Functional correlation between a novel amino acid insertion at codon 19 in the protease of human immunodeficiency virus type 1 and polymorphism in the p1/p6 Gag cleavage site in drug resistance and replication fitness

Journal of Virology

Volumn 80, Issue 12, 2006, Pages 6136-6145

  Brann, Terrence W ^a   Dewar, Robin L ^a   Jiang, Min Kan ^a   Shah, Akram ^a   Nagashima, Kunio ^a   Metcalf, Julia A ^b   Falloon, Judith ^b   Lane, H Clifford ^b   Imamichi, Tomozumi ^a  

^a SAIC FREDERICK INC   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; AMPRENAVIR; ATAZANAVIR; GAG PROTEIN; INDINAVIR; LEUCINE; LOPINAVIR; NELFINAVIR; PROLINE; PROTEINASE; PROTEINASE INHIBITOR; RITONAVIR; SAQUINAVIR; ZIDOVUDINE;

AMINO ACID METABOLISM; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CODON; CORRELATION ANALYSIS; GENE INSERTION; GENE MUTATION; GENETIC POLYMORPHISM; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IC 50; MORPHOLOGICAL TRAIT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SITE DIRECTED MUTAGENESIS; VIRUS LOAD; VIRUS MUTANT; VIRUS REPLICATION;

CODON; DRUG RESISTANCE, VIRAL; HIV CORE PROTEIN P24; HIV PROTEASE; HIV-1; HUMANS; MUTATION; POLYMORPHISM, GENETIC; PROTEASE INHIBITORS; TREATMENT FAILURE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33744912483     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02212-05     Document Type: Article

