Characterization of a Subtype D Human Immunodeficiency Virus Type 1 Isolate That Was Obtained from an Untreated Individual and That Is Highly Resistant to Nonnucleoside Reverse Transcriptase Inhibitors

Journal of Virology

Volumn 78, Issue 10, 2004, Pages 5390-5401

  Gao, Yong ^a   Paxinos, Ellen ^b   Galovich, Justin ^b   Troyer, Ryan ^a   Baird, Heather ^a   Abreha, Measho ^a   Kityo, Cissy ^c   Mugyenyi, Peter ^c   Petropoulos, Christos ^b   Arts, Eric J ^a,d  

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

^b MONOGRAM BIOSCIENCES   (United States)

^c JOINT CLINICAL RESEARCH CENTRE   (Uganda)

^d CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DELAVIRDINE; EFAVIRENZ; ISOLEUCINE; LEUCINE; NEVIRAPINE; POL PROTEIN; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR; THREONINE; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; CELL CULTURE; CROSS RESISTANCE; DRUG SENSITIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MOLECULAR CLONING; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; UGANDA; VIRUS INHIBITION; VIRUS RECOMBINANT; VIRUS STRAIN;

DRUG RESISTANCE, VIRAL; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; HUMANS; MUTATION; POLYMORPHISM, GENETIC; REVERSE TRANSCRIPTASE INHIBITORS;

EID: 2342484502     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.78.10.5390-5401.2004     Document Type: Article

References (54)

