Human immunodeficiency virus type 1 protease inhibitor drug-resistant mutants give discordant results when compared in single-cycle and multiple-cycle fitness assays

Journal of Clinical Microbiology

Volumn 48, Issue 11, 2010, Pages 4035-4043

  Dykes, Carrie ^a   Wu, Hulin ^a   Sims, Matthew ^a,b   Holden Wiltse, Jeanne ^a   Demeter, Lisa M ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b WILLIAM BEAUMONT HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRAL RESISTANCE; ARTICLE; ASSAY; CELL CULTURE; CLINICAL ASSESSMENT; FLOW CYTOMETRY; GENOTYPE; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERMETHOD COMPARISON; MULTIPLE CYCLE ASSAY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; REVERSE TRANSCRIPTION; SINGLE CYCLE ASSAY; VIRUS DNA CELL DNA INTERACTION; VIRUS ENTRY; VIRUS REPLICATION;

DRUG RESISTANCE, VIRAL; HIV INFECTIONS; HIV PROTEASE; HIV PROTEASE INHIBITORS; HIV-1; HUMANS; VIROLOGY; VIRULENCE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 78049514116     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.00605-10     Document Type: Article

References (51)

1. Ahlsen, G., J. Hulten, C. F. Shuman, A. Poliakov, M. T. Lindgren, M. Alterman, B. Samuelsson, A. Hallberg, and U. H. Danielson. 2002. Resistance profiles of cyclic and linear inhibitors of HIV-1 protease. Antivir. Chem. Chemother. 13:27-37.
2. Aiken, C. 1997. Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J. Virol. 71:5871-5877. (Pubitemid 27304923)
3. Akkina, R. K., R. M. Walton, M. L. Chen, Q. X. Li, V. Planelles, and I. S. Chen. 1996. High-efficiency gene transfer into CD34+ cells with a human immunodeficiency virus type 1-based retroviral vector pseudotyped with vesicular stomatitis virus envelope glycoprotein G. J. Virol. 70:2581-2585.
4. 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.
5. Arien, K. K., A. Abraha, M. E. Quinones-Mateu, L. Kestens, G. Vanham, and E. J. Arts. 2005. The replicative fitness of primary human immunodeficiency virus type 1 (HIV-1) group M, HIV-1 group O, and HIV-2 isolates. J. Virol. 79:8979-8990.
6. Barbour, J. D., F. M. Hecht, T. Wrin, M. R. Segal, C. A. Ramstead, T. J. Liegler, M. P. Busch, C. J. Petropoulos, N. S. Hellmann, J. O. Kahn, and R. M. Grant. 2004. Higher CD4+ 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.
7. Barbour, J. D., T. Wrin, R. M. Grant, J. N. Martin, M. R. Segal, C. J. Petropoulos, and S. G. Deeks. 2002. Evolution of phenotypic drug susceptibility and viral replication capacity during long-term virologic failure of protease inhibitor therapy in human immunodeficiency virus-infected adults. J. Virol. 76:11104-11112.
8. Campbell, T. B., K. Schneider, T. Wrin, C. J. Petropoulos, and E. Connick. 2003. Relationship between in vitro human immunodeficiency virus type 1 replication rate and virus load in plasma. J. Virol. 77:12105-12112.
9. Cao, J., J. McNevin, M. McSweyn, Y. Liu, J. I. Mullins, and M. J. McElrath. 2008. Novel cytotoxic T-lymphocyte escape mutation by a three-amino-acid insertion in the human immunodeficiency virus type 1 p6Pol and p6Gag late domain associated with drug resistance. J. Virol. 82:495-502.
10. Clemente, J. C., R. Hemrajani, L. E. Blum, M. M. Goodenow, and B. M. Dunn. 2003. Secondary mutations M36I and A71V in the human immunodeficiency virus type 1 protease can provide an advantage for the emergence of the primary mutation D30N. Biochemistry 42:15029-15035.
11. Coffin, J. M. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
12. Collins, J. A., M. G. Thompson, E. Paintsil, M. Ricketts, J. Gedzior, and L. Alexander. 2004. Competitive fitness of nevirapine-resistant human immunodeficiency virus type 1 mutants. J. Virol. 78:603-611.
13. Cong, M. E., W. Heneine, and J. G. Garcia-Lerma. 2007. The fitness cost of mutations associated with human immunodeficiency virus type 1 drug resistance is modulated by mutational interactions. J. Virol. 81:3037-3041.