References (45)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retroviras in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Bally, F., R. Martinez, S. Peters, P. Sudre, and A. Telenti. 2000. Polymorphism of HIV type 1 gag p7/p1 and p1/p6 cleavage sites: clinical significance and implications for resistance to protease inhibitors. AIDS Res. Hum. Retrovir. 16:1209-1213.
3. Carrillo, A., K. D. Stewart, H. L. Sham, D. W. Norbeck, W. E. Kohlbrenner, J. M. Leonard, D. J. Kempf, and A. Molla. 1998. In vitro selection and characterization of human immunodeficiency virus type 1 variants with increased resistance to ABT-378, a novel protease inhibitor. J. Virol. 72:7532-7541.
4. Clavel, F., E. Race, and F. Mammano. 2000. HIV drug resistance and viral fitness. Adv. Pharmacol. 49:41-66.
5. 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.
6. Croteau, G., L. Doyon, D. Thibeault, G. McKercher, L. Pilote, and D. Lamarre. 1997. Impaired fitness of human immunodeficiency virus type 1 variants with high-level resistance to protease inhibitors. J. Virol. 71:1089-1096.
7. de Jong, J. J., J. Goudsmit, V. V. Lukashov, M. E. Hillebrand, E. Baan, R. Huismans, S. A. Danner, J. H. ten Veen, F. de Wolf, and S. Jurriaans. 1999. Insertion of two amino acids combined with changes in reverse transcriptase containing tyrosine-215 of HIV-1 resistant to multiple nucleoside analogs. AIDS 13:75-80.
8. de Oliveira, T., S. Engelbrecht, E. Janse van Rensburg, M. Gordon, K. Bishop, J. zur Megede, S. W. Barnett, and S. Cassol. 2003. Variability at human immunodeficiency virus type 1 subtype C protease cleavage sites: an indication of viral fitness? J. Virol. 77:9422-9430.
9. Dewar, R. L., H. C. Highbarger, M. D. Sarmiento, J. A. Todd, M. B. Vasudevachari, R. T. Davey, Jr., J. A. Kovacs, N. P. Salzman, H. C. Lane, and M. S. Urdea. 1994. Application of branched DNA signal amplification to monitor human immunodeficiency virus type 1 burden in human plasma. J. Infect. Dis. 170:1172-1179.
10. Doyen, L., G. Croteau, D. Thibeault, F. Poulin, L. Pilote, and D. Lamarre. 1996. Second locus involved in human immunodeficiency virus type 1 resistance to protease inhibitors. J. Virol. 70:3763-3769.
11. Gonda, M. A., S. A. Aaronson, N. Ellmore. V. H. Zeve, and K. Nagashima. 1976. Ultrastructural studies of surface features of human normal and tumor cells in tissue culture by scanning and transmission electron microscopy. J. Natl. Cancer Inst. 56:245-263.
12. Haertle, T., C. J. Carrera, D. B. Wasson, L. C. Sowers, D. D. Richman, and D. A. Carson. 1988. Metabolism and anti-human immunodeficiency virus-1 activity of 2-halo-2′,3′-dideoxyadenosine derivatives. J. Biol. Chem. 263: 5870-5875.
13. Harada, S., Y. Koyanagi, and N. Yamamoto. 1985. Infection of HTLV-III/LAV in HTLV-carrying cells MT-2 and MT-4 and application in a plaque assay. Science 229:563-566.
14. Harrigan, P. R., B. Stuart, and B. A. Larder. 1998. Relative replicative fitness of zidovudine-resistant human immunodeficiency virus type 1 isolates in vitro. J. Virol. 72:3773-3778.
15. Imamichi, T., S. C. Berg, H. Imamichi, J. C. Lopez, J. A. Metcalf, J. Falloon, and H. C. Lane. 2000. Relative replication fitness of a high-level 3′Azido-3′-deoxythimidien resistant variant of human Immunodeficiency virus type-1 possessing an amino acid deletion at codon 67 and a novel substitution (Thr to Gly) at codon 69. J. Virol. 74:10958-10964.
16. Kagan, R., M. Winters, T. Merigan, and P. Heseltine. 2004. HIV type 1 genotypic resistance in a clinical database correlates with antiretroviral utilization. AIDS Res. Hum. Retrovir. 20:1-9.
17. 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.
18. Kim, E. Y., M. A. Winters, R. M. Kagan, and T. C. Merigan. 2001. Functional correlates of insertion mutations in the protease gene of human immunodeficiency virus type 1 isolates from patients. J. Virol. 75:11227-11233.
19. Kohl, N. E., E. A. Emini, W. A. Schleif, L. J. Davis, J. C. Heimbach, R. A. Dixon, E. M. Scolnick, and I. S. Sigal. 1988. Active human immunodeficiency virus protease is required for viral infectivity. Proc. Natl. Acad. Sci. USA 85:4686-4690.
20. Kovacs, J. A., S. Vogel, J. M. Albert, J. Falloon, R. T. Davey, Jr., R. E. Walker, M. A. Polis, K. Spooner, J. A. Metcalf, M. Baseler, G. Fyfe, and H. C. Lane. 1996. Controlled trial of interleukin-2 infusions in patients infected with the human immunodeficiency virus. N. Engl. J. Med. 335:1350-1356.
21. Larder, B. A., S. Bloor, S. D. Kemp, K. Hertogs, R. L. Desmet, V. Miller, M. Sturmer, S. Staszewski, J. Ren, D. K. Stammers, D. I. Stuart, and R. Pauwels. 1999. A family of insertion mutations between codons 67 and 70 of human immunodeficiency virus type 1 reverse transcriptase confer multinucleoside analog resistance. Antimicrob. Agents Chemother. 43:1961-1967.
22. Lobato, R. L., E. Y. Kim, R. M. Kagan, and T. C. Merigan. 2002. Genotypic and phenotypic analysis of a novel 15-base insertion occurring between codons 69 and 70 of HIV type 1 reverse transcriptase. AIDS Res. Hum. Retrovir. 18:733-736.
23. Logsdon, B. C., J. F. Vickrey, P. Martin, G. Proteasa, J. I. Koepke, S. R. Terlecky, Z. Wawrzak, M. A. Winters, T. C. Merigan, and L. C. Kovari. 2004. Crystal structures of a multidrug-resistant human immunodeficiency virus type 1 protease reveal an expanded active-site cavity. J. Virol. 78:3123-3132.
