Infectivity and replication capacity of drug-resistant human immunodeficiency virus type 1 variants isolated during primary infection

Journal of Virology

Volumn 77, Issue 14, 2003, Pages 7736-7745

  Simon, Viviana ^a,d   Padte, Neal ^a   Murray, Deya ^a   Vanderhoeven, Jeroen ^a   Wrin, Terri ^b   Parkin, Neil ^b   Di Mascio, Michele ^c,e   Markowitz, Martin ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MONOGRAM BIOSCIENCES   (United States)

^c LOS ALAMOS NATIONAL LABORATORY   (United States)

^d AARON DIAMOND AIDS RESEARCH CENTER   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; GAG PROTEIN; PROTEINASE; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR; ZIDOVUDINE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL LINE; CHIMERA; CLINICAL ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMARY INFECTION; PRIORITY JOURNAL; T LYMPHOCYTE; VIROGENESIS; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS MUTATION; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS TRANSMISSION;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; DRUG RESISTANCE, MULTIPLE, VIRAL; DRUG RESISTANCE, VIRAL; FEMALE; GENE PRODUCTS, GAG; GENES, GAG; HIV INFECTIONS; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; HUMANS; MALE; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE INHIBITORS; SEQUENCE ANALYSIS, DNA; VIRUS REPLICATION;

EID: 0038082378     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.14.7736-7745.2003     Document Type: Article

References (48)

