Fitness of drug resistant HIV-1: methodology and clinical implications

Antinori, 2001, Drug-resistant mutants of HIV-1 in patients exhibiting increasing CD4 cell count despite virological failure of highly active antiretroviral therapy, AIDS, 15, 2325, 10.1097/00002030-200111230-00017 Archer, 2000, Mutants of human immunodeficiency virus type 1 (HIV-1) reverse transcriptase resistant to nonnucleoside reverse transcriptase inhibitors demonstrate altered rates of RNase H cleavage that correlate with HIV-1 replication fitness in cell culture, J. Virol., 74, 8390, 10.1128/JVI.74.18.8390-8401.2000 Arts, E.J., Ball, S.C., Abraha, A., 2002. Ex vivo fitness studies provides evidence of the natural attenuation of human immunodeficiency virus type 1 subtype C during the AIDS epidemic, Barcelona, Spain. pp. 349–350. Berkhout, 1999, HIV-1 evolution under pressure of protease inhibitors: climbing the stairs of viral fitness, J. Biomed. Sci., 6, 298, 10.1007/BF02253518 Berkhout, 1999, Proposed alternatives for the use of anti-HIV drugs, Drug Resist. Updat., 2, 69, 10.1054/drup.1998.0067 Birk, 2001, Kinetics of HIV-1 RNA and resistance-associated mutations after cessation of antiretroviral combination therapy, AIDS, 15, 1359, 10.1097/00002030-200107270-00005 Blaak, 1998, In vitro replication kinetics of human immunodeficiency virus type 1 (HIV-1) variants in relation to virus load in long-term survivors of HIV-1 infection, J. Infect. Dis., 177, 600, 10.1086/514219 Bleiber, 2001, Individual contributions of mutant protease and reverse transcriptase to viral infectivity, replication, and protein maturation of antiretroviral drug-resistant human immunodeficiency virus type 1, J. Virol., 75, 3291, 10.1128/JVI.75.7.3291-3300.2001 Borman, 1996, Resistance of human immunodeficiency virus type 1 to protease inhibitors: selection of resistance mutations in the presence and absence of the drug, J. Gen. Virol., 77, 419, 10.1099/0022-1317-77-3-419 Buhler, 2001, Viral evolution in response to the broad-based retroviral protease inhibitor TL-3, J. Virol., 75, 9502, 10.1128/JVI.75.19.9502-9508.2001 Clavel, 2000, HIV drug resistance and viral fitness, Adv. Pharmacol., 49, 41, 10.1016/S1054-3589(00)49023-X Coffin, 1995, HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy, Science, 267, 483, 10.1126/science.7824947 Croteau, 1997, Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors, J. Virol., 71, 1089, 10.1128/JVI.71.2.1089-1096.1997 De Ronde, 2001, Establishment of new transmissible and drug-sensitive human immunodeficiency virus type 1 wild types due to transmission of nucleoside analogue-resistant virus, J. Virol., 75, 595, 10.1128/JVI.75.2.595-602.2001 Deeks, 2000, Determinants of virological response to antiretroviral therapy: implications for long-term strategies, Clin. Infect. Dis., 30, S177, 10.1086/313855 Deeks, 2001, International perspectives on antiretroviral resistance. Nonnucleoside reverse transcriptase inhibitor resistance, J. Acquir. Immune. Defic. Syndr., 26, S25, 10.1097/00042560-200103011-00004 Deeks, 2000, Sustained CD4+ T cell response after virologic failure of protease inhibitor-based regimens in patients with human immunodeficiency virus infection, J. Infect. Dis., 181, 946, 10.1086/315334 Deeks, 2001, Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia, N. Engl. J. Med., 344, 472, 10.1056/NEJM200102153440702 Devereux, 2001, Replicative fitness in vivo of HIV-1 variants with multiple drug resistance-associated mutations, J. Med. Virol., 65, 218, 10.1002/jmv.2023 Devereux, 2000, Substantial correlation between HIV type 1 drug-associated resistance mutations in plasma and peripheral blood mononuclear cells in treatment-experienced patients, AIDS Res. Hum. Retroviruses, 16, 1025, 10.1089/08892220050075273 Domingo, 2000, Viruses at the edge of adaptation, Virology, 270, 251, 10.1006/viro.2000.0320 Domingo, E., Escarmis, C., Menendez-Arias, L., Holland, J., 1999. Viral quasispecies and fitness variations. In: Domingo, E., Webster, R., Holland, J. (Eds.), Origin and Evolution of Viruses. Academic Press, San Diego, pp. 141–161. Domingo, 