Impact of Y143 HIV-1 integrase mutations on resistance to raltegravir in vitro and in vivo

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 1, 2010, Pages 491-501

  Delelis, Olivier ^a   Thierry, Sylvain ^a   Subra, Frédéric ^a   Simon, Françoise ^a   Malet, Isabelle ^b,c,d   Alloui, Chakib ^e   Sayon, Sophie ^b,c,d   Calvez, Vincent ^b,c,d   Deprez, Eric ^a   Marcelin, Anne Geneviève ^b,c,d   Tchertanov, Luba ^a   Mouscadet, Jean François ^a  

^a Ecole Normale Superieure de Cachan   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c INSERM   (France)

^d ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^e UNIVERSITÉ PARIS 13   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRASE; RALTEGRAVIR;

ARTICLE; CASE REPORT; CONTROLLED STUDY; DNA INTEGRATION; ENZYME ACTIVITY; GENE MUTATION; GENETIC SUSCEPTIBILITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; IN VIVO STUDY; PRIORITY JOURNAL; VIRUS ISOLATION; VIRUS LOAD; VIRUS RESISTANCE;

EID: 73849095055     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01075-09     Document Type: Article

References (39)

1. Agapkina, J., M. Smolov, S. Barbe, E. Zubin, T. Zatsepin, E. Deprez, B. M. Le, J. F. Mouscadet, and M. Gottikh. 2006. Probing of HIV-1 integrase-DNA interactions using novel analogs of viral DNA. J. Biol. Chem. 281: 11530-11540.
2. Brown, P. O. 1990. Integration of retroviral DNA. Curr. Top. Microbiol. Immunol. 157:19-48.
3. Brussel, A., O. Delelis, and P. Sonigo. 2005. Alu-LTR real-time nested PCR assay for quantifying integrated HIV-1 DNA. Methods Mol. Biol. 304:139-154.
4. Bushman, F. D., and R. Craigie. 1991. Activities of human immunodeficiency virus (HIV) integration protein in vitro: specific cleavage and integration of HIV DNA. Proc. Natl. Acad. Sci. U. S. A. 88:1339-1343.
5. Ceccherini-Silberstein, F., I. Malet, R. D'Arrigo, A. Antinori, A. G. Marcelin, and C. F. Perno. 2009. Characterization and structural analysis of HIV-1 integrase conservation. AIDS Rev. 11:17-29.
6. Chen, A., I. T. Weber, R. W. Harrison, and J. Leis. 2006. Identification of amino acids in HIV-1 and avian sarcoma virus integrase subsites required for specific recognition of the long terminal repeat ends. J. Biol. Chem. 281: 4173-4182.
7. Connolly, M. L. 1983. Solvent-accessible surfaces of proteins and nucleicacids. Science 221:709-713.
8. Cooper, D. A., R. T. Steigbigel, J. M. Gatell, J. K. Rockstroh, C. Katlama, P. Yeni, A. Lazzarin, B. Clotet, P. N. Kumar, J. E. Eron, M. Schechter, M. Markowitz, M. R. Loutfy, J. L. Lennox, J. Zhao, J. Chen, D. M. Ryan, R. R. Rhodes, J. A. Killar, L. R. Gilde, K. M. Strohmaier, A. R. Meibohm, M. D. Miller, D. J. Hazuda, M. L. Nessly, M. J. DiNubile, R. D. Isaacs, H. Teppler, B. Y. Nguyen, and B. S. Teams. 2008. Subgroup and resistance analyses of raltegravir for resistant HIV-1 infection. N. Engl. J. Med. 359:355-365.
9. Croxtall, J. D., and S. J. Keam. 2009. Raltegravir: a review of its use in the management of HIV infection in treatment-experienced patients. Drugs 69:1059-1075.
10. Delelis, O., K. Carayon, E. Guiot, H. Leh, P. Tauc, J. C. Brochon, J. F. Mouscadet, and E. Deprez. 2008. Insight into the integrase-DNA recognition mechanism. A specific DNA-binding mode revealed by an enzymatically labeled integrase. J. Biol. Chem. 283:27838-27849.
11. Delelis, O., K. Carayon, A. Saib, E. Deprez, and J. F. Mouscadet. 2008. Integrase and integration: biochemical activities of HIV-1 integrase. Retrovirology 5:114.