14. De Luca, A., J. Weidler, S. Di Giambenedetto, E. Coakley, A. Cingolani, M. Bates, Y. Lie, R. Pesano, R. Cauda, and J. Schapiro. 2007. Association of HIV-1 replication capacity with treatment outcomes in patients with virologic treatment failure. J. Acquir. Immune Defic. Syndr. 45:411-417.
15. Deval, J., K. L. White, M. D. Miller, N. T. Parkin, J. Courcambeck, P. Halfon, B. Selmi, J. Boretto, and B. Canard. 2004. Mechanistic basis for reduced viral and enzymatic fitness of HIV-1 reverse transcriptase containing both K65R and M184V mutations. J. Biol. Chem. 279:509-516.
16. Domingo, E., E. Martinez-Salas, F. Sobrino, J. C. de la Torre, A. Portela, J. Ortin, C. Lopez-Galindez, P. Perez-Brena, N. Villanueva, R. Najera, et al. 1985. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance - a review. Gene 40:1-8.
17. Domingo, E., L. Menendez-Arias, and J. J. Holland. 1997. RNA virus fitness. Rev. Med. Virol. 7:87-96.
18. Dykes, C., M. Balakrishnan, V. Planelles, Y. Zhu, R. A. Bambara, and L. M. Demeter. 2004. Identification of a preferred region for recombination and mutation in HIV-1 gag. Virology 326:262-279.
19. Dykes, C., and L. M. Demeter. 2007. Clinical significance of human immunodeficiency virus type 1 replication fitness. Clin. Microbiol. Rev. 20:550-578.
20. 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.
21. Dykes, C., J. Wang, X. Jin, V. Planelles, D. S. An, A. Tallo, Y. Huang, H. Wu, and L. M. Demeter. 2006. Evaluation of a multiple-cycle, recombinant virus, growth competition assay that uses flow cytometry to measure replication efficiency of human immunodeficiency virus type 1 in cell culture. J. Clin. Microbiol. 44:1930-1943.
22. Freed, E. O. 2003. The HIV-TSG101 interface: recent advances in a budding field. Trends Microbiol. 11:56-59. (Pubitemid 36207497)
23. Garcia-Lerma, J. G., P. J. Gerrish, A. C. Wright, S. H. Qari, and W. Heneine. 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. 74:9339-9346.
24. Gerondelis, P., R. H. Archer, C. Palaniappan, R. C. Reichman, P. J. Fay, R. A. Bambara, and L. M. Demeter. 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. 73:5803-5813.
25. Gottlinger, H. G., T. Dorfman, J. G. Sodroski, and W. A. Haseltine. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. U. S. A. 88:3195-3199.
26. Harada, S., Y. Koyanagi, and N. Yamamoto. 1985. Infection of HTLV-III/LAV in HTLV-I-carrying cells MT-2 and MT-4 and application in a plaque assay. Science 229:563-566.
27. Harrigan, P. R., S. Bloor, and B. A. Larder. 1998. Relative replicative fitness of zidovudine-resistant human immunodeficiency virus type 1 isolates in vitro. J. Virol. 72:3773-3778.
28. Koval, C. E., C. Dykes, J. Wang, and L. M. Demeter. 2006. Relative replication fitness of efavirenz-resistant mutants of HIV-1: correlation with frequency during clinical therapy and evidence of compensation for the reduced fitness of K103N + L100I by the nucleoside resistance mutation L74V. Virology 353:184-192.
29. Landau, N. R., K. A. Page, and D. R. Littman. 1991. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65:162-169.
30. Larder, B. A., G. Darby, and D. D. Richman. 1989. HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy. Science 243:1731-1734.
31. Lu, J., and D. R. Kuritzkes. 2001. A novel recombinant marker virus assay for comparing the relative fitness of HIV-1 reverse transcriptase variants. J. Acquir. Immune Defic. Syndr. 27:7-13.
32. Lu, J., P. Sista, F. Giguel, M. Greenberg, and D. R. Kuritzkes. 2004. Relative replicative fitness of human immunodeficiency virus type 1 mutants resistant to enfuvirtide (T-20). J. Virol. 78:4628-4637.
33. Lusso, P., F. Cocchi, C. Balotta, P. D. Markham, A. Louie, P. Farci, R. Pal, R. C. Gallo, and M. S. Reitz, Jr. 1995. Growth of macrophage-tropic and primary human immunodeficiency virus type 1 (HIV-1) isolates in a unique CD4+ T-cell clone (PM1): failure to downregulate CD4 and to interfere with cell-line-tropic HIV-1. J. Virol. 69:3712-3720.