24. 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.
25. Martin, P., J. F. Vickrey, G. Proteasa, Y. L. Jimenez, Z. Wawrzak, M. A. Winters, T. C. Merigan, and L. C. Kovari. 2005. "Wide-open" 1.3 A structure of a multidrug-resistant HIV-1 protease as a drug target. Structure 13:1887-1895.
26. 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.
27. Masquelier, B., E. Race, C. Tamalet, D. Descamps, J. Izopet, C. Buffet-Janvresse, A. Ruffault, A. S. Mohammed, J. Cottalorda, A. Schmuck, V. Calvez, E. Dam, H. Fleury, F. Brun-Vezinet, and ANRS AC11 Resistance Study Group. 2001. Genotypic and phenotypic resistance patterns of human immunodeficiency virus type 1 variants with insertions or deletions in the reverse transcriptase (RT): multicenter study of patients treated with RT inhibitors. Antimicrob. Agents. Chemother. 45:1835-1842.
28. Nijhuis, M., R. Schuurman, 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.
29. Palella, F. J., K. M. Delaney, A. C. Moorman, M. O. Loveless, J. Fuhrer, G. A. Satten, D. J. Aschman, S. D. Holmberg, et al. 1998. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N. Engl. J. Med. 338:853-860.
30. Pettit, S. C., N. Sheng, R. Tritch, S. Erickson-Viitanen, and R. Swanstrom. 1998. The regulation of sequential processing of HIV-1 Gag by the viral protease. Adv. Exp. Med. Biol. 436:15-25.
31. Picchio, G. R., H. Valdez, R. Sabbe, A. L. Landay, D. R. Kuritzkes, M. M. Lederman, and D. E. Mosier. 2000. Altered viral fitness of HIV-1 following failure of protease inhibitor-based therapy. J. Acquir. Immune Defic. Syndr. 25:289-295.
32. Rambaut, A., D. Posada, K. A. Crandall, and E. C. Holmes. 2004. The causes and consequences of HIV evolution. Nat. Rev. Genet. 5:52-61.
33. 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. Retrovir. 16:1149-1156.
34. Schinazi, R. F., B. A. Larder, and J. W. Mellors. 2000. Mutations in retroviral genes associated with drug resistance: 1999-2000 update. Int. Antivir. News 7:46-69.
35. Sturmer, M., S. Staszewski, H. W. Doerr, and K. Hertogs. 2003. A 6-base pair insertion in the protease gene of HIV type 1 detected in a protease inhibitor-naive patient is not associated with indinavir treatment failure. AIDS Res. Hum. Retrovir. 19:967-968.
36. Tramuto, F., F. Bonura, S. Mancuso, N. Romano, and F. Vitale. 2005. Detection of a new 3-base pair insertion mutation in the protease gene of human immunodeficiency virus type 1 during highly active antiretroviral therapy (HAART). AIDS Res. Hum. Retrovir. 21:420-423.
37. van der Hoek, L., N. Back, M. F. Jebbink, A. de Ronde, M. Bakker, S. Jurriaans, P. Reiss, N. Parkin, and B. Berkhout. 2005. Increased multinucleoside drug resistance and decreased replicative capacity of a human immunodeficiency virus type 1 variant with an 8-amino-acid insert in the reverse transcriptase. J. Virol. 79:3536-3543.
38. van Vaerenbergh, K., K. Van Laethem, J. Albert, C. A. Boucher, B. Clotet, M. Floridia, J. Gerstoft, B. Hejdeman, C. Nielsen, C. Pannecouque, L. Perrin, M. F. Pirillo, L. Ruiz, J. C. Schmit, F. Schneider, A. Schoolmeester, R. Schuurman, H. J. Stellbrink, L. Stuyver, J. Van Lunzen, B. Van Remoortel, E. Van Wijngaerden, S. Vella, M. Witvrouw, S. Yerly, E. De Clercq, J. Destmyer, and A. M. Vandamme. 2000. Prevalence and characteristics of multinucleoside-resistant human immunodeficiency virus type 1 among European patients receiving combinations of nucleoside analogues. Antimicrob. Agents Chemother. 44:2109-2117.
39. Winters, M. A., K. L. Coolley, Y. A. Girard, D. J. Levee, H. Hamdan, R. W. Shafer, D. A. Katzenstein, and T. C. Merigan. 1998. A 6-basepair insert in the reverse transcriptase gene of human immunodeficiency virus type 1 confers resistance to multiple nucleoside inhibitors. J. Clin. Investig. 102: 1769-1775.
40. Winters, M. A., R. M. Kagan, P. N. Heseltine, and T. C. Merigan. 2005. New two-amino acid insertion near codon 70 of the HIV type 1 protease gene. AIDS Res. Hum. Retrovir. 21:311-313.
41. Wlodawer, A., and J. W. Erickson. 1993. Structure-based inhibitors of HIV-1 protease. Annu. Rev. Biochem. 62:543-583.
42. Wu, T. D., C. A. Schiffer, M. J. Gonzales, J. Taylor, R. Kantor, S. Chou, D. Israelski, A. R. Zolopa, W. J. Fessel, and R. W. Shafer. 2003. Mutation patterns and structural correlates in human immunodeficiency virus type 1 protease following different protease inhibitor treatments. J. Virol. 77:4836-4847.
43. Yeni, P. G., S. M. Hammer, C. C. Carpenter, D. A. Cooper, M. A. Fischl, J. M. Gatell, B. G. Gazzard, M. S. Hirsch, D. M. Jacobsen, D. A. Katzenstein, J. S. Montaner, D. D. Richman, M. S. Saag, M. Schechter, R. T. Schooley, M. A. Thompson, S. Vella, and P. A. Volberding. 2002. Antiretroviral treatment for adult HIV infection in 2002. Updated recommendations of the International AIDS Society-USA Panel. JAMA 288:222-235.
44. Zennou, V., F. Mammano, S. Paulous, D. Mathez, and F. Clavel. 1998. Loss of viral fitness associated with multiple Gag and Gag-Pol processing defects in human immunodeficiency virus type 1 variants selected for resistance to protease inhibitors in vivo. J. Virol. 72:3300-3306.
45. 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.