1. Adje, C., R. Cheingsong, T. H. Roels, C. Maurice, G. Djomand, W. Verbiest, K. Hertogs, B. Larder, B. Monga, M. Peeters, S. Eholie, E. Bissagene, M. Coulibaly, R. Respess, S. Z. Wiktor, T. Chorba, and J. N. Nkengasong. 2001. High prevalence of genotypic and phenotypic HIV-1 drug-resistant strains among patients receiving antiretroviral therapy in Abidjan, Cote d'Ivoire. J. Acquir. Immune. Defic. Syndr. 26:501-506.
2. Adje-Toure, C., B. Celestin, D. Hanson, T. H. Roels, K. Hertogs, B. Larder, F. Diomande, M. Peeters, S. Eholie, E. Lackritz, T. Chorba, and J. N. Nkengasong. 2003. Prevalence of genotypic and phenotypic HIV-1 drug-resistant strains among patients who have rebound in viral load while receiving antiretroviral therapy in the UNAIDS-Drug Access Initiative in Abidjan, Cote d'Ivoire. AIDS 17(Suppl. 3):S23-S29.
3. Artico, M. 1996. Non-nucleoside anti-HIV-1 reverse transcriptase inhibitors (NNRTIs): a chemical survey from lead compounds to selected drugs for clinical trials. Farmaco 51:305-331.
4. Arts, E. J., and M. A. Wainberg. 1996. Mechanisms of nucleoside analog antiviral activity and resistance during human immunodeficiency virus reverse transcription. Antimicrob. Agents Chemother. 40:527-540.
5. Bacheler, L. T. 1999. Resistance to non-nucleoside inhibitors of HIV-1 reverse transcriptase. Drug Resist. Update 2:56-67.
6. Bacheler, L. T., E. D. Anton, P. Kudish, D. Baker, J. Bunville, K. Krakowski, L. Bolling, M. Aujay, X. V. Wang, D. Ellis, M. F. Becker, A. L. Lasut, H. J. George, D. R. Spalding, G. Hollis, and K. Abremski. 2000. Human immunodeficiency virus type 1 mutations selected in patients failing efavirenz combination therapy. Antimicrob. Agents Chemother. 44:2475-2484.
7. Ball, S. C., A. Abraha, K. R. Collins, A. J. Marozsan, H. Baird, M. E. Quinones-Mateu, A. Penn-Nicholson, M. Murray, N. Richard, M. Lobritz, P. A. Zimmerman, T. Kawamura, A. Blauvelt, and E. J. Arts. 2003. Comparing the ex vivo fitness of CCR5-tropic human immunodeficiency virus type 1 isolates of subtypes B and C. J. Virol. 77:1021-1038.
8. Balzarini, J., and E. De Clercq. 2001. Nucleoside and nucleotide reverse transcriptase inhibitors, p. 31-62. In E. D. A. De Clercq (ed.), Antiretroviral therapy. ASM Press, Washington, D.C.
9. Balzarini, J., R. Esnouf, and E. De Clercq. 2001. Nonnucleoside reverse transcriptase inhibitors, p. 63-86. In E. D. A. De Clercq (ed.), Antiretroviral therapy. ASM Press, Washington, D.C.
10. Balzarini, J., W. G. Brouwer, E. E. Felauer, E. De Clercq, and A. Karlsson. 1995. Activity of various thiocarboxanilide derivatives against wild-type and several mutant human immunodeficiency virus type 1 strains. Antiviral Res. 27:219-236.
11. Barreiro, P., V. Soriano, F. Blanco, C. Casimiro, J. J. de la Cruz, and J. Gonzalez-Lahoz. 2000. Risks and benefits of replacing protease inhibitors by nevirapine in HIV-infected subjects under long-term successful triple combination therapy. AIDS 14:807-812.
12. Boyer, P. L, J. Ding, E. Arnold, and S. H. Hughes. 1994. Subunit specificity of mutations that confer resistance to nonnucleoside inhibitors in human immunodeficiency virus type 1 reverse transcriptase. Antimicrob. Agents Chemother. 38:1909-1914.
13. Brenner, B., D. Turner, M. Oliveira, D. Moisi, M. Detorio, M. Carobene, R. G. Marlink, J. Schapiro, M. Roger, and M. A. Wainberg. 2003. A V106M mutation in HIV-1 clade C viruses exposed to efavirenz confers cross-resistance to non-nucleoside reverse transcriptase inhibitors. AIDS 17:F1-F5.
