Role of the envelope genetic context in the development of enfuvirtide resistance in human immunodeficiency virus type 1-infected patients

Journal of Virology

Volumn 80, Issue 17, 2006, Pages 8807-8819

  Labrosse, Béatrice ^a,b   Morand Joubert, Laurence ^c,d   Goubard, Armelle ^a,b   Rochas, Séverine ^e   Labernardière, Jean Louis ^e   Pacanowski, Jerôme ^c,d   Meynard, Jean Luc ^c,d   Hance, Allan J ^a,b   Clavel, François ^a,b   Mammano, Fabrizio ^a,b  

^a BICHAT HOSPITAL   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL SAINT ANTOINE   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e BioAlliance Pharma   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENFUVIRTIDE; GLYCOPROTEIN GP 41; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; VIRUS ENVELOPE PROTEIN;

ARTICLE; CLINICAL ARTICLE; DRUG RESISTANCE; DRUG SENSITIVITY; EVOLUTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IC 50; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; SALVAGE THERAPY; VIRUS MUTATION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; CELL LINE; DRUG RESISTANCE, VIRAL; EVOLUTION, MOLECULAR; GENOTYPE; HIV ENVELOPE PROTEIN GP120; HIV ENVELOPE PROTEIN GP41; HIV FUSION INHIBITORS; HIV-1; HUMANS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHENOTYPE; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33748669404     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02706-05     Document Type: Article

References (46)

