Mutations in variable domains of the HIV-1 envelope gene can have a significant impact on maraviroc and vicriviroc resistance

AIDS Research and Therapy

Volumn 10, Issue 1, 2013, Pages

  Asin Milan, Odalis ^a,b   Chamberland, Annie ^a,b   Wei, Yi ^a   Haidara, Alpha ^a,b   Sylla, Mohamed ^a,b   Tremblay, Cécile L ^a,b,c  

^a CENTRE HOSPITALIER DE L UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c INSTITUT NATIONAL DE SANTÉ PUBLIQUE DU QUÉBEC   (Canada)

Author keywords

CCR5 Inhibitors; Maraviroc; Resistance; Vicriviroc

Indexed keywords

GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; MARAVIROC; VICRIVIROC; VIRUS RNA;

AMINO ACID SUBSTITUTION; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; CONTROLLED STUDY; DNA POLYMORPHISM; GENE AMPLIFICATION; GENE MUTATION; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VITRO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; VIRAL TROPISM; VIRUS INFECTIVITY;

EID: 84878639976     PISSN: None     EISSN: 17426405     Source Type: Journal    
DOI: 10.1186/1742-6405-10-15     Document Type: Article

References (42)

1. Chen B, Vogan EM, Gong H, Skehel JJ, Wiley DC, Harrison SC. Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 2005, 433:834-841. 10.1038/nature03327, 15729334.
2. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, Hendrickson WA. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998, 393:648-659. 10.1038/31405, 9641677.
3. Pfaff JM, Wilen CB, Harrison JE, Demarest JF, Lee B, Doms RW, Tilton JC. HIV-1 resistance to CCR5 antagonists associated with highly efficient use of CCR5 and altered tropism on primary CD4+ T cells. J Virol 2010, 84:6505-6514. 10.1128/JVI.00374-10, 2903254, 20410277.
4. Tilton JC, Doms RW. Entry inhibitors in the treatment of HIV-1 infection. Antiviral Res 2010, 85:91-100. 10.1016/j.antiviral.2009.07.022, 19683546.
5. Berro R, Klasse PJ, Moore JP, Sanders RW. V3 determinants of HIV-1 escape from the CCR5 inhibitors Maraviroc and Vicriviroc. Virology 2012, 427:158-165. 10.1016/j.virol.2012.02.006, 3320651, 22424737.
6. Kondru R, Zhang J, Ji C, Mirzadegan T, Rotstein D, Sankuratri S, Dioszegi M. Molecular interactions of CCR5 with major classes of small-molecule anti-HIV CCR5 antagonists. Mol Pharmacol 2008, 73:789-800.
7. Strizki JM, Tremblay C, Xu S, Wojcik L, Wagner N, Gonsiorek W, Hipkin RW, Chou CC, Pugliese-Sivo C, Xiao Y, et al. Discovery and characterization of vicriviroc (SCH 417690), a CCR5 antagonist with potent activity against human immunodeficiency virus type 1. Antimicrob Agents Chemother 2005, 49:4911-4919. 10.1128/AAC.49.12.4911-4919.2005, 1315929, 16304152.
8. McNicholas PM, Mann PA, Wojcik L, Phd PQ, Lee E, McCarthy M, Shen J, Black TA, Strizki JM. Mapping and characterization of vicriviroc resistance mutations from HIV-1 isolated from treatment-experienced subjects enrolled in a phase II study (VICTOR-E1). J Acquir Immune Defic Syndr 2011, 56:222-229. 10.1097/QAI.0b013e3181ff63ee, 21209592.
9. Roche M, Jakobsen MR, Sterjovski J, Ellett A, Posta F, Lee B, Jubb B, Westby M, Lewin SR, Ramsland PA, et al. HIV-1 escape from the CCR5 antagonist maraviroc associated with an altered and less-efficient mechanism of gp120-CCR5 engagement that attenuates macrophage tropism. J Virol 2011, 85:4330-4342. 10.1128/JVI.00106-11, 3126252, 21345957.
10. McNicholas P, Wei Y, Whitcomb J, Greaves W, Black TA, Tremblay CL, Strizki JM. Characterization of emergent HIV resistance in treatment-naive subjects enrolled in a vicriviroc phase 2 trial. J Infect Dis 2010, 201:1470-1480. 10.1086/652189, 20373959.
11. Jensen MA, Li FS, van't Wout AB, Nickle DC, Shriner D, He HX, McLaughlin S, Shankarappa R, Margolick JB, Mullins JI. Improved coreceptor usage prediction and genotypic monitoring of R5-to-X4 transition by motif analysis of human immunodeficiency virus type 1 env V3 loop sequences. J Virol 2003, 77:13376-13388. 10.1128/JVI.77.24.13376-13388.2003, 296044, 14645592.
