Persistence versus reversion of 3TC resistance in HIV-1 determine the rate of emergence of NVP resistance

Viruses

Volumn 4, Issue 8, 2012, Pages 1212-1234

  Rath, Barbara A ^a,b   Olshen, Richard A ^a   Halpern, Jerry ^a   Merigan, Thomas C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Adefovir; HIV 1; Lamivudine; Nevirapine; Resistance; Selection; Serial passage

Indexed keywords

ADEFOVIR; LAMIVUDINE; NEVIRAPINE; RNA DIRECTED DNA POLYMERASE INHIBITOR; TENOFOVIR;

ANIMAL CELL; ARTICLE; CODON; CONTROLLED STUDY; DRUG WITHDRAWAL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PERSISTENT VIRUS INFECTION; PROTEIN BINDING; REVERTANT; STATISTICAL MODEL; VIRUS ISOLATION; VIRUS PARTICLE; VIRUS RESISTANCE; VIRUS STRAIN;

ADEFOVIR; HIV-1; LAMIVUDINE; NEVIRAPINE; RESISTANCE; SELECTION; SERIAL PASSAGE.;

ANTI-HIV AGENTS; DRUG RESISTANCE, VIRAL; HIV INFECTIONS; HIV-1; HUMANS; LAMIVUDINE; MUTATION; NEVIRAPINE; SERIAL PASSAGE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84868606978     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v4081212     Document Type: Article

References (65)