1. Baldwin, C. E., R. W. Sanders, and B. Berkhout. 2003. Inhibiting HIV-1 entry with fusion inhibitors. Curr. Med. Chem. 10:1633-1642.
2. Baldwin, C. E., R. W. Sanders, Y. Deng, S. Jurriaans, J. M. Lange, M. Lu, and B. Berkhout. 2004. Emergence of a drug-dependent human immunodeficiency virus type 1 variant during therapy with the T20 fusion inhibitor. J. Virol. 78:12428-12437.
3. Centers for Disease Control and Prevention. 1993. From the Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. JAMA 269:729-730.
4. Chan, D. C., D. Fass, J. M. Berger, and P. S. Kim. 1997. Core structure of gp41 from the HIV envelope glycoprotein. Cell 89:263-273.
5. Chen, C. H., T. J. Matthews, C. B. McDanal, D. P. Bolognesi, and M. L. Greenberg. 1995. A molecular clasp in the human immunodeficiency virus (HIV) type 1 TM protein determines the anti-HIV activity of gp41 derivatives: implication for viral fusion. J. Virol. 69:3771-3777.
6. Chou, T.-C. 1991. The median-effect principle and the combination index for quantitation of synergism and antagonism, p. 61-102. In T.-C. Chou and D. C. Rideout (ed.), Synergism and antagonism in chemotherapy. Academic Press, San Diego, Calif.
7. Clavel, F., and A. J. Hance. 2004. HIV drug resistance. N. Engl. J. Med. 350:1023-1035.
8. 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.
9. Derdeyn, C. A., J. M. Decker, J. N. Sfakianos, Z. Zhang, W. A. O'Brien, L. Ratner, G. M. Shaw, and E. Hunter. 2001. Sensitivity of human immunodeficiency virus type 1 to fusion inhibitors targeted to the gp41 first heptad repeat involves distinct regions of gp41 and is consistently modulated by gp120 interactions with the coreceptor. J. Virol. 75:8605-8614.
10. Dong, X. N., Y. Xiao, M. P. Dierich, and Y. H. Chen. 2001. N and C domains of HIV-1 gp41: mutation, structure and functions. Immunol. Lett. 75:215-220.
11. Eckert, D. M., and P. S. Kim. 2001. Mechanisms of viral membrane fusion and its inhibition. Annu. Rev. Biochem. 70:777-810.
12. Edwards, T. G., S. Wyss, J. D. Reeves, S. Zolla-Pazner, J. A. Hoxie, R. W. Doms, and F. Baribaud. 2002. Truncation of the cytoplasmic domain induces exposure of conserved regions in the ectodomain of human immunodeficiency virus type 1 envelope protein. J. Virol. 76:2683-2691.
13. Gabuzda, D. H., A. Lever, E. Terwilliger, and J. Sodroski. 1992. Effects of deletions in the cytoplasmic domain on biological functions of human immunodeficiency virus type 1 envelope glycoproteins. J. Virol. 66:3306-3315.
14. Gallo, S. A., C. M. Finnegan, M. Viard, Y. Raviv, A. Dimitrov, S. S. Rawat, A. Puri, S. Durell, and R. Blumenthal. 2003. The HIV Env-mediated fusion reaction. Biochim. Biophys. Acta 1614:36-50.
15. Heil, M. L., J. M. Decker, J. N. Sfakianos, G. M. Shaw, E. Hunter, and C. A. Derdeyn. 2004. Determinants of human immunodeficiency virus type 1 baseline susceptibility to the fusion inhibitors enfuvirtide and T-649 reside outside the peptide interaction site. J. Virol. 78:7582-7589.
16. Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J. Mol. Evol. 29:170-179.
17. Kliger, Y., S. A. Gallo, S. G. Peisajovich, I. Munoz-Barroso, S. Avkin, R. Blumenthal, and Y. Shai. 2001. Mode of action of an antiviral peptide from HIV-1. Inhibition at a post-lipid mixing stage. J. Biol. Chem. 276:1391-1397.
18. Labrijn, A. F., and W. H. I. Parren. 1999. Neutralizing epitopes of HIV-1, p. 18-34. In C. Kuiken, B. Foley, B. H. Hahn, P. Marx, F. E. McCutchan, J. Mellors, et al. (ed.), HIV sequence compendium 1999. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N. Mex.
19. Labrosse, B., A. Brelot, N. Heveker, N. Sol, D. Schols, E. De Clercq, and M. Alizon. 1998. Determinants for sensitivity of human immunodeficiency virus coreceptor CXCR4 to the bicyclam AMD3100. J. Virol. 72:6381-6388.
20. Labrosse, B., J. L. Labernardiere, E. Dam, V. Trouplin, K. Skrabal, F. Clavel, and F. Mammano. 2003. Baseline susceptibility of primary human immunodeficiency virus type 1 to entry inhibitors. J. Virol. 77:1610-1613.
21. Lalezari, J. P., E. DeJesus, D. W. Northfelt, G. Richmond, P. Wolfe, R. Haubrich, D. Henry, W. Powderly, S. Becker, M. Thompson, F. Valentine, D. Wright, M. Carlson, S. Riddler, F. F. Haas, R. DeMasi, P. R. Sista, M. Salgo, and J. Delehanty. 2003. A controlled phase II trial assessing three doses of enfuvirtide (T-20) in combination with abacavir, amprenavir, ritonavir and efavirenz in non-nucleoside reverse transcriptase inhibitor-naive HIV-infected adults. Antivir. Ther. 8:279-287.
22. Lalezari, J. P., J. J. Eron, M. Carlson, C. Cohen, E. DeJesus, R. C. Arduino, J. E. Gallant, P. Volberding, R. L. Murphy, F. Valentine, E. L. Nelson, P. R. Sista, A. Dusek, and J. M. Kilby. 2003. A phase II clinical study of the long-term safety and antiviral activity of enfuvirtide-based antiretroviral therapy. Aids 17:691-698.
23. Lalezari, J. P., K. Henry, M. O'Hearn, J. S. Montaner, P. J. Piliero, B. Trottier, S. Walmsley, C. Cohen, D. R. Kuritzkes, J. J. Eron, Jr., J. Chung, R. DeMasi, L. Donatacci, C. Drobnes, J. Delehanty, and M. Salgo. 2003. Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in North and South America. N. Engl. J. Med. 348:2175-2185.