1. Archer, R. H., C. Dykes, P. Gerondelis, A. Lloyd, P. Fay, R. C. Reichman, R. A. Bambara, and L. M. Demeter. 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. 74:8390-8401.
2. Back, N. K., and B. Berkhout. 1997. Limiting deoxynucleoside triphosphate concentrations emphasize the processivity defect of lamivudine-resistant variants of human immunodeficiency virus type 1 reverse transcriptase. Antimicrob. Agents Chemother. 41:2484-2491.
3. Bleiber, G., M. Munoz, A. Ciuffi, P. Meylan, and A. Telenti. 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. 75:3291-3300.
4. Blower, S. M., A. N. Aschenbach, H. B. Gershengorn, and J. O. Kahn. 2001. Predicting the unpredictable: transmission of drug-resistant HIV. Nat. Med. 7:1016-1020.
5. Boden, D., A. Hurley, L. Zhang, Y. Cao, Y. Guo, E. Jones, J. Tsay, J. Ip, C. Farthing, K. Limoli, N. Parkin, and M. Markowitz. 1999. HIV-1 drug resistance in newly infected individuals. JAMA 282:1135-1141.
6. Borman, A. M., S. Paulous, and F. Clavel. 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. 77:419-426.
7. Brenner, B. G., J. P. Routy, M. Petrella, D. Moisi, M. Oliveira, M. Detorio, B. Spira, V. Essabag, B. Conway, R. Lalonde, R. P. Sekaly, and M. A. Wainberg. 2002. Persistence and fitness of multidrug-resistant human immunodeficiency virus type 1 acquired in primary infection. J. Virol. 76:1753-1761.
8. Caliendo, A. M., A. Savara, D. An, K. DeVore, J. C. Kaplan, and R. T. D'Aquila. 1996. Effects of zidovudine-selected human immunodeficiency virus type 1 reverse transcriptase amino acid substitutions on processive DNA synthesis and viral replication. J. Virol. 70:2146-2153.
9. 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.
10. Dauber, D. S., R. Ziermann, N. Parkin, D. J. Maly, S. Mahrus, J. L. Harris, J. A. Ellman, C. Petropoulos, and C. S. Craik. 2002. Altered substrate specificity of drug-resistant human immunodeficiency virus type 1 protease. J. Virol. 76:1359-1368.
11. Deeks, S. G., T. Wrin, T. Liegler, R. Hoh, M. Hayden, J. D. Barbour, N. S. Hellmann, C. J. Petropoulos, J. M. McCune, M. K. Hellerstein, and R. M. Grant. 2001. Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia. N. Engl. J. Med. 344:472-480.
12. de Ronde, A., M. van Dooren, L. van Der Hoek, D. Bouwhuis, E. de Rooij, B. van Gemen, R. de Boer, and J. Goudsmit. 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. 75:595-602.
13. Dykes, C., K. Fox, A. Lloyd, M. Chiulli, E. Morse, and L. M. Demeter. 2001. Impact of clinical reverse transcriptase sequences on the replication capacity of HIV-1 drug-resistant mutants. Virology 285:193-203.
14. Ferbas, J., E. S. Daar, K. Grovit-Ferbas, W. J. Lech, R. Detels, J. V. Giorgi, and A. H. Kaplan. 1996. Rapid evolution of human immunodeficiency virus strains with increased replicative capacity during the seronegative window of primary infection. J. Virol. 70:7285-7289.
15. Garcia-Lerma, J. G., S. Nidtha, K. Blumoff, H. Weinstock, and W. Heneine. 2001. Increased ability for selection of zidovudine resistance in a distinct class of wild-type HIV-1 from drug-naive persons. Proc. Natl. Acad. Sci. USA 98:13907-13912.
16. Gatanaga, H., Y. Suzuki, H. Tsang, K. Yoshimura, M. F. Kavlick, K. Nagashima, R. J. Gorelick, S. Mardy, C. Tang, M. F. Summers, and H. Mitsuya. 2002. Amino acid substitutions in Gag protein at non-cleavage sites are indispensable for the development of a high multitude of HIV-1 resistance against protease inhibitors. J. Biol. Chem. 277:5952-5961.
17. Gotte, M., and M. A. Wainberg. 2000. Biochemical mechanisms involved in overcoming HIV resistance to nucleoside inhibitors of reverse transcriptase. Drug Resist. Update 3:30-38.
18. Grant, R. M., F. M. Hecht, M. Warmerdam, L. Liu, T. Liegler, C. J. Petropoulos, N. S. Hellmann, M. Chesney, M. P. Busch, and J. O. Kahn. 2002. Time trends in primary HIV-1 drug resistance among recently infected persons. JAMA 288:181-188.
19. Gray, R. H., M. J. Wawer, R. Brookmeyer, N. K. Sewankambo, D. Serwadda, F. Wabwire-Mangen, T. Lutalo, X. Li, T. vanCott, and T. C. Quinn. 2001. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 357:1149-1153.
20. Hance, A. J., V. Lemiale, J. Izopet, D. Lecossier, V. Joly, P. Massip, F. Mammano, D. Descamps, F. Brun-Vezinet, and F. Clavel. 2001. Changes in human immunodeficiency virus type 1 populations after treatment interruption in patients failing antiretroviral therapy. J. Virol. 75:6410-6417.
21. Izopet, J., P. Massip, C. Souyris, K. Sandres, B. Puissant, M. Obadia, C. Pasquier, E. Bonnet, B. Marchou, and J. Puel. 2000. Shift in HIV resistance genotype after treatment interruption and short-term antiviral effect following a new salvage regimen. AIDS 14:2247-2255.
22. Kaufmann, D., M. Munoz, G. Bleiber, S. Fleury, B. Lotti, R. Martinez, W. Pichler, P. Meylan, and A. Telenti. 2000. Virological and immunological characteristics of HIV treatment failure. AIDS 14:1767-1774.
23. Lawson, V. A., R. Oelrichs, C. Guillon, A. A. Imrie, D. A. Cooper, N. J. Deacon, and D. A. McPhee. 2002. Adaptive changes after human immunodeficiency virus type 1 transmission. AIDS Res. Hum. Retroviruses 18:545-556.
24. Learn, G. H., D. Muthui, S. J. Brodie, T. Zhu, K. Diem, J. I. Mullins, and L. Corey. 1959. 2002. Virus population homogenization following acute human immunodeficiency virus type 1 infection. J. Virol. 76:11953-11959.