1997, RNA virus mutations and fitness for survival, Annu. Rev. Microbiol., 51, 151, 10.1146/annurev.micro.51.1.151 Doyon, 1996, Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors, J. Virol., 70, 3763, 10.1128/JVI.70.6.3763-3769.1996 Eastman, 1998, Genotypic changes in human immunodeficiency virus type 1 associated with loss of suppression of plasma viral RNA levels in subjects treated with ritonavir (Norvir) monotherapy, J. Virol., 72, 5154, 10.1128/JVI.72.6.5154-5164.1998 Eastman, 1995, Comparison of selective polymerase chain reaction primers and differential probe hybridization of polymerase chain reaction products for determination of relative amounts of codon 215 mutant and wild-type HIV-1 populations, J. Acquir. Immune. Defic. Syndr. Hum. Retrovirol., 9, 264, 10.1097/00042560-199507000-00007 Garcia-Lerma, 2000, Evidence of a role for the Q151L mutation and the viral background in development of multiple dideoxynucleoside-resistant human immunodeficiency virus type 1, J. Virol., 74, 9339, 10.1128/JVI.74.20.9339-9346.2000 Gerondelis, 1999, The P236L delavirdine-resistant human immunodeficiency virus type 1 mutant is replication defective and demonstrates alterations in both RNA 5′-end- and DNA 3′-end-directed RNase H activities, J. Virol., 73, 5803, 10.1128/JVI.73.7.5803-5813.1999 Goudsmit, 1997, Broad spectrum of in vivo fitness of human immunodeficiency virus type 1 subpopulations differing at reverse transcriptase codons 41 and 215, J. Virol., 71, 4479, 10.1128/JVI.71.6.4479-4484.1997 Goudsmit, 1996, Human immunodeficiency virus fitness in vivo: calculations based on a single zidovudine resistance mutation at codon 215 of reverse transcriptase, J. Virol., 70, 5662, 10.1128/JVI.70.8.5662-5664.1996 Grant, R.M., Liegler, T., Bonhoeffer, S., Elkin, C., Nijjar, S., Wrin, T., Ho, R., Kolberg, J., Hellerstein, M.K., Hellmann, N.S., Petropoulos, C.J., Deeks, S.G., 2001. Large fitness differences between protease inhibitor susceptible and resistant HIV-1 in vivo. In: Proceedings of the 8th Annual HIV Dynamics and Evolution Meeting. Hance, 2001, Changes in human immunodeficiency virus type 1 populations after treatment interruption in patients failing antiretroviral therapy, J. Virol., 75, 6410, 10.1128/JVI.75.14.6410-6417.2001 Harrigan, 1998, Relative replicative fitness of zidovudine-resistant human immunodeficiency virus type 1 isolates in vitro, J. Virol., 72, 3773, 10.1128/JVI.72.5.3773-3778.1998 Havlir, 1996, Nevirapine-resistant human immunodeficiency virus: kinetics of replication and estimated prevalence in untreated patients, J. Virol., 70, 7894, 10.1128/JVI.70.11.7894-7899.1996 Hertogs, 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, 10.1128/AAC.42.2.269 Hirsch, 1998, Antiretroviral drug resistance testing in adults with HIV infection: implications for clinical management. International AIDS Society—USA Panel, JAMA, 279, 1984, 10.1001/jama.279.24.1984 Ho, 1994, Characterization of human immunodeficiency virus type 1 variants with increased resistance to a C2-symmetric protease inhibitor, J. Virol., 68, 2016, 10.1128/JVI.68.3.2016-2020.1994 Holland, 1991, Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses, J. Virol., 65, 2960, 10.1128/JVI.65.6.2960-2967.1991 Iglesias-Ussel, 2002, In vitro analysis of HIV-1 resistance to nevirapine and fitness determination of resistant variants, J. Gen. Virol., 83, 93, 10.1099/0022-1317-83-1-93 Imamichi, 2000, Relative replication fitness of a high-level 3′-azido-3′-deoxythymidine- resistant variant of human immunodeficiency virus type 1 possessing an amino acid deletion at codon 67 and a novel substitution (Thr → Gly) at codon 69, J. Virol., 74, 10958, 10.1128/JVI.74.23.10958-10964.2000 Imamichi, 2001, Amino acid deletion at codon 67 and Thr-to-Gly change at codon 69 of human immunodeficiency virus type 1 reverse transcriptase confer novel drug resistance profiles, J. Virol., 75, 3988, 10.1128/JVI.75.8.3988-3992.2001 Kellam, 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, 10.1128/AAC.38.1.23 Kijak, 2002, Origin of human immunodeficiency virus type 1 quasispecies emerging