Clinical resistance to vicriviroc through adaptive V3 loop mutations in HIV-1 subtype D gp120 that alter interactions with the N-terminus and ECL2 of CCR5

Virology

Volumn 400, Issue 1, 2010, Pages 145-155

  Ogert, Robert A ^a   Hou, Yan ^a   Ba, Lei ^a   Wojcik, Lisa ^a   Qiu, Ping ^a   Murgolo, Nicholas ^a   Duca, Jose ^a   Dunkle, Lisa M ^a   Ralston, Robert ^a   Howe, John A ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

Author keywords

CCR5 antagonists; CCR5 co receptor; gp120 resistance mutations; GPCR; HIV 1; Vicriviroc; Virus entry

Indexed keywords

ALANINE; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; VICRIVIROC;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ANTIGEN EXPRESSION; ANTIVIRAL RESISTANCE; ARTICLE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MODEL; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; SEQUENCE ANALYSIS; VIRUS ENVELOPE; VIRUS GENE; VIRUS INFECTIVITY; VIRUS REPLICATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTIBODIES, MONOCLONAL; CELL LINE; DRUG RESISTANCE, VIRAL; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; HOST-PATHOGEN INTERACTIONS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PIPERAZINES; PYRIMIDINES; RECEPTORS, CCR5; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 77649188640     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.01.037     Document Type: Article

References (40)