14. Brown, A. J., H. M. Precious, J. M. Whitcomb, J. K. Wong, M. Quigg, W. Huang, E. S. Daar, R. T. D'Aquila, P. H. Keiser, E. Connick, N. S. Hellmann, C. J. Petropoulos, D. D. Richman, and S. J. Little. 2000. Reduced susceptibility of human immunodeficiency virus type 1 (HIV-1) from patients with primary HIV infection to nonnucleoside reverse transcriptase inhibitors is associated with variation at novel amino acid sites. J. Virol. 74:10269-10273.
15. Caride, E., R. Brindeiro, K. Hertogs, B. Larder, P. Dehertogh, E. Machado, C. A. de Sa, W. A. Eyer-Silva, F. S. Sion, L. F. Passioni, J. A. Menezes, A. R. Calazans, and A. Tanuri. 2000. Drug-resistant reverse transcriptase genotyping and phenotyping of B and non-B subtypes (F and A) of human immunodeficiency virus type I found in Brazilian patients failing HAART. Virology 275:107-115.
16. Cherrington, J. M., M. D. Fuller, A. S. Mulato, S. J. Allen, S. C. Kunder, M. A. Ussery, Z. Lesnikowski, R. F. Schinazi, J. P. Sommadossi, and M. S. Chen. 1996. Comparative kinetic analyses of interaction of inhibitors with Rauscher murine leukemia virus and human immunodeficiency virus reverse transcriptases. Antimicrob. Agents Chemother. 40:1270-1273.
17. Condra, J. H., E. A. Emini, L. Gotlib, D. J. Graham, A. J. Schlabach, J. A. Wolfgang, R. J. Colonno, and V. V. Sardana. 1992. Identification of the human immunodeficiency virus reverse transcriptase residues that contribute to the activity of diverse nonnucleoside inhibitors. Antimicrob. Agents Chemother. 36:1441-1446.
18. Daluge, S. M., S. S. Good, M. B. Faletto, W. H. Miller, M. H. St. Clair, L. R. Boone, M. Tisdale, N. R. Pany, J. E. Reardon, R. E. Dornsife, D. R. Averett, and T. A. Krenitsky. 1997. 1592U89, a novel carbocyclic nucleoside analog with potent, selective anti-human immunodeficiency virus activity. Antimicrob. Agents Chemother. 41:1082-1093.
19. De Clercq, E. 1998. The role of non-nucleoside reverse transcriptase inhibitors (NNRTIs) in the therapy of HIV-1 infection. Antiviral Res. 38:153-179.
20. Derdeyn, C. A., J. M. Decker, J. N. Sfakianos, X. Wu, W. A. O'Brien, L. Ratner, J. C. Kappes, G. M. Shaw, and E. Hunter. 2000. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 74:8358-8367.
21. Descamps, D., G. Collin, F. Letourneur, C. Apetrei, F. Damond, I. Loussert-Ajaka, F. Simon, S. Saragosti, and F. Brun-Vezinet. 1997. Susceptibility of human immunodeficiency virus type 1 group O isolates to antiretroviral agents: in vitro phenotypic and genotypic analyses. J. Virol. 71:8893-8898.
22. Domingo, E., and J. J. Holland. 1997. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51:151-178.
23. Eshleman, S. H., and J. B. Jackson. 2002. Nevirapine resistance after single dose prophylaxis. AIDS Rev. 4:59-63.
24. Esnouf, R., J. Ren, C. Ross, Y. Jones, D. Stammers, and D. Stuart. 1995. Mechanism of inhibition of HIV-1 reverse transcriptase by non-nucleoside inhibitors. Nat. Struct. Biol. 2:303-308.
25. Guay, L. A., P. Musoke, T. Fleming, D. Bagenda, M. Allen, C. Nakabiito, J. Sherman, P. Bakaki, C. Ducar, M. Deseyve, L. Emel, M. Mirochnick, M. G. Fowler, L. Mofenson, P. Miotti, K. Dransfield, D. Bray, F. Mmiro, and J. B. Jackson. 1999. Intrapartum and neonatal single-dose nevirapine compared with zidovudine for prevention of mother-to-child transmission of HIV-1 in Kampala, Uganda: HIVNET 012 randomised trial. Lancet 354:795-802.
26. Harrigan, P. R., J. S. Montaner, S. A. Wegner, W. Verbiest, V. Miller, R. Wood, and B. A. Larder. 2001. World-wide variation in HIV-1 phenotypic susceptibility in untreated individuals: biologically relevant values for resistance testing. AIDS 15:1671-1677.