1. Camacho, R.; Teofilo, E. Antiretroviral therapy in treatment-naive patients with HIV infection. Current opinion in HIV and AIDS 2011, 6 Suppl 1, S3-S11.
2. Akanbi, M.O.; Scarci, K.; Taiwo, B.; Murphy, R.L. Combination nucleoside/nucleotide reverse transcriptase inhibitors for treatment of HIV infection. Expert Opin. Pharmacother. 2012, 13, 65-79.
3. Rouleau, D.; Fortin, C.; Trottier, B.; Lalonde, R.; Lapointe, N.; Cote, P.; Routy, J.P.; Matte, M.F.; Tsarevsky, I.; Baril, J.G. Antiretroviral therapy for adults infected with HIV: Guidelines for health care professionals from the Quebec HIV care committee. Can. J. Infect. Dis. Med. Microbiol. 2011, 22, 52-60.
4. Sierra-Aragon, S.; Walter, H. Targets for inhibition of HIV replication: Entry, enzyme action, release and maturation. Intervirology 2012, 55, 84-97.
5. Van Rompay, K.K.; Matthews, T.B.; Higgins, J.; Canfield, D.R.; Tarara, R.P.; Wainberg, M.A.; Schinazi, R.F.; Pedersen, N.C.; North, T.W. Virulence and reduced fitness of simian immunodeficiency virus with the M184V mutation in reverse transcriptase. J. Virol. 2002, 76, 6083-6092.
6. McColl, D.J.; Margot, N.; Chen, S.S.; Harris, J.; Borroto-Esoda, K.; Miller, M.D. Reduced emergence of the M184V/I resistance mutation when antiretroviral-naive subjects use emtricitabine versus lamivudine in regimens composed of two NRTIs plus the NNRTI efavirenz. HIV Clin. Trials 2011, 12, 61-70.
7. Svedhem, V.; Bergroth, T.; Lidman, K.; Sonnerborg, A. Presence of M184I/V in minor HIV-1 populations of patients with lamivudine and/or didanosine treatment failure. HIV Med. 2007, 8, 504-510.
8. Sarafianos, S.G.; Das, K.; Clark, A.D., Jr.; Ding, J.; Boyer, P.L.; Hughes, S.H.; Arnold, E. Lamivudine (3TC) resistance in HIV-1 reverse transcriptase involves steric hindrance with beta-branched amino acids. Proc. Natl. Acad. Sci. USA 1999, 96, 10027-10032.
9. Wei, X.; Liang, C.; Gotte, M.; Wainberg, M.A. Negative effect of the M184V mutation in HIV-1 reverse transcriptase on initiation of viral DNA synthesis. Virology 2003, 311, 202-212.
10. Wei, X.; Liang, C.; Gotte, M.; Wainberg, M.A. The M184V mutation in HIV-1 reverse transcriptase reduces the restoration of wild-type replication by attenuated viruses. AIDS (London, England) 2002, 16, 2391-2398.
11. Diallo, K.; Gotte, M.; Wainberg, M.A. Molecular impact of the M184V mutation in human immunodeficiency virus type 1 reverse transcriptase. Antimicrob. Agents Chemother. 2003, 47, 3377-3383.
12. Diallo, K.; Brenner, B.; Oliveira, M.; Moisi, D.; Detorio, M.; Gotte, M.; Wainberg, M.A. The M184V substitution in human immunodeficiency virus type 1 reverse transcriptase delays the development of resistance to amprenavir and efavirenz in subtype B and C clinical isolates. Antimicrob. Agents Chemother. 2003, 47, 2376-2379.
13. Gotte, M.; Arion, D.; Parniak, M.A.; Wainberg, M.A. The M184V mutation in the reverse transcriptase of human immunodeficiency virus type 1 impairs rescue of chain-terminated DNA synthesis. J. Virol. 2000, 74, 3579-3585.
14. Sanjuan, R.; Nebot, M.R.; Chirico, N.; Mansky, L.M.; Belshaw, R. Viral mutation rates. J. Virol. 2010, 84, 9733-9748.
15. Dapp, M.J.; Holtz, C.M.; Mansky, L.M. Concomitant lethal mutagenesis of human immunodeficiency virus type 1. J. Mol. Biol. 2012, 419, 158-170.
16. Chen, R.; Quinones-Mateu, M.E.; Mansky, L.M. Drug resistance, virus fitness and HIV-1 mutagenesis. Curr. Pharm. Des. 2004, 10, 4065-4070.
17. Stumpp, S.N.; Heyn, B.; Brakmann, S. Activity-based selection of HIV-1 reverse transcriptase variants with decreased polymerization fidelity. Biol. Chem. 2010, 391, 665-674.
18. Wainberg, M.A. The impact of the M184V substitution on drug resistance and viral fitness. Expert Rev. Anti Infect. Ther. 2004, 2, 147-151.