12. Jensen MA, Coetzer M, van't Wout AB, Morris L, Mullins JI. A reliable phenotype predictor for human immunodeficiency virus type 1 subtype C based on envelope V3 sequences. J Virol 2006, 80:4698-4704. 10.1128/JVI.80.10.4698-4704.2006, 1472078, 16641263.
13. Lengauer T, Sander O, Sierra S, Thielen A, Kaiser R. Bioinformatics prediction of HIV coreceptor usage. Nat Biotechnol 2007, 25:1407-1410. 10.1038/nbt1371, 18066037.
14. Westby M, Smith-Burchnell C, Mori J, Lewis M, Mosley M, Stockdale M, Dorr P, Ciaramella G, Perros M. Reduced maximal inhibition in phenotypic susceptibility assays indicates that viral strains resistant to the CCR5 antagonist maraviroc utilize inhibitor-bound receptor for entry. J Virol 2007, 81:2359-2371. 10.1128/JVI.02006-06, 1865946, 17182681.
15. Marozsan AJ, Kuhmann SE, Morgan T, Herrera C, Rivera-Troche E, Xu S, Baroudy BM, Strizki J, Moore JP. Generation and properties of a human immunodeficiency virus type 1 isolate resistant to the small molecule CCR5 inhibitor, SCH-417690 (SCH-D). Virology 2005, 338:182-199. 10.1016/j.virol.2005.04.035, 15935415.
16. Trkola A, Kuhmann SE, Strizki JM, Maxwell E, Ketas T, Morgan T, Pugach P, Xu S, Wojcik L, Tagat J, et al. HIV-1 escape from a small molecule, CCR5-specific entry inhibitor does not involve CXCR4 use. Proc Natl Acad Sci USA 2002, 99:395-400. 10.1073/pnas.012519099, 117571, 11782552.
17. Kuhmann SE, Pugach P, Kunstman KJ, Taylor J, Stanfield RL, Snyder A, Strizki JM, Riley J, Baroudy BM, Wilson IA, et al. Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor. J Virol 2004, 78:2790-2807. 10.1128/JVI.78.6.2790-2807.2004, 353740, 14990699.
18. Roche M, Jakobsen MR, Ellett A, Salimiseyedabad H, Jubb B, Westby M, Lee B, Lewin SR, Churchill MJ, Gorry PR. HIV-1 predisposed to acquiring resistance to maraviroc (MVC) and other CCR5 antagonists in vitro has an inherent, low-level ability to utilize MVC-bound CCR5 for entry. Retrovirology 2011, 8:89. 10.1186/1742-4690-8-89, 3217884, 22054077.
19. Zolla-Pazner S, Cardozo T. Structure-function relationships of HIV-1 envelope sequence-variable regions refocus vaccine design. Nat Rev Immunol 2010, 10:527-535. 10.1038/nri2801, 3167078, 20577269.
20. Anastassopoulou CG, Ketas TJ, Klasse PJ, Moore JP. Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41. Proc Natl Acad Sci USA 2009, 106:5318-5323. 10.1073/pnas.0811713106, 2664029, 19289833.
21. Yu X, Yuan L, Huang Y, Xu W, Fang Z, Liu S, Shao Y, Jiang S, Ma L. Susceptibility of HIV-1 Subtypes B′, CRF07_BC and CRF01_AE that Are Predominantly Circulating in China to HIV-1 Entry Inhibitors. PLoS One 2011, 6:e17605. 10.1371/journal.pone.0017605, 3055885, 21412427.
22. Yuan Y, Maeda Y, Terasawa H, Monde K, Harada S, Yusa K. A combination of polymorphic mutations in V3 loop of HIV-1 gp120 can confer noncompetitive resistance to maraviroc. Virology 2011, 413:293-299. 10.1016/j.virol.2011.02.019, 21440278.
23. Munoz-Nieto M, Perez-Alvarez L, Thomson M, Garcia V, Ocampo A, Casado G, Delgado E, Miralles C, de Parga EV, Sierra M, et al. HIV type 1 intersubtype recombinants during the evolution of a dual infection with subtypes B and G. AIDS Res Hum Retroviruses 2008, 24:337-343. 10.1089/aid.2007.0230, 18284328.
24. Wilkin TJ, Gulick RM. CCR5 antagonism in HIV infection: current concepts and future opportunities. Annu Rev Med 2012, 63:81-93. 10.1146/annurev-med-052010-145454, 3298858, 22034870.
25. Tilton JC, Wilen CB, Didigu CA, Sinha R, Harrison JE, Agrawal-Gamse C, Henning EA, Bushman FD, Martin JN, Deeks SG, Doms RW. A maraviroc-resistant HIV-1 with narrow cross-resistance to other CCR5 antagonists depends on both N-terminal and extracellular loop domains of drug-bound CCR5. J Virol 2010, 84:10863-10876. 10.1128/JVI.01109-10, 2950574, 20702642.