1. Agrawal-Gamse C., Lee F.H., Haggarty B., Jordan A.P., Yi Y., Lee B., Collman R.G., Hoxie J.A., Doms R.W., and Laakso M.M. Adaptive mutations in a human immunodeficiency virus type 1 envelope protein with a truncated V3 loop restore function by improving interactions with CD4. J. Virol. 83 21 (2009) 11005-11015
2. Berro R., Sanders R.W., Lu M., Klasse P.J., and Moore J.P. Two HIV-1 variants resistant to small molecule CCR5 inhibitors differ in how they use CCR5 for entry. PLoS Pathog. 5 8 (2009) e1000548
3. Blanpain C., Lee B., Vakili J., Doranz B.J., Govaerts C., Migeotte I., Sharron M., Dupriez V., Vassart G., Doms R.W., and Parmentier M. Extracellular cysteines of CCR5 are required for chemokine binding, but dispensable for HIV-1 coreceptor activity. J. Biol. Chem. 274 27 (1999) 18902-18908
4. Buontempo P.J., Wojcik L., Buontempo C.A., Ogert R.A., Strizki J.M., Howe J.A., and Ralston R. Quantifying the relationship between HIV-1 susceptibility to CCR5 antagonists and virus affinity for antagonist-occupied co-receptor. Virology 395 2 (2009) 268-279
5. Cherezov V., Rosenbaum D.M., Hanson M.A., Rasmussen S.G., Thian F.S., Kobilka T.S., Choi H.J., Kuhn P., Weis W.I., Kobilka B.K., and Stevens R.C. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318 5854 (2007) 1258-1265
6. Dragic T., Trkola A., Thompson D.A., Cormier E.G., Kajumo F.A., Maxwell E., Lin S.W., Ying W., Smith S.O., Sakmar T.P., and Moore J.P. A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5. Proc. Natl. Acad. Sci. U. S. A. 97 10 (2000) 5639-5644
7. Gulick R.M., Lalezari J., Goodrich J., Clumeck N., DeJesus E., Horban A., Nadler J., Clotet B., Karlsson A., Wohlfeiler M., Montana J.B., McHale M., Sullivan J., Ridgway C., Felstead S., Dunne M.W., van der Ryst E., and Mayer H. Maraviroc for previously treated patients with R5 HIV-1 infection. N. Engl. J. Med. 359 14 (2008) 1429-1441
8. Gulick R.M., Su Z., Flexner C., Hughes M.D., Skolnik P.R., Wilkin T.J., Gross R., Krambrink A., Coakley E., Greaves W.L., Zolopa A., Reichman R., Godfrey C., Hirsch M., and Kuritzkes D.R. Phase 2 study of the safety and efficacy of vicriviroc, a CCR5 inhibitor, in HIV-1-infected, treatment-experienced patients: AIDS Clinical Trials Group 5211. J. Infect. Dis. 196 2 (2007) 304-312
9. Huang C.C., Lam S.N., Acharya P., Tang M., Xiang S.H., Hussan S.S., Stanfield R.L., Robinson J., Sodroski J., Wilson I.A., Wyatt R., Bewley C.A., and Kwong P.D. Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317 5846 (2007) 1930-1934
10. Huang C.C., Tang M., Zhang M.Y., Majeed S., Montabana E., Stanfield R.L., Dimitrov D.S., Korber B., Sodroski J., Wilson I.A., Wyatt R., and Kwong P.D. Structure of a V3-containing HIV-1 gp120 core. Science 310 5750 (2005) 1025-1028
11. Ji C., Zhang J., Dioszegi M., Chiu S., Rao E., Derosier A., Cammack N., Brandt M., and Sankuratri S. CCR5 small-molecule antagonists and monoclonal antibodies exert potent synergistic antiviral effects by cobinding to the receptor. Mol. Pharmacol. 72 1 (2007) 18-28
12. Kondru R., Zhang J., Ji C., Mirzadegan T., Rotstein D., Sankuratri S., and Dioszegi M. Molecular interactions of CCR5 with major classes of small-molecule anti-HIV CCR5 antagonists. Mol. Pharmacol. 73 3 (2008) 789-800
13. Laakso M.M., Lee F.H., Haggarty B., Agrawal C., Nolan K.M., Biscone M., Romano J., Jordan A.P., Leslie G.J., Meissner E.G., Su L., Hoxie J.A., and Doms R.W. V3 loop truncations in HIV-1 envelope impart resistance to coreceptor inhibitors and enhanced sensitivity to neutralizing antibodies. PLoS Pathog. 3 8 (2007) e117
14. Landovitz R.J., Angel J.B., Hoffmann C., Horst H., Opravil M., Long J., Greaves W., and Fatkenheuer G. Phase II study of vicriviroc versus efavirenz (both with zidovudine/lamivudine) in treatment-naive subjects with HIV-1 infection. J. Infect. Dis. 198 8 (2008) 1113-1122
15. Lee B., Sharron M., Blanpain C., Doranz B.J., Vakili J., Setoh P., Berg E., Liu G., Guy H.R., Durell S.R., Parmentier M., Chang C.N., Price K., Tsang M., and Doms R.W. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274 14 (1999) 9617-9626
16. Lin G., Bertolotti-Ciarlet A., Haggarty B., Romano J., Nolan K.M., Leslie G.J., Jordan A.P., Huang C.C., Kwong P.D., Doms R.W., and Hoxie J.A. Replication-competent variants of human immunodeficiency virus type 2 lacking the V3 loop exhibit resistance to chemokine receptor antagonists. J. Virol. 81 18 (2007) 9956-9966
17. Maeda K., Das D., Ogata-Aoki H., Nakata H., Miyakawa T., Tojo Y., Norman R., Takaoka Y., Ding J., Arnold G.F., Arnold E., and Mitsuya H. Structural and molecular interactions of CCR5 inhibitors with CCR5. J. Biol. Chem. 281 18 (2006) 12688-12698
18. Maeda K., Das D., Yin P.D., Tsuchiya K., Ogata-Aoki H., Nakata H., Norman R.B., Hackney L.A., Takaoka Y., and Mitsuya H. Involvement of the second extracellular loop and transmembrane residues of CCR5 in inhibitor binding and HIV-1 fusion: insights into the mechanism of allosteric inhibition. J. Mol. Biol. 381 4 (2008) 956-974
19. Marozsan A.J., Kuhmann S.E., Morgan T., Herrera C., Rivera-Troche E., Xu S., Baroudy B.M., Strizki J., and Moore J.P. Generation and properties of a human immunodeficiency virus type 1 isolate resistant to the small molecule CCR5 inhibitor, SCH-417690 (SCH-D). Virology 338 1 (2005) 182-199