19. Turner, D.; Brenner, B.G.; Routy, J.P.; Petrella, M.; Wainberg, M.A. Rationale for maintenance of the M184v resistance mutation in human immunodeficiency virus type 1 reverse transcriptase in treatment experienced patients. New Microbiol. 2004, 27, 31-39.
20. Hauser, A.; Mugenyi, K.; Kabasinguzi, R.; Kuecherer, C.; Harms, G.; Kunz, A. Emergence and persistence of minor drug-resistant HIV-1 variants in Ugandan women after nevirapine single-dose prophylaxis. PLoS One 2011, 6, doi:10.1371/journal.pone.0020357.
21. Petrella, M.; Wainberg, M.A. Might the M184V substitution in HIV-1 RT confer clinical benefit? AIDS Rev. 2002, 4, 224-232.
22. Mansky, L.M.; Cunningham, K.S. Virus mutators and antimutators: Roles in evolution, pathogenesis and emergence. Trends Genet. 2000, 16, 512-517.
23. Palmer, S.; Margot, N.; Gilbert, H.; Shaw, N.; Buckheit, R., Jr.; Miller, M. Tenofovir, adefovir, and zidovudine susceptibilities of primary human immunodeficiency virus type 1 isolates with non-B subtypes or nucleoside resistance. AIDS Res. Hum. Retrovir. 2001, 17, 1167-1173.
24. Miller, M.D.; Anton, K.E.; Mulato, A.S.; Lamy, P.D.; Cherrington, J.M. Human immunodeficiency virus type 1 expressing the lamivudine-associated M184V mutation in reverse transcriptase shows increased susceptibility to adefovir and decreased replication capability in vitro. J. Infect. Dis. 1999, 179, 92-100.
25. Lehmann, E.; D'Abrera, H. Nonparametrics: Statistical Methods based on Ranks; Mcgraw-Hill: New York, NY, USA, 1975; 240-247.
26. Efron, B. Large-Scale Inference: Empirical Bayes Methods for Estimation, Testing, and Prediction; Cambridge University Press: Cambridge, United Kingdom, 2010; Volume 1.
27. Kekitiinwa, A.; Asiimwe, A.R.; Kasirye, P.; Korutaro, V.; Kitaka, S.; Maganda, A.; Madalon, M.; Graziano, F.M. Prospective long-term outcomes of a cohort of ugandan children with laboratory monitoring during antiretroviral therapy. Pediatr. Infect. Dis. J. 2012, 31, e117-e125
28. Prosperi, M.C.; De Luca, A. Computational models for prediction of response to antiretroviral therapies. AIDS Rev. 2012, 14, 145-153.
29. Baxter, J.D.; Mayers, D.L.; Wentworth, D.N.; Neaton, J.D.; Hoover, M.L.; Winters, M.A.; Mannheimer, S.B.; Thompson, M.A.; Abrams, D.I.; Brizz, B.J., et al. A randomized study of antiretroviral management based on plasma genotypic antiretroviral resistance testing in patients failing therapy. CPCRA 046 Study Team for the Terry Beirn Community Programs for Clinical Research on AIDS. AIDS (London, England) 2000, 14, F83-F93.
30. Hill, A.L.; Rosenbloom, D.I.; Nowak, M.A. Evolutionary dynamics of HIV at multiple spatial and temporal scales. J. Mol. Med. (Berl. Ger.) 2012, 90, 543-561.
31. Fox, Z.; Dragsted, U.B.; Gerstoft, J.; Phillips, A.N.; Kjaer, J.; Mathiesen, L.; Youle, M.; Katlama, C.; Hill, A.; Bruun, J.N., et al. A randomized trial to evaluate continuation versus discontinuation of lamivudine in individuals failing a lamivudine-containing regimen: The COLATE trial. Antivir. Ther. 2006, 11, 761-770.
32. Quan, Y.; Brenner, B.G.; Oliveira, M.; Wainberg, M.A. Lamivudine can exert a modest antiviral effect against human immunodeficiency virus type 1 containing the M184V mutation. Antimicrob. Agents Chemother. 2003, 47, 747-754.
33. Rezende, L.F.; Prasad, V.R. Nucleoside-analog resistance mutations in HIV-1 reverse transcriptase and their influence on polymerase fidelity and viral mutation rates. Int. J. Biochem. Cell Biol. 2004, 36, 1716-1734.
34. Keulen, W.; van Wijk, A.; Schuurman, R.; Berkhout, B.; Boucher, C.A. Increased polymerase fidelity of lamivudine-resistant HIV-1 variants does not limit their evolutionary potential. AIDS (London, England) 1999, 13, 1343-1349.
35. Jonckheere, H.; Witvrouw, M.; de Clercq, E.; Anne, J. Lamivudine resistance of HIV type 1 does not delay development of resistance to nonnucleoside HIV type 1-specific reverse transcriptase inhibitors as compared with wild-type HIV type 1. AIDS Res. Hum. Retrovir. 1998, 14, 249-253.