after antiretroviral treatment interruption in patients with therapeutic failure, J. Virol., 76, 7000, 10.1128/JVI.76.14.7000-7009.2002 Kosalaraksa, 1999, Comparative fitness of multi-dideoxynucleoside-resistant human immunodeficiency virus type 1 (HIV-1) in an in vitro competitive HIV-1 replication assay, J. Virol., 73, 5356, 10.1128/JVI.73.7.5356-5363.1999 Louwagie, 1994, Genetic analysis of HIV-1 isolates from Brazil reveals presence of two distinct genetic subtypes, AIDS Res. Hum. Retroviruses, 10, 561, 10.1089/aid.1994.10.561 Loveday, 2001, International perspectives on antiretroviral resistance. Nucleoside reverse transcriptase inhibitor resistance, J. Acquir. Immune. Defic. Syndr., 26, S10, 10.1097/00042560-200103011-00003 Lu, 2001, A novel recombinant marker virus assay for comparing the relative fitness of HIV-1 reverse transcriptase variants, J. Acquir. Immune. Defic. Syndr., 27, 7, 10.1097/00042560-200105010-00002 Maeda, 1998, Altered drug sensitivity, fitness, and evolution of human immunodeficiency virus type 1 with pol gene mutations conferring multi-dideoxynucleoside resistance, J. Infect. Dis., 177, 1207, 10.1086/515282 Mammano, 1998, Resistance-associated loss of viral fitness in human immunodeficiency virus type 1: phenotypic analysis of protease and gag coevolution in protease inhibitor-treated patients, J. Virol., 72, 7632, 10.1128/JVI.72.9.7632-7637.1998 Mammano, 2000, Retracing the evolutionary pathways of human immunodeficiency virus type 1 resistance to protease inhibitors: virus fitness in the absence and in the presence of drug, J. Virol., 74, 8524, 10.1128/JVI.74.18.8524-8531.2000 Markowitz, 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, 10.1128/JVI.69.2.701-706.1995 Martinez-Picado, 2000, Fitness of human immunodeficiency virus type 1 protease inhibitor-selected single mutants, Virology, 275, 318, 10.1006/viro.2000.0527 Martinez-Picado, 1999, Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1, J. Virol., 73, 3744, 10.1128/JVI.73.5.3744-3752.1999 Meroni, 2002, Reduced levels of CD4 cell spontaneous apoptosis in human immunodeficiency virus-infected patients with discordant response to protease inhibitors, J. Infect. Dis., 186, 143, 10.1086/341075 Miller, 2001, International perspectives on antiretroviral resistance. Resistance to protease inhibitors, J. Acquir. Immune. Defic. Syndr., 26, S34, 10.1097/00042560-200103011-00005 Miller, 2001, Structured treatment interruptions in antiretroviral management of HIV-1, Curr. Opin. Infect. Dis., 14, 29, 10.1097/00001432-200102000-00006 Nelson, 2000, Patterns of changes in human immunodeficiency virus type 1 V3 sequence populations late in infection, J. Virol., 74, 8494, 10.1128/JVI.74.18.8494-8501.2000 Nijhuis, 2001, Implications of antiretroviral resistance on viral fitness, Curr. Opin. Infect. Dis., 14, 23, 10.1097/00001432-200102000-00005 Nijhuis, 1999, Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy, AIDS, 13, 2349, 10.1097/00002030-199912030-00006 Ortiz, 2001, Structured antiretroviral treatment interruptions in chronically HIV-1-infected subjects, Proc. Natl. Acad. Sci. U.S.A., 98, 13288, 10.1073/pnas.221452198 Pazhanisamy, 1996, Kinetic characterization of human immunodeficiency virus type-1 protease-resistant variants, J. Biol. Chem., 271, 17979, 10.1074/jbc.271.30.17979 Petropoulos, 2000, A novel phenotypic drug susceptibility assay for human immunodeficiency virus type 1, Antimicrob. Agents Chemother., 44, 920, 10.1128/AAC.44.4.920-928.2000 Picchio, 2000, Altered viral fitness of HIV-1 following failure of protease inhibitor-based therapy, J. Acquir. Immune. Defic. Syndr., 25, 289, 10.1097/00042560-200012010-00001 Pierson, 2000, Reservoirs for HIV-1: mechanisms for viral persistence in the presence of antiviral immune responses and antiretroviral therapy, Annu. Rev. Immunol., 18, 665, 10.1146/annurev.immunol.18.1.665 Piketty, 2001, Long-term clinical outcome of human immunodeficiency virus-infected patients with discordant immunologic and virologic responses to a protease inhibitor-containing regimen, J. Infect. Dis., 183, 1328, 10.1086/319861 