24. Lawless, M. K., S. Barney, K. I. Guthrie, T. B. Bucy, S. R. Petteway, Jr., and G. Merutka. 1996. HIV-1 membrane fusion mechanism: structural studies of the interactions between biologically active peptides from gp41. Biochemistry 35:13697-13708.
25. 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.
26. Menzo, S., A. Castagna, A. Monachetti, H. Hasson, A. Danise, E. Carini, P. Bagnarelli, A. Lazzarin, and M. Clementi. 2004. Genotype and phenotype patterns of human immunodeficiency virus type 1 resistance to enfuvirtide during long-term treatment. Antimicrob. Agents Chemother. 48:3253-3259.
27. Mink, M., M. Greenberg, L. Mosier, S. Janumpalli, D. Davison, L. Jin, T. Melby, P. Sista, D. Lambert, N. Cammack, M. Salgo, and T. Matthews. 2002. Impact of HIV-1 gp41 amino acid substitutions (positions 36-45) on susceptibility to T-20 (enfuvirtide) in vitro: analysis of primary virus isolates recovered from patients during chronic enfuvirtide treatment and site-directed mutants in NL4-3, abstr. 22. Antivir. Ther. 7(Suppl. 1):S24.
28. Moore, J. P., and R. W. Doms. 2003. The entry of entry inhibitors: a fusion of science and medicine. Proc. Natl. Acad. Sci. USA 100:10598-10602.
29. Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
30. Platt, E. J., J. P. Durnin, and D. Kabat. 2005. Kinetic factors control efficiencies of cell entry, efficacies of entry inhibitors, and mechanisms of adaptation of human immunodeficiency virus. J. Virol. 79:4347-4356.
31. + cells expressing the rat homolog of CXCR-4 (fusin). J. Virol. 71:3259-3262.
32. Poveda, E., B. Rodes, J. L. Labernardiere, J. M. Benito, C. Toro, J. Gonzalez-Lahoz, J. L. Faudon, F. Clavel, J. Schapiro, and V. Soriano. 2004. Evolution of genotypic and phenotypic resistance to enfuvirtide in HIV-infected patients experiencing prolonged virologic failure. J. Med. Virol. 74:21-28.
33. Quinones-Mateu, M. E., and E. J. Arts. 2001. HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution, p. 134-170. In C. Kuiken, B. Foley, B. H. Hahn, P. Marx, F. E. McCutchan, J. Mellors, et al. (ed.), HIV sequence compendium 2001. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N. Mex.
34. Reeves, J. D., S. A. Gallo, N. Ahmad, J. L. Miamidian, P. E. Harvey, M. Sharron, S. Pohlmann, J. N. Sfakianos, C. A. Derdeyn, R. Blumenthal, E. Hunter, and R. W. Doms. 2002. Sensitivity of HIV-1 to entry inhibitors correlates with envelope/coreceptor affinity, receptor density, and fusion kinetics. Proc. Natl. Acad. Sci. USA 99:16249-16254.
35. Rimsky, L. T., D. C. Shugars, and T. J. Matthews. 1998. Determinants of human immunodeficiency virus type 1 resistance to gp41-derived inhibitory peptides. J. Virol. 72:986-993.
36. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
37. Sanders, R. W., B. Korber, M. Lu, B. Berkhout, and J. P. Moore. 2002. Mutational analyses and natural variability of the gp41 ectodomain, p. 43-68. In C. Kuiken, B. Foley, B. H. Hahn, P. Marx, F. E. McCutchan, J. Mellors, et al. (ed.) HIV sequence compendium 2002. Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, N. Mex.
38. Sista, P., T. Melby, M. L. Greenberg, R. DeMasi, D. Kuritzkes, M. Nelson, C. Petropoulos, M. Salgo, N. Cammack, and T. J. Matthews. 2003. Subgroup analysis of baseline susceptibility and early virological response to enfuvirtide in the combined TORO studies. Antivir. Ther. 8:S60.
39. Sista, P. R., T. Melby, D. Davison, L. Jin, S. Mosier, M. Mink, E. L. Nelson, R. DeMasi, N. Cammack, M. P. Salgo, T. J. Matthews, and M. L. Greenberg. 2004. Characterization of determinants of genotypic and phenotypic resistance to enfuvirtide in baseline and on-treatment HIV-1 isolates. AIDS 18:1787-1794.
40. Tan, K., J. Liu, J. Wang, S. Shen, and M. Lu. 1997. Atomic structure of a thermostable subdomain of HIV-1 gp41. Proc. Natl. Acad. Sci. USA 94:12303-12308.
41. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
42. Wei, X., J. M. Decker, H. Liu, Z. Zhang, R. B. Arani, J. M. Kilby, M. S. Saag, X. Wu, G. M. Shaw, and J. C. Kappes. 2002. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46:1896-1905.
43. Weissenhorn, W., A. Dessen, S. C. Harrison, J. J. Skehel, and D. C. Wiley. 1997. Atomic structure of the ectodomain from HIV-1 gp41. Nature 387:426-430.
44. Wild, C. T., D. C. Shugars, T. K. Greenwell, C. B. McDanal, and T. J. Matthews. 1994. Peptides corresponding to a predictive alpha-helical domain of human immunodeficiency virus type 1 gp41 are potent inhibitors of virus infection. Proc. Natl. Acad. Sci. USA 91:9770-9774.
45. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
46. Xu, L., A. Pozniak, A. Wildfire, S. A. Stanfield-Oakley, S. M. Mosier, D. Ratcliffe, J. Workman, A. Joall, R. Myers, E. Smit, P. A. Cane, M. L. Greenberg, and D. Pillay. 2005. Emergence and evolution of enfuvirtide resistance following long-term therapy involves heptad repeat 2 mutations within gp41. Antimicrob. Agents Chemother. 49:1113-1119.