36. Balzarini, J.; Pelemans, H.; Karlsson, A.; de Clerc, Q.E.; Kleim, J.P. Concomitant combination therapy for HIV infection preferable over sequential therapy with 3TC and non-nucleoside reverse transcriptase inhibitors. Proc. Natl. Acad. Sci. USA 1996, 93, 13152-13157.
37. Shafer, R.W.; Hertogs, K.; Zolopa, A.R.; Warford, A.; Bloor, S.; Betts, B.J.; Merigan, T.C.; Harrigan, R.; Larder, B.A. High degree of interlaboratory reproducibility of human immunodeficiency virus type 1 protease and reverse transcriptase sequencing of plasma samples from heavily treated patients. J. Clin. Microbiol. 2001, 39, 1522-1529.
38. Winters, M.A.; Holodniy, M.; Katzenstein, D.A.; Merigan, T.C. Quantitative RNA and DNA gene amplification can rapidly monitor HIV infection and antiviral activity in cell cultures. PCR Methods Appl. 1992, 1, 257-262.
39. Holodniy, M.; Katzenstein, D.A.; Sengupta, S.; Wang, A.M.; Casipit, C.; Schwartz, D.H.; Konrad, M.; Groves, E.; Merigan, T.C. Detection and quantification of human immunodeficiency virus RNA in patient serum by use of the polymerase chain reaction. J. Infect. Dis. 1991, 163, 862-866.
40. Tang, M.W.; Shafer, R.W. HIV-1 Antiretroviral resistance: Scientific principles and clinical applications. Drugs 2012, 72, e1-e25.
41. Melikian, G.L.; Rhee, S.Y.; Taylor, J.; Fessel, W.J.; Kaufman, D.; Towner, W.; Troia-Cancio, P.V.; Zolopa, A.; Robbins, G.K.; Kagan, R.; Israelski, D.; Shafer, R.W. Standardized comparison of the relative impacts of HIV-1 reverse transcriptase (RT) mutations on nucleoside RT inhibitor susceptibility. Antimicrob. Agents Chemother. 2012, 56, 2305-2313.
42. Palmer, S.; Shafer, R.W.; Merigan, T.C. Highly drug-resistant HIV-1 clinical isolates are cross-resistant to many antiretroviral compounds in current clinical development. AIDS 1999, 13, 661-667.
43. Paxton, W.B.; Coombs, R.W.; McElrath, M.J.; Keefer, M.C.; Hughes, J.; Sinangil, F.; Chernoff, D.; Demeter, L.; Williams, B.; Corey, L. Longitudinal analysis of quantitative virologic measures in human immunodeficiency virus-infected subjects with > or = 400 CD4 lymphocytes: Implications for applying measurements to individual patients. National Institute of Allergy and Infectious Diseases AIDS Vaccine Evaluation Group. J. Infect. Dis. 1997, 175, 247-254.
44. Rizzo, R.C.; Tirado-Rives, J.; Jorgensen, W.L. Estimation of binding affinities for HEPT and nevirapine analogues with HIV-1 reverse transcriptase via Monte Carlo simulations. J. Med. Chem. 2001, 44, 145-154.
45. Delaugerre, C.; Gallien, S.; Flandre, P.; Mathez, D.; Amarsy, R.; Ferret, S.; Timsit, J.; Molina, J.M.; de Truchis, P. Impact of low-level-viremia on HIV-1 drug-resistance evolution among antiretroviral treated-patients. PLoS One 2012, 7, doi:10.1371/journal.pone.0036673.
46. Messiaen, P.; Verhofstede, C.; Vandenbroucke, I.; Dinakis, S.; Van Eygen, V.; Thys, K.; Winters, B.; Aerssens, J.; Vogelaers, D.; Stuyver, L.J.; Vandekerckhove, L. Ultra-deep sequencing of HIV-1 reverse transcriptase before start of an NNRTI-based regimen in treatment-naive patients. Virology 2012, 426, 7-11.
47. Murry, J.P.; Higgins, J.; Matthews, T.B.; Huang, V.Y.; van Rompay, K.K.; Pedersen, N.C.; North, T.W. Reversion of the M184V mutation in simian immunodeficiency virus reverse transcriptase is selected by tenofovir, even in the presence of lamivudine. J. Virol. 2003, 77, 1120-1130.
48. Diallo, K.; Oliveira, M.; Moisi, D.; Brenner, B.; Wainberg, M.A.; Gotte, M. Pressure of zidovudine accelerates the reversion of lamivudine resistance-conferring M184V mutation in the reverse transcriptase of human immunodeficiency virus type 1. Antimicrob. Agents Chemother. 2002, 46, 2254-2256.
49. Mansky, L.M.; Bernard, L.C. 3'-Azido-3'-deoxythymidine (AZT) and AZT-resistant reverse transcriptase can increase the in vivo mutation rate of human immunodeficiency virus type 1. J. Virol. 2000, 74, 9532-9539.