12. Delelis, O., I. Malet, L. Na, L. Tchertanov, V. Calvez, A. G. Marcelin, F. Subra, E. Deprez, and J. F. Mouscadet. 2009. The G140S mutation in HIV integrases from raltegravir-resistant patients rescues catalytic defect due to the resistance Q148H mutation. Nucleic Acids Res. 37:1193-1201.
13. Engelman, A., and R. Craigie. 1992. Identification of conserved amino acid residues critical for human immunodeficiency virus type 1 integrase function in vitro. J. Virol. 66:6361-6369.
14. Espeseth, A. S., P. Felock, A. Wolfe, M. Witmer, J. Grobler, N. Anthony, M. Egbertson, J. Y. Melamed, S. Young, T. Hamill, J. L. Cole, and D. J. Hazuda. 2000. HIV-1 integrase inhibitors that compete with the target DNA substrate define a unique strand transfer conformation for integrase. Proc. Natl. Acad. Sci. U. S. A. 97:11244-11249.
15. Esposito, D., and R. Craigie. 1998. Sequence specificity of viral end DNA binding by HIV-1 integrase reveals critical regions for protein-DNA interaction. EMBO J. 17:5832-5843.
16. Ghose, A. K., and G. M. Crippen. 1986. Atomic physicochemical parameters for 3-dimensional structure-directed quantitative structure-activity-relationships. 1. Partition-coefficients as a measure of hydrophobicity. J. Comput. Chem. 7:565-577.
17. Grinsztejn, B., B. Y. Nguyen, C. Katlama, J. M. Gatell, A. Lazzarin, D. Vittecoq, C. J. Gonzalez, J. Chen, C. M. Harvey, and R. D. Isaacs. 2007. Safety and efficacy of the HIV-1 integrase inhibitor raltegravir (MK-0518) in treatment-experienced patients with multidrug-resistant virus: a phase II randomised controlled trial. Lancet 369:1261-1269.
18. Guiot, E., K. Carayon, O. Delelis, F. Simon, P. Tauc, E. Zubin, M. Gottikh, J. F. Mouscadet, J. C. Brochon, and E. Deprez. 2006. Relationship between the oligomeric status of HIV-1 integrase on DNA and enzymatic activity. J. Biol. Chem. 281:22707-22719.
19. Hazuda, D. J., P. Felock, M. Witmer, A. Wolfe, K. Stillmock, J. A. Grobler, A. Espeseth, L. Gabryelski, W. Schleif, C. Blau, and M. D. Miller. 2000. Inhibitors of strand transfer that prevent integration and inhibit HIV-1 replication in cells. Science 287:646-650.
20. Heiden, W., G. Moeckel, and J. Brickmann. 1993. A new approach to analysis and display of local lipophilicity hydrophilicity mapped on molecular-Surfaces. J. Comput. Aided Mol. Des. 7:503-514.
21. Johnson, A. A., C. Marchand, S. S. Patil, R. Costi, S. R. Di, T. R. Burke, Jr., and Y. Pommier. 2007. Probing HIV-1 integrase inhibitor binding sites with position-specific integrase-DNA cross-linking assays. Mol. Pharmacol. 71: 893-901.
22. Khan, E., J. P. Mack, R. A. Katz, J. Kulkosky, and A. M. Skalka. 1991. Retroviral integrase domains: DNA binding and the recognition of LTR sequences. Nucleic Acids Res. 19:851-860.
23. Kobayashi, M., K. Nakahara, T. Seki, S. Miki, S. Kawauchi, A. Suyama, C. Wakasa-Morimoto, M. Kodama, T. Endoh, E. Oosugi, Y. Matsushita, H. Murai, T. Fujishita, T. Yoshinaga, E. Garvey, S. Foster, M. Underwood, B. Johns, A. Sato, and T. Fujiwara. 2008. Selection of diverse and clinically relevant integrase inhibitor-resistant human immunodeficiency virus type 1 mutants. Antiviral Res. 80:213-222.
24. Laskowski, R. A., M. W. Macarthur, D. S. Moss, and J. M. Thornton. 1993. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
25. Leh, H., P. Brodin, J. Bischerour, E. Deprez, P. Tauc, J. C. Brochon, E. LeCam, D. Coulaud, C. Auclair, and J. F. Mouscadet. 2000. Determinants of Mg2+-dependent activities of recombinant human immunodeficiency virus type 1 integrase. Biochemistry 39:9285-9294.