Prado, 2002, Amprenavir resistant HIV-1 exhibits lopinavir cross-resistance and reduced replication capacity, AIDS, 16, 1009, 10.1097/00002030-200205030-00007 Quiñones-Mateu, M.E., Arts, E.J., 2001. HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution. In: Kuiken, C., Foley, B., Hahn, B., Marx, P., McCutchan, F., Mellors, J., Wolinsky, S., Korber, B. (Eds.), HIV Sequence Compendium 2001, Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM, pp. 134–170. Quiñones-Mateu, 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, 10.1128/JVI.74.19.9222-9233.2000 Quiñones-Mateu, M.E., Weber, J., Rangel, H.R., Chakraborty, B., Martinez, M.A., Este, J.A., Martinez-Picado, J., Ruiz, L., Clotet, B., Wrin, T., Petropoulos, C.J., 2002. A novel TaqMan real-time PCR method to estimate HIV-1 fitness in the era of multi-target antiretroviral therapy. In: Proceedings of the XI International HIV Drug Resistance Meeting, Seville, Spain. Rayner, 1997, Population dynamics studies of wild-type and drug-resistant mutant HIV in mixed infections, Virology, 236, 85, 10.1006/viro.1997.8620 Resch, 2001, A multiple-site-specific heteroduplex tracking assay as a tool for the study of viral population dynamics, Proc. Natl. Acad. Sci. U.S.A., 98, 176, 10.1073/pnas.011511298 Resch, 2002, Nelfinavir-resistant, amprenavir-hypersusceptible strains of human immunodeficiency virus type 1 carrying an N88S mutation in protease have reduced infectivity, reduced replication capacity, and reduced fitness and process the Gag polyprotein precursor aberrantly, J. Virol., 76, 8659, 10.1128/JVI.76.17.8659-8666.2002 Ripamonti, 2002, Discordant immunological response in HIV-positive patients on non-nucleoside reverse transcriptase inhibitor-based regimens, AIDS, 16, 130, 10.1097/00002030-200201040-00019 Robinson, 2000, HIV type 1 protease cleavage site mutations and viral fitness: implications for drug susceptibility phenotyping assays, AIDS Res. Hum. Retroviruses, 16, 1149, 10.1089/088922200414992 Ruiz-Jarabo, 2000, Memory in viral quasispecies, J. Virol., 74, 3543, 10.1128/JVI.74.8.3543-3547.2000 Sharma, 1997, Attenuated replication of human immunodeficiency virus type 1 with a didanosine-selected reverse transcriptase mutation [published erratum appears in J Virol 1998 Apr;72(4):3504], J. Virol., 71, 8846, 10.1128/JVI.71.11.8846-8851.1997 Sharma, 1999, Decreased processivity of human immunodeficiency virus type 1 reverse transcriptase (RT) containing didanosine-selected mutation Leu74Val: a comparative analysis of RT variants Leu74Val and lamivudine-selected Met184Val, J. Virol., 73, 8448, 10.1128/JVI.73.10.8448-8456.1999 Shi, 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, 10.1128/AAC.41.12.2781 Stoddart, 2001, Impaired replication of protease inhibitor-resistant HIV-1 in human thymus, Nat. Med., 7, 712, 10.1038/89090 Verhofstede, 1999, Interruption of reverse transcriptase inhibitors or a switch from reverse transcriptase to protease inhibitors resulted in a fast reappearance of virus strains with a reverse transcriptase inhibitor-sensitive genotype, AIDS, 13, 2541, 10.1097/00002030-199912240-00007 Wood, 2002, “Discordant” increases in CD4 cell count relative to plasma viral load in a closely followed cohort of patients initiating antiretroviral therapy, J. Acquir. Immune. Defic. Syndr., 30, 159, 10.1097/00042560-200206010-00004 Wrin, T., Gamarnik, A., Whitehurst, N., Beauchaine, J., Whitcomb, J.M., Hellmann, N.S., Petropoulos, C.J., 2001. Natural variation of replication capacity measurements in drug-naive/susceptible HIV-1. In: Proceedings of the 5th International Workshop on HIV Drug Resistance & Treatment Strategies, Scottsdale, Arizona, June 2001, Abstract 24. Yerly, 1998, Switch to unusual amino acids at codon 215 of the human immunodeficiency virus type 1 reverse transcriptase gene in seroconvertors infected with zidovudine-resistant variants, J. Virol., 72, 3520, 10.1128/JVI.72.5.3520-3523.1998 Zhang, 1999, Quantifying residual HIV-1 replication in patients receiving combination antiretroviral therapy, N. Engl. J. Med., 340, 1605, 10.1056/NEJM199905273402101