34. Mahalingam, B., J. M. Louis, C. C. Reed, J. M. Adomat, J. Krouse, Y. F. Wang, R. W. Harrison, and I. T. Weber. 1999. Structural and kinetic analysis of drug resistant mutants of HIV-1 protease. Eur. J. Biochem. 263:238-245.
35. 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.
36. Martinez-Picado, J., A. V. Savara, L. Sutton, and R. T. D'Aquila. 1999. Replicative fitness of protease inhibitor-resistant mutants of human immunodeficiency virus type 1. J. Virol. 73:3744-3752.
37. Miura, T., M. A. Brockman, Z. L. Brumme, C. J. Brumme, F. Pereyra, A. Trocha, B. L. Block, A. Schneidewind, T. M. Allen, D. Heckerman, and B. D. Walker. 2009. HLA-associated alterations in replication capacity of chimeric NL4-3 viruses carrying gag-protease from elite controllers of human immunodeficiency virus type 1. J. Virol. 83:140-149.
38. Miura, T., Z. L. Brumme, M. A. Brockman, P. Rosato, J. Sela, C. J. Brumme, F. Pereyra, D. E. Kaufmann, A. Trocha, B. L. Block, E. S. Daar, E. Connick, H. Jessen, A. D. Kelleher, E. Rosenberg, M. Markowitz, K. Schafer, F. Vaida, A. Iwamoto, S. Little, and B. D. Walker. 2010. Impaired replication capacity of acute/early viruses in persons who become HIV controllers. J. Virol. 84:7581-7591.
39. Perez-Bercoff, D., S. Wurtzer, S. Compain, H. Benech, and F. Clavel. 2007. Human immunodeficiency virus type 1: resistance to nucleoside analogues and replicative capacity in primary human macrophages. J. Virol. 81:4540-4550.
40. Perrin, V., and F. Mammano. 2003. Parameters driving the selection of nelfinavir-resistant human immunodeficiency virus type 1 variants. J. Virol. 77:10172-10175.
41. 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.
42. 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.
43. Poeschla, E., P. Corbeau, and F. Wong-Staal. 1996. Development of HIV vectors for anti-HIV gene therapy. Proc. Natl. Acad. Sci. U. S. A. 93:11395-11399.
44. Prado, J. G., T. Wrin, J. Beauchaine, L. Ruiz, C. J. Petropoulos, S. D. Frost, B. Clotet, R. T. D'Aquila, and J. Martinez-Picado. 2002. Amprenavir-resistant HIV-1 exhibits lopinavir cross-resistance and reduced replication capacity. AIDS 16:1009-1017.
45. Reiser, J., G. Harmison, S. Kluepfel-Stahl, R. O. Brady, S. Karlsson, and M. Schubert. 1996. Transduction of nondividing cells using pseudotyped defective high-titer HIV type 1 particles. Proc. Natl. Acad. Sci. U. S. A. 93:15266-15271.
46. Rose, R. E., Y. F. Gong, J. A. Greytok, C. M. Bechtold, B. J. Terry, B. S. Robinson, M. Alam, R. J. Colonno, and P. F. Lin. 1996. Human immunodeficiency virus type 1 viral background plays a major role in development of resistance to protease inhibitors. Proc. Natl. Acad. Sci. U. S. A. 93:1648-1653.
47. Velazquez-Campoy, A., S. Vega, and E. Freire. 2002. Amplification of the effects of drug resistance mutations by background polymorphisms in HIV-1 protease from African subtypes. Biochemistry 41:8613-8619.
48. Wang, J., C. Dykes, R. A. Domaoal, C. E. Koval, R. A. Bambara, and L. M. Demeter. 2006. The HIV-1 reverse transcriptase mutants G190S and G190A, which confer resistance to non-nucleoside reverse transcriptase inhibitors, demonstrate reductions in RNase H activity and DNA synthesis from tRNA(Lys, 3) that correlate with reductions in replication efficiency. Virology 348:462-474.
49. Wu, H., Y. Huang, C. Dykes, D. Liu, J. Ma, A. S. Perelson, and L. M. Demeter. 2006. Modeling and estimation of replication fitness of human immunodeficiency virus type 1 in vitro experiments by using a growth competition assay. J. Virol. 80:2380-2389.
50. Yee, J. K., A. Miyanohara, P. LaPorte, K. Bouic, J. C. Burns, and T. Friedmann. 1994. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 91:9564-9568.
51. Zhang, H., Y. Zhou, C. Alcock, T. Kiefer, D. Monie, J. Siliciano, Q. Li, P. Pham, J. Cofrancesco, D. Persaud, and R. F. Siliciano. 2004. Novel single-cell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J. Virol. 78:1718-1729.