26. Li, M., and R. Craigie. 2005. Processing of viral DNA ends channels the HIV-1 integration reaction to concerted integration. J. Biol. Chem. 280: 29334-29339.
27. Malet, I., O. Delelis, C. Soulie, M. Wirden, L. Tchertanov, P. Mottaz, G. Peytavin, C. Katlama, J. F. Mouscadet, V. Calvez, and A. G. Marcelin. 2009. Quasispecies variant dynamics during emergence of resistance to raltegravir in HIV-1-infected patients. J. Antimicrob. Chemother. 63:795-804.
28. Malet, I., O. Delelis, M. A. Valantin, B. Montes, C. Soulie, M. Wirden, L. Tchertanov, G. Peytavin, J. Reynes, J. F. Mouscadet, C. Katlama, V. Calvez, and A. G. Marcelin. 2008. Mutations associated with failure of raltegravir treatment affect integrase sensitivity to the inhibitor in vitro. Antimicrob. Agents Chemother. 52:1351-1358.
29. Marinello, J., C. Marchand, B. T. Mott, A. Bain, C. J. Thomas, and Y. Pommier. 2008. Comparison of raltegravir and elvitegravir on HIV-1 integrase catalytic reactions and on a series of drug-resistant integrase mutants. Biochemistry 47:9345-9354.
30. Markowitz, M., B. Y. Nguyen, E. Gotuzzo, F. Mendo, W. Ratanasuwan, C. Kovacs, G. Prada, J. O. Morales-Ramirez, C. S. Crumpacker, R. D. Isaacs, L. R. Gilde, H. Wan, M. D. Miller, L. A. Wenning, and H. Teppler. 2007. Rapid and durable antiretroviral effect of the HIV-1 integrase inhibitor raltegravir as part of combination therapy in treatment-naive patients with HIV-1 infection: results of a 48-week controlled study. J. Acquir. Immune Defic. Syndr. 46:125-133.
31. Mouscadet, J. F., R. Arora, J. Andre, J. C. Lambry, O. Delelis, I. Malet, A. G. Marcelin, V. Calvez, and L. Tchertanov. 2009. HIV-1 IN alternative molecular recognition of DNA induced by raltegravir resistance mutations. J. Mol. Recognit. 22:480-494.
32. Pauza, C. D., P. Trivedi, T. S. McKechnie, D. D. Richman, and F. M. Graziano. 1994. 2-LTR circular viral DNA as a marker for human immunodeficiency virus type 1 infection in vivo. Virology 205:470-478.
33. Quercia, R., E. Dam, D. Perez-Bercoff, and F. Clavel. 2009. Selective-advantage profile of HIV-1 integrase mutants explains in vivo evolution of raltegravir resistance genotypes. J. Virol. 83:10245-10249.
34. Shin, C. G., B. Taddeo, W. A. Haseltine, and C. M. Farnet. 1994. Genetic analysis of the human immunodeficiency virus type 1 integrase protein. J. Virol. 68:1633-1642.
35. Sichtig, N., S. Sierra, R. Kaiser, M. Daumer, S. Reuter, E. Schulter, A. Altmann, G. Fatkenheuer, U. Dittmer, H. Pfister, and S. Esser. 2009. Evolution of raltegravir resistance during therapy. J. Antimicrob. Chemother. 64:25-32.
36. Smolov, M., M. Gottikh, V. Tashlitskii, S. Korolev, I. Demidyuk, J. C. Brochon, J. F. Mouscadet, and E. Deprez. 2006. Kinetic study of the HIV-1 DNA 3′-end processing. FEBS J. 273:1137-1151.
37. Svarovskaia, E. S., R. Barr, X. Zhang, G. C. Pais, C. Marchand, Y. Pommier, T. R. Burke, Jr., and V. K. Pathak. 2004. Azido-containing diketo acid derivatives inhibit human immunodeficiency virus type 1 integrase in vivo and influence the frequency of deletions at two-long-terminal-repeat-circle junctions. J. Virol. 78:3210-3222.
38. Wielens, J., I. T. Crosby, and D. K. Chalmers. 2005. A three-dimensional model of the human immunodeficiency virus type 1 integration complex. J. Comput. Aided Mol. Des. 19:301-317.
39. Yeni, P. 2008. Prise en charge médicale des personnes infectées par le VIH. http://www.sante.gouv.fr/htm/actu/yeni-sida/ rapport-experts-2006.pdf.