25. Little, S. J., E. S. Daar, R. T. D'Aquila, P. H. Keiser, E. Connick, J. M. Whitcomb, N. S. Hellmann, C. J. Petropoulos, L. Sutton, J. A. Pitt, E. S. Rosenberg, R. A. Koup, B. D. Walker, and D. D. Richman. 1999. Reduced antiretroviral drug susceptibility among patients with primary HIV infection. JAMA 282:1142-1149.
26. Little, S. J., S. Holte, J. P. Routy, E. S. Daar, M. Markowitz, A. C. Collier, R. A. Koup, J. W. Mellors, E. Connick, B. Conway, M. Kilby, L. Wang, J. M. Whitcomb, N. S. Hellmann, and D. D. Richman. 2002. Antiretroviral-drug resistance among patients recently infected with HIV. N. Engl. J. Med. 347:385-394.
27. Long, E. M., H. L. Martin, Jr., J. K. Kreiss, S. M. Rainwater, L. Lavreys, D. J. Jackson, J. Rakwar, K. Mandaliya, and J. Overbaugh. 2000. Gender differences in HIV-1 diversity at time of infection. Nat. Med. 6:71-75.
28. Lukashov, V. V., and J. Goudsmit. 1997. Founder virus population related to route of virus transmission: a determinant of intrahost human immunodeficiency virus type 1 evolution? J. Virol. 71:2023-2030.
29. Mammano, F., C. Petit, and F. Clavel. 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. 72:7632-7637.
30. Mammano, F., V. Trouplin, V. Zennou, and F. Clavel. 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. 74:8524-8531.
31. Miller, C. J., M. Marthas, J. Greenier, D. Lu, P. J. Dailey, and Y. Lu. 1998. In vivo replication capacity rather than in vitro macrophage tropism predicts efficiency of vaginal transmission of simian immunodeficiency virus or simian/human immunodeficiency virus in rhesus macaques. J. Virol. 72:3248-3258.
32. Morner, A., A. Bjorndal, J. Albert, V. N. Kewalramani, D. R. Littman, R. Inoue, R. Thorstensson, E. M. Fenyo, and E. Bjorling. 1999. Primary human immunodeficiency virus type 2 (HIV-2) isolates, like HIV-1 isolates, frequently use CCR5 but show promiscuity in coreceptor usage. J. Virol. 73:2343-2349.
33. Murray, J. 1989. Continuous population models for single species. Mathematical biology. Springer Verlag, Berlin, Germany.
34. Olsen, D. B., M. W. Stahlhut, C. A. Rutkowski, H. B. Schock, A. L. vanOlden, and L. C. Kuo. 1999. Non-active site changes elicit broad-based cross-resistance of the HIV-1 protease to inhibitors. J. Biol. Chem. 274:23699-23701.
35. Peters, S., M. Munoz, S. Yerly, V. Sanchez-Merino, C. Lopez-Galindez, L. Perrin, B. Larder, D. Cmarko, S. Fakan, P. Meylan, and A. Telenti. 2001. Resistance to nucleoside analog reverse transcriptase inhibitors mediated by human immunodeficiency virus type 1 p6 protein. J. Virol. 75:9644-9653.
36. 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.
37. Pettit, S. C., G. J. Henderson, C. A. Schiffer, and R. Swanstrom. 2002. Replacement of the P1 amino acid of human immunodeficiency virus type 1 Gag processing sites can inhibit or enhance the rate of cleavage by the viral protease. J. Virol. 76:10226-10233.
38. Precious, H. M., H. F. Gunthard, J. K. Wong, R. T. D'Aquila, V. A. Johnson, D. R. Kuritzkes, D. D. Richman, and A. J. Leigh Brown. 2000. Multiple sites in HIV-1 reverse transcriptase associated with virological response to combination therapy. AIDS 14:31-36.
39. Resch, W., R. Ziermann, N. Parkin, A. Gamarnik, and R. Swanstrom. 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. 76:8659-8666.
40. Robinson, L. H., R. E. Myers, B. W. Snowden, M. Tisdale, and E. D. Blair. 2000. HIV type 1 protease cleavage site mutations and viral fitness: implications for drug susceptibility phenotyping assays. AIDS Res. Hum. Retroviruses 16:1149-1156.
41. Salomon, H., M. A. Wainberg, B. Brenner, Y. Quan, D. Rouleau, P. Cote, R. LeBlanc, E. Lefebvre, B. Spira, C. Tsoukas, R. P. Sekaly, B. Conway, D. Mayers, J. P. Routy, et al. 2000. Prevalence of HIV-1 resistant to antiretroviral drugs in 81 individuals newly infected by sexual contact or injecting drug use. AIDS 14:F17-F23.
42. Simon, V., J. Vanderhoeven, A. Hurley, B. Ramratnam, M. Louie, K. Dawson, N. Parkin, D. Boden, and M. Markowitz. 2002. Evolving patterns of HIV-1 resistance to antiretroviral agents in newly infected individuals. AIDS 16:1511-1519.
43. Stoddart, C. A., T. J. Liegler, F. Mammano, V. D. Linquist-Stepps, M. S. Hayden, S. G. Deeks, R. M. Grant, F. Clavel, and J. M. McCune. 2001. Impaired replication of protease inhibitor-resistant HIV-1 in human thymus. Nat. Med. 7:712-718.
44. Vodros, D., C. Tscherning-Casper, L. Navea, D. Schols, E. De Clercq, and E. M. Fenyo. 2001. Quantitative evaluation of HIV-1 coreceptor use in the GHOST3 cell assay. Virology 291:1-11.
45. Wrin, T., A. Gamarnik, N. Whitehurst, J. Beauchaine, J. M. Whitcomb, N. S. Hellmann, and C. J. Petropoulos. 2001. Natural variation of replication capacity measurements in drug-naïve/susceptible HIV-1. Antiviral Ther. 6:20.
46. Yerly, S., L. Kaiser, E. Race, J. P. Bru, F. Clavel, and L. Perrin. 1999. Transmission of antiretroviral-drug-resistant HIV-1 variants. Lancet 354:729-733.
47. Zhang, Y. J., T. Hatziioannou, T. Zang, D. Braaten, J. Luban, S. P. Goff, and P. D. Bieniasz. 2002. Envelope-dependent, cyclophilin-independent effects of glycosaminoglycans on human immunodeficiency virus type 1 attachment and infection. J. Virol. 76:6332-6343.
48. Zhang, Y. M., H. Imamichi, T. Imamichi, H. C. Lane, J. Falloon, M. B. Vasudevachari, and N. P. Salzman. 1997. Drug resistance during indinavir therapy is caused by mutations in the protease gene and in its Gag substrate cleavage sites. J. Virol. 71:6662-6670.