27. Ho, D. D., T. Toyoshima, H. Mo, D. J. Kempf, D. Norbeck, C. M. Chen, N. E. Wideburg, S. K. Burt, J. W. Erickson, and M. K. Singh. 1994. Characterization of human immunodeficiency virus type 1 variants with increased resistance to a C2-symmetric protease inhibitor. J. Virol. 68:2016-2020.
28. Jackson, J. B., G. Becker-Pergola, L. A. Guay, P. Musoke, M. Mracna, M. G. Fowler, L. M. Mofenson, M. Mirochnick, F. Mmiro, and S. H. Eshleman. 2000. Identification of the K103N resistance mutation in Ugandan women receiving nevirapine to prevent HIV-1 vertical transmission. AIDS 14:F111-F115.
29. Jonckheere, H., J. M. Taymans, J. Balzarini, S. Velazquez, M. J. Camarasa, J. Desmyter, E. De Clercq, and J. Anne. 1994. Resistance of HIV-1 reverse transcriptase against [2′,5′ -bis-O-(tert-butyldimethylsilyl)-3′-spiro-5″-(4″ -amino-1″,2″-oxathiole-2″,2″-dioxide)] (TSAO) derivatives is determined by the mutation Glu138→Lys on the p51 subunit. J. Biol. Chem. 269:25255-25258.
30. Kantor, R., and D. Katzenstein. 2003. Polymorphism in HIV-1 non-subtype B protease and reverse transcriptase and its potential impact on drug susceptibility and drug resistance evolution. AIDS Rev. 5:25-35.
31. Kantor, R., L. S. Zijenah, R. W. Shafer, S. Mutetwa, E. Johnston, R. Lloyd, A. von Lieven, D. Israelski, and D. A. Katzenstein. 2002. HIV-1 subtype C reverse transcriptase and protease genotypes in Zimbabwean patients failing antiretroviral therapy. AIDS Res. Hum. Retrovir. 18:1407-1413.
32. Kebba, A., D. Atwine, R. Mwebaze, C. Kityo, R. Nakityo, and M. Peter. 2002. Therapeutic responses to AZT + 3TC + EFV in advanced antiretroviral naive HIV type 1-infected Ugandan patients. AIDS Res. Hum. Retrovir. 18:1181-1187.
33. Lindberg, J., S. Sigurdsson, S. Lowgren, H. O. Andersson, C. Sahlberg, R. Noreen, K. Fridborg, H. Zhang, and T. Unge. 2002. Structural basis for the inhibitory efficacy of efavirenz (DMP-266), MSC194 and PNU142721 toward the HIV-1 RT K103N mutant. Eur. J. Biochem. 269:1670-1677.
34. Najera, I., A. Holguin, M. E. Quinones-Mateu, M. A. Munoz-Fernandez, R. Najera, C. Lopez-Galindez, and E. Domingo. 1995. Pol gene quasispecies of human immunodeficiency virus: mutations associated with drug resistance in virus from patients undergoing no drug therapy. J. Virol. 69:23-31.
35. Nijhuis, M., S. Deeks, and C. Boucher. 2001. Implications of antiretroviral resistance on viral fitness. Curr. Opin. Infect. Dis. 14:23-28.
36. Nijhuis, M., R. Schumman, D. de Jong, J. Erickson, E. Gustchina, J. Albert, P. Schipper, S. Gulnik, and C. A. Boucher. 1999. Increased fitness of drug resistant HIV-1 protease as a result of acquisition of compensatory mutations during suboptimal therapy. AIDS 13:2349-2359.
37. Nunberg, J. H., W. A. Schleif, E. J. Boots, J. A. O'Brien, J. C. Quintero, J. M. Hoffman, E. A. Emini, and M. E. Goldman. 1991. Viral resistance to human immunodeficiency virus type 1-specific pyridinone reverse transcriptase inhibitors. J. Virol. 65:4887-4892.
38. Parikh, U., C. Calef, B. Larder, R. Schinazi, and J. W. Mellors. 2003. Mutations in retroviral genes associated with drug resistance, p. 94-183. In C. Kuiken, B. Foley, E. Freed, B. Hahn, P. Marx, F. McCutchan, J. W. Mellors, S. Wolinksy, and B. Korber (ed.), HIV sequence compendium 2002. Technical report no. LA-UR 03-3564. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N.Mex.
39. Petrella, M., B. Brenner, H. Loemba, and M. A. Wainberg. 2001. HIV drug resistance and implications for the introduction of antiretroviral therapy in resource-poor countries. Drug Resist. Update 4:339-346.
40. 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.
41. Powderly, W. G., and A. Carr. 2001. AIDS 2001. Clinical treatment. Overview. AIDS 15(Suppl. 5):S159-S160.
