K., et al. 2009. A combined genotypic and phenotypic human immunodeficiency virus type 1 recombinant virus assay for the reverse transcriptase and integrase genes. J. Virol. Methods 161:231-239.
72. Van Houtte, M., et al. 2009. A comparison of HIV-1 drug susceptibility as provided by conventional phenotyping and by a phenotype prediction tool based on viral genotype. J. Med. Virol. 81:1702-1709.
73. Verlinden, Y., et al. 2005. Assessment of the antivirogram performance over time including a revised definition of biological test cut-off values. Antivir. Ther. 10:S51.
74. Vermeiren, H., et al. 2007. Prediction of HIV-1 drug susceptibility phenotype from the viral genotype using linear regression modeling. J. Virol. Methods 145:47-55. (Pubitemid 47247892)
75. Wang, J., R. A. Bambara, L. M. Demeter, and C. Dykes. 2010. Reduced fitness in cell culture of HIV-1 with nonnucleoside reverse transcriptase inhibitor-resistant mutations correlates with relative levels of reverse transcriptase content and RNase H activity in virions. J. Virol. 84:9377-9389.
76. Wang, K., R. Samudrala, and J. E. Mittler. 2004. Antivirogram or PhenoSense: a comparison of their reproducibility and an analysis of their correlation. Antivir. Ther. 9:703-712.
77. Weber, J., and M. E. Quinones-Mateu. 2007. Novel anti-HIV-1 screening system based on intact recombinant viruses expressing synthetic firefly and Renilla luminescent proteins. Antivir. Ther. 12:S155.
78. Weber, J., et al. 2010. Characterization of mutations associated with resistance to MPC-4326 and their effect on HIV-1 replicative fitness. Antivir. Ther. 15:A56.
79. Weber, J., et al. 2010. Resistance mutations in protease, reverse transcriptase, and integrase genes: do they have an epistatic effect on drug susceptibility and/or HIV-1 replicative fitness? Antivir. Ther. 15:A94.
80. Weber, J., et al. 2006. Use of a novel assay based on intact recombinant viruses expressing green (EGFP) or red (DsRed2) fluorescent proteins to examine the contribution of pol and env genes to overall HIV-1 replicative fitness. J. Virol. Methods 136:102-117. (Pubitemid 44051582)
81. Winters, B., et al. 2008. Determination of clinically relevant cutoffs for HIV-1 phenotypic resistance estimates through a combined analysis of clinical trial and cohort data. J. Acquir. Immune. Defic. Syndr. 48:26-34.
82. Winters, B., et al. 2009. Clinical cut-offs for HIV-1 phenotypic resistance estimates: update based on recent pivotal clinical trial data and a revised approach to viral mixtures. J. Virol. Methods 162:101-108.
83. World Health Organization. 2010. Towards universal access: scaling up priority HIV/AIDS interventions in the health sector. Progress report 2010. World Health Organization, Geneva, Switzerland. http://www.who.int/hiv/pub/ 2010progressreport/en/.
84. Yap, S. H., et al. 2007. N348I in the connection domain of HIV-1 reverse transcriptase confers zidovudine and nevirapine resistance. PLoS Med. 4:e335.
85. Zazzi, M., et al. 2004. Comparative evaluation of three computerized algorithms for prediction of antiretroviral susceptibility from HIV type 1 genotype. J. Antimicrob. Chemother. 53:356-360.
86. Zhang, J., S. Y. Rhee, J. Taylor, and R. W. Shafer. 2005. Comparison of the precision and sensitivity of the Antivirogram and PhenoSense HIV drug susceptibility assays. J. Acquir. Immune. Defic. Syndr. 38:439-444.
87. Zolopa, A. R. 2010. The evolution of HIV treatment guidelines: current state-of-the-art of ART. Antiviral Res. 85:241-244.