50. Chen, R.; Yokoyama, M.; Sato, H.; Reilly, C.; Mansky, L.M. Human immunodeficiency virus mutagenesis during antiviral therapy: Impact of drug-resistant reverse transcriptase and nucleoside and nonnucleoside reverse transcriptase inhibitors on human immunodeficiency virus type 1 mutation frequencies. J. Virol. 2005, 79, 12045-12057.
51. Opravil, M.; Klimkait, T.; Louvel, S.; Wolf, E.; Battegay, M.; Fux, C.A.; Bernasconi, E.; Vogel, M.; Speck, R.; Weber, R. Prior therapy influences the efficacy of lamivudine monotherapy in patients with lamivudine-resistant HIV-1 infection. J. Acquir. Immune Defic. Syndr. (1999) 2010, 54, 51-58.
52. Deeks, S.G.; Wrin, T.; Liegler, T.; Hoh, R.; Hayden, M.; Barbour, J.D.; Hellmann, N.S.; Petropoulos, C.J.; McCune, J.M.; Hellerstein, M.K.; Grant, R.M. Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia. N. Engl. J. Med. 2001, 344, 472-480.
53. Metzner, K.J.; Leemann, C.; di Giallonardo, F.; Grube, C.; Scherrer, A.U.; Braun, D.; Kuster, H.; Weber, R.; Guenthard, H.F. Reappearance of minority K103N HIV-1 variants after interruption of ART initiated during primary HIV-1 infection. PLoS One 2011, 6, doi:10.1371/journal.pone.0021734.
54. Paquet, A.C.; Baxter, J.; Weidler, J.; Lie, Y.; Lawrence, J.; Kim, R.; Bates, M.; Coakley, E.; Chappey, C. Differences in reversion of resistance mutations to wild-type under structured treatment interruption and related increase in replication capacity. PLoS One 2011, 6, doi:10.1371/journal.pone.0014638.
55. Campbell, T.B.; Shulman, N.S.; Johnson, S.C.; Zolopa, A.R.; Young, R.K.; Bushman, L.; Fletcher, C.V.; Lanier, E.R.; Merigan, T.C.; Kuritzkes, D.R. Antiviral activity of lamivudine in salvage therapy for multidrug-resistant HIV-1 infection. Clin. Infect. Dis. 2005, 41, 236-242.
56. Lecossier, D.; Shulman, N.S.; Morand-Joubert, L.; Shafer, R.W.; Joly, V.; Zolopa, A.R.; Clavel, F.; Hance, A.J. Detection of minority populations of HIV-1 expressing the K103N resistance mutation in patients failing nevirapine. J. Acquir. Immune Defic. Syndr. (1999) 2005, 38, 37-42.
57. Shulman, N.S.; Zolopa, A.R.; Passaro, D.J.; Murlidharan, U.; Israelski, D.M.; Brosgart, C.L.; Miller, M.D.; Van Doren, S.; Shafer, R.W.; Katzenstein, D.A. Efavirenz- and adefovir dipivoxilbased salvage therapy in highly treatment-experienced patients: Clinical and genotypic predictors of virologic response. J. Acquir. Immune Defic. Syndr. (1999) 2000, 23, 221-226.
58. Winters, M.A.; Schapiro, J.M.; Lawrence, J.; Merigan, T.C. 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. 1998, 72, 5303-5306.
59. Nijhuis, M.; Boucher, C.A.; Schuurman, R. Sensitive procedure for the amplification of HIV-1 RNA using a combined reverse-transcription and amplification reaction. Biotechniques 1995, 19, 178-180, 182.
60. Schapiro, J.M.; Winters, M.A.; Stewart, F.; Efron, B.; Norris, J.; Kozal, M.J.; Merigan, T.C. The effect of high-dose saquinavir on viral load and CD4+ T-cell counts in HIV-infected patients. Ann. Internal Med. 1996, 124, 1039-1050.
61. Winters, M.A.; Coolley, K.L.; Girard, Y.A.; Levee, D.J.; Hamdan, H.; Shafer, R.W.; Katzenstein, D.A.; Merigan, T.C. A 6-basepair insert in the reverse transcriptase gene of human immunodeficiency virus type 1 confers resistance to multiple nucleoside inhibitors. J. Clin. Invest. 1998, 102, 1769-1775.
62. Efron, B.; Tibshirani, R.J. An Introduction to the Bootstrap; Chapman & Hall/CRC: New York, NY, USA, 1993; Volume 57.
63. Rice, J.A. Mathematical Statistics and Data Analysis, 3rd ed.; Thompson Higher Education: Belmont, CA, USA, 2006.
64. Raikov, D. On the decomposition of Gauss and Poisson laws (in Russian). Izv. Ross. Akad. Nauk. Ser. Mat. 1938, 2, 91-124.
65. Fisher, R. Statistical Methods for Research Workers; Oliver and Boyd: Edinburgh, Scotland, UK, 1963; 19th Edition.