20. Moore J.P., and Kuritzkes D.R. A piece de resistance: how HIV-1 escapes small molecule CCR5 inhibitors. Curr. Opin. HIV AIDS 4 2 (2009) 118-124
21. Nishikawa M., Takashima K., Nishi T., Furuta R.A., Kanzaki N., Yamamoto Y., and Fujisawa J. Analysis of binding sites for the new small-molecule CCR5 antagonist TAK-220 on human CCR5. Antimicrob. Agents Chemother. 49 11 (2005) 4708-4715
22. Nolan K.M., Del Prete G.Q., Jordan A.P., Haggarty B., Romano J., Leslie G.J., and Hoxie J.A. Characterization of a human immunodeficiency virus type 1 V3 deletion mutation that confers resistance to CCR5 inhibitors and the ability to use aplaviroc-bound receptor. J. Virol. 83 8 (2009) 3798-3809
23. Nolan K.M., Jordan A.P., and Hoxie J.A. Effects of partial deletions within the human immunodeficiency virus type 1 V3 loop on coreceptor tropism and sensitivity to entry inhibitors. J. Virol. 82 2 (2008) 664-673
24. Ogert R.A., Ba L., Hou Y., Buontempo C., Qiu P., Duca J., Murgolo N., Buontempo P., Ralston R., and Howe J.A. Structure-function analysis of human immunodeficiency virus type 1 gp120 amino acid mutations associated with resistance to the CCR5 coreceptor antagonist vicriviroc. J. Virol. 83 23 (2009) 12151-12163
25. Ogert R.A., Wojcik L., Buontempo C., Ba L., Buontempo P., Ralston R., Strizki J., and Howe J.A. Mapping resistance to the CCR5 co-receptor antagonist vicriviroc using heterologous chimeric HIV-1 envelope genes reveals key determinants in the C2-V5 domain of gp120. Virology 373 2 (2008) 387-399
26. Pfizer, Inc. Maraviroc Tablets NDA 22-128: Antiviral Drugs Advisory Committee (AVDAC) Briefing Document (2007), Pfizer Inc, New York, NY. http://www.fda.gov/OHRMS/DOCKETS/AC/07/briefing/ http://www.fda.gov/OHRMS/DOCKETS/AC/07/briefing/
27. Pugach P., Marozsan A.J., Ketas T.J., Landes E.L., Moore J.P., and Kuhmann S.E. HIV-1 clones resistant to a small molecule CCR5 inhibitor use the inhibitor-bound form of CCR5 for entry. Virology 361 1 (2007) 212-228
28. Pugach P., Ray N., Klasse P.J., Ketas T.J., Michael E., Doms R.W., Lee B., and Moore J.P. Inefficient entry of vicriviroc-resistant HIV-1 via the inhibitor-CCR5 complex at low cell surface CCR5 densities. Virology 387 2 (2009) 296-302
29. Rizzuto C., and Sodroski J. Fine definition of a conserved CCR5-binding region on the human immunodeficiency virus type 1 glycoprotein 120. AIDS Res. Hum. Retroviruses 16 8 (2000) 741-749
30. Rizzuto C.D., Wyatt R., Hernandez-Ramos N., Sun Y., Kwong P.D., Hendrickson W.A., and Sodroski J. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280 5371 (1998) 1949-1953
31. Schurmann D., Fatkenheuer G., Reynes J., Michelet C., Raffi F., van Lier J., Caceres M., Keung A., Sansone-Parsons A., Dunkle L.M., and Hoffmann C. Antiviral activity, pharmacokinetics and safety of vicriviroc, an oral CCR5 antagonist, during 14-day monotherapy in HIV-infected adults. Aids 21 10 (2007) 1293-1299
32. Seibert C., Ying W., Gavrilov S., Tsamis F., Kuhmann S.E., Palani A., Tagat J.R., Clader J.W., McCombie S.W., Baroudy B.M., Smith S.O., Dragic T., Moore J.P., and Sakmar T.P. Interaction of small molecule inhibitors of HIV-1 entry with CCR5. Virology 349 1 (2006) 41-54
33. Tsamis F., Gavrilov S., Kajumo F., Seibert C., Kuhmann S., Ketas T., Trkola A., Palani A., Clader J.W., Tagat J.R., McCombie S., Baroudy B., Moore J.P., Sakmar T.P., and Dragic T. Analysis of the mechanism by which the small-molecule CCR5 antagonists SCH-351125 and SCH-350581 inhibit human immunodeficiency virus type 1 entry. J. Virol. 77 9 (2003) 5201-5208
34. Tsibris A.M., Sagar M., Gulick R.M., Su Z., Hughes M., Greaves W., Subramanian M., Flexner C., Giguel F., Leopold K.E., Coakley E., and Kuritzkes D.R. In vivo emergence of vicriviroc resistance in a human immunodeficiency virus type 1 subtype C-infected subject. J. Virol. 82 16 (2008) 8210-8214
35. Westby M., Smith-Burchnell C., Mori J., Lewis M., Mosley M., Stockdale M., Dorr P., Ciaramella G., and 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. 81 5 (2007) 2359-2371
36. Whitcomb J.M., Huang W., Fransen S., Limoli K., Toma J., Wrin T., Chappey C., Kiss L.D., Paxinos E.E., and Petropoulos C.J. Development and characterization of a novel single-cycle recombinant-virus assay to determine human immunodeficiency virus type 1 coreceptor tropism. Antimicrob. Agents Chemother. 51 2 (2007) 566-575
37. Wu L., Gerard N.P., Wyatt R., Choe H., Parolin C., Ruffing N., Borsetti A., Cardoso A.A., Desjardin E., Newman W., Gerard C., and Sodroski J. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 384 6605 (1996) 179-183
38. Wu L., LaRosa G., Kassam N., Gordon C.J., Heath H., Ruffing N., Chen H., Humblias J., Samson M., Parmentier M., Moore J.P., and Mackay C.R. Interaction of chemokine receptor CCR5 with its ligands: multiple domains for HIV-1 gp120 binding and a single domain for chemokine binding. J. Exp. Med. 186 8 (1997) 1373-1381
39. Wyatt R., Kwong P.D., Desjardins E., Sweet R.W., Robinson J., Hendrickson W.A., and Sodroski J.G. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393 6686 (1998) 705-711
40. Wyatt R., and Sodroski J. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 5371 (1998) 1884-1888