26. Platt EJ, Shea DM, Rose PP, Kabat D. Variants of human immunodeficiency virus type 1 that efficiently use CCR5 lacking the tyrosine-sulfated amino terminus have adaptive mutations in gp120, including loss of a functional N-glycan. J Virol 2005, 79:4357-4368. 10.1128/JVI.79.7.4357-4368.2005, 1061536, 15767436.
27. Wyatt R, Kwong PD, Desjardins E, Sweet RW, Robinson J, Hendrickson WA, Sodroski JG. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 1998, 393:705-711. 10.1038/31514, 9641684.
28. Wyatt R, Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 1998, 280:1884-1888. 10.1126/science.280.5371.1884, 9632381.
29. Xiang SH, Finzi A, Pacheco B, Alexander K, Yuan W, Rizzuto C, Huang CC, Kwong PD, Sodroski J. A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodeficiency virus envelope glycoprotein trimer. J Virol 2010, 84:3147-3161. 10.1128/JVI.02587-09, 2838131, 20089638.
30. Cormier EG, Dragic T. The crown and stem of the V3 loop play distinct roles in human immunodeficiency virus type 1 envelope glycoprotein interactions with the CCR5 coreceptor. J Virol 2002, 76:8953-8957. 10.1128/JVI.76.17.8953-8957.2002, 136967, 12163614.
31. Cormier EG, Tran DN, Yukhayeva L, Olson WC, Dragic T. Mapping the determinants of the CCR5 amino-terminal sulfopeptide interaction with soluble human immunodeficiency virus type 1 gp120-CD4 complexes. J Virol 2001, 75:5541-5549. 10.1128/JVI.75.12.5541-5549.2001, 114266, 11356961.
32. Huang CC, Lam SN, Acharya P, Tang M, Xiang SH, Hussan SS, Stanfield RL, Robinson J, Sodroski J, Wilson IA, et al. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 2007, 317:1930-1934. 10.1126/science.1145373, 2278242, 17901336.
33. Thielen A, Sichtig N, Kaiser R, Lam J, Harrigan PR, Lengauer T. Improved prediction of HIV-1 coreceptor usage with sequence information from the second hypervariable loop of gp120. J Infect Dis 2010, 202:1435-1443. 10.1086/656600, 20874088.
34. Monno L, Saracino A, Scudeller L, Punzi G, Brindicci G, Altamura M, Lagioia A, Ladisa N, Angarano G. Impact of mutations outside the V3 region on coreceptor tropism phenotypically assessed in patients infected with HIV-1 subtype B. Antimicrob Agents Chemother 2011, 55:5078-5084. 10.1128/AAC.00743-11, 3195025, 21876051.
35. Gonzalez-Ortega E, Ballana E, Badia R, Clotet B, Este JA. Compensatory mutations rescue the virus replicative capacity of VIRIP-resistant HIV-1. Antiviral Res 2011, 92:479-483. 10.1016/j.antiviral.2011.10.010, 22027647.
36. Lucas GM. Antiretroviral adherence, drug resistance, viral fitness and HIV disease progression: a tangled web is woven. J Antimicrob Chemother 2005, 55:413-416. 10.1093/jac/dki042, 15722389.
37. Poveda E, Alcami J, Paredes R, Cordoba J, Gutierrez F, Llibre JM, Delgado R, Pulido F, Iribarren JA, Garcia Deltoro M, et al. Genotypic determination of HIV tropism - clinical and methodological recommendations to guide the therapeutic use of CCR5 antagonists. AIDS Rev 2010, 12:135-148.
38. The stratagene's web-based Primer Design Program QuikChange® available at website at [http://www.genomics.agilent.com/primerDesignProgram.jsp]
39. GJM W, Robb FT, Kanoksilapatham Directed-Mutagenesis and Deletion Generated through an Improved Overlapping-Extension PCR Based Procedure. Silpakorn U Sci Tech J Vol 2007, 1:7-12. Kanoksilapatham.
40. Aiyar A, Xiang Y, Leis J. Site-directed mutagenesis using overlap extension PCR. Methods Mol Biol 1996, 57:177-191.
41. Connor RI, Sheridan KE, Lai C, Zhang L, Ho DD. Characterization of the functional properties of env genes from long-term survivors of human immunodeficiency virus type 1 infection. J Virol 1996, 70:5306-5311. 190488, 8764041.
42. Singh A, Page T, Moore PL, Allgaier RL, Hiramen K, Coovadia HM, Walker BD, Morris L, Ndung'u T. Functional and genetic analysis of coreceptor usage by dualtropic HIV-1 subtype C isolates. Virology 2009, 393:56-67. 10.1016/j.virol.2009.07.021, 3492694, 19695656.