42. Quiñones-Mateu, M. E., and E. J. Arts. 2002. HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution, p. 134-170. In C. Kuiken, B. Foley, B. Hahn, P. Marx, F. McCutchan, J. Mellors, S. Wolinsky, and B. Korber (ed.), HIV sequence compendium 2001. Technical report no. LA-UR 02-2877. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N.Mex.
43. Quinones-Mateu, M. E., S. C. Ball, A. J. Marozsan, V. S. Torre, J. L. Albright, G. Vanham, G. van Der Groen, R. L. Colebunders, and E. J. Arts. 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.
44. Reed, L. J. M. H. 1938. A simple method of estimating fifty percent end-points. Am. J. Hyg. 27:493-497.
45. Ren, J., C. Nichols, L. Bird, P. Chamberlain, K. Weaver, S. Short, D. I. Stuart, and D. K. Stammers. 2001. Structural mechanisms of drug resistance for mutations at codons 181 and 188 in HIV-1 reverse transcriptase and the improved resilience of second generation non-nucleoside inhibitors. J. Mol. Biol. 312:795-805.
46. 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.
47. Richard, N., M. Juntilla, A. Abraha, K. Demers, E. Paxinos, J. Galovich, C. J. Petropoulos, C. C. Whalen, F. Kyeyune, D. Atwine, C. Kityo, P. Mugyenyi, and E. J. Arts. 2004. High prevalence of antiviral resistance in treated Ugandans infected with non-subtype B human immunodeficiency virus type-1. AIDS Res. Hum. Retrovir. 20:355-364.
48. Richman, D., A. S. Rosenthal, M. Skoog, R. J. Eckner, T. C. Chou, J. P. Sabo, and V. J. Merluzzi. 1991. BI-RG-587 is active against zidovudine-resistant human immunodeficiency virus type 1 and synergistic with zidovudine. Antimicrob. Agents Chemother. 35:305-308.
49. Smerdon, S. J., J. Jager, J. Wang, L. A. Kohlstaedt, A. J. Chirino, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1994. Structure of the binding site for nonnucleoside inhibitors of the reverse transcriptase of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 91:3911-3915.
50. Staszewski, S., J. Morales-Ramirez, K. T. Tashima, A. Rachlis, D. Skiest, J. Stanford, R. Stryker, P. Johnson, D. F. Labriola, D. Farina, D. J. Manion, and N. M. Ruiz. 1999. Efavirenz plus zidovudine and lamivudine, efavirenz plus indinavir, and indinavir plus zidovudine and lamivudine in the treatment of HIV-1 infection in adults. N. Engl. J. Med. 341:1865-1873.
51. Torre, V. S., A. J. Marozsan, J. L. Albright, K. R. Collins, O. Hartley, R. E. Offord, M. E. Quinones-Mateu, and E. J. Arts. 2000. Variable sensitivity of CCR5-tropic human immunodeficiency virus type 1 isolates to inhibition by RANTES analogs. J. Virol. 74:4868-4876.
52. van Leeuwen, R., C. Katlama, R. L. Murphy, K. Squires, J. Gatell, A. Horban, B. Clotet, S. Staszewski, A. van Eeden, N. Clumeck, M. Moroni, A. T. Pavia, R. E. Schmidt, J. Gonzalez-Lahoz, J. Montaner, F. Antunes, R. Gulick, D. Banhegyi, d. van, V., P. Reiss, L. van Weert, F. van Leth, V. A. Johnson, J. P. Sommadossi, and J. M. Lange. 2003. A randomized trial to study first-line combination therapy with or without a protease inhibitor in HIV-1-infected patients. AIDS 17:987-999.
53. Weidle, P. J., C. M. Kityo, P. Mugyenyi, R. Downing, A. Kebba, D. Pieniazek, R. Respess, K. Hertogs, V. De, V., P. Dehertogh, S. Bloor, B. Larder, and E. Lackritz. 2001. Resistance to antiretroviral therapy among patients in Uganda. J. Acquir. Immune. Defic. Syndr. 26:495-500.
54. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution, p. 161-171, 356-366. In W. B. Provine (ed.), Evolution: selected papers. Proceedings of the Sixth International Congress of Genetics. University of Chicago Press, Chicago, Ill.