Effects of sequence changes in the HIV-1 gp41 fusion peptide on CCR5 inhibitor resistance

Virology

Volumn 428, Issue 2, 2012, Pages 86-97

  Anastassopoulou, Cleo G ^a   Ketas, Thomas J ^a   Sanders, Rogier W ^a,b   Johan Klasse, Per ^a   Moore, John P ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

CCR5 coreceptor; Entry inhibitors; Escape mutants; Gp120 inner domain; Gp41; Vicriviroc

Indexed keywords

CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 41; VICRIVIROC;

ANTIVIRAL RESISTANCE; ARTICLE; BINDING AFFINITY; CELL TYPE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG RECEPTOR BINDING; HUMAN IMMUNODEFICIENCY VIRUS 1; IC 50; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; VIRUS ENTRY; VIRUS MUTATION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; CELL LINE; DRUG RESISTANCE, VIRAL; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PIPERAZINES; PYRIMIDINES; RECEPTORS, CCR5; SEQUENCE ALIGNMENT;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84860837386     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.03.008     Document Type: Article

References (38)

1. Anastassopoulou C.G., Ketas T.J., Depetris R.S., Thomas A.M., Klasse P.J., Moore J.P. Resistance of a human immunodeficiency virus type 1 isolate to a small molecule CCR5 inhibitor can involve sequence changes in both gp120 and gp41. Virology 2011, 413(1):47-59.
2. Anastassopoulou C.G., Ketas T.J., Klasse P.J., Moore J.P. Resistance to CCR5 inhibitors caused by sequence changes in the fusion peptide of HIV-1 gp41. Proc. Natl. Acad. Sci. USA 2009, 106(13):5318-5323.
3. Anastassopoulou C.G., Marozsan A.J., Matet A., Snyder A.D., Arts E.J., Kuhmann S.E., Moore J.P. Escape of HIV-1 from a small molecule CCR5 inhibitor is not associated with a fitness loss. PLoS Pathog. 2007, 3(6):e79.
4. Baba M., Miyake H., Wang X., Okamoto M., Takashima K. Isolation and characterization of human immunodeficiency virus type 1 resistant to the small-molecule CCR5 antagonist TAK-652. Antimicrob. Agents Chemother. 2007, 51(2):707-715.
5. Berro R., Klasse P.J., Lascano D., Flegler A., Nagashima K.A., Sanders R.W., Sakmar T.P., Hope T.J., Moore J.P. Multiple CCR5 conformations on the cell surface are used differentially by human immunodeficiency viruses resistant or sensitive to CCR5 inhibitors. J. Virol. 2011, 85(16):8227-8240.
6. Berro R., Klasse P.J., Jakobsen M.R., Gorry P.R., Moore J.P., Sanders R.W. V3 determinants of HIV-1 escape from the CCR5 inhibitors Maraviroc and Vicriviroc. Virology 2012, 427(2):158-165.
7. Berro R., Sanders R.W., Lu M., Klasse P.J., Moore J.P. Two HIV-1 variants resistant to small molecule CCR5 inhibitors differ in how they use CCR5 for entry. PLoS Pathog. 2009, 5(8):e1000548.
8. Coetzer M., Cilliers T., Papathanasopoulos M., Ramjee G., Karim S.A., Williamson C., Morris L. Longitudinal analysis of HIV type 1 subtype C envelope sequences from South Africa. AIDS Res. Hum. Retroviruses 2007, 23(2):316-321.
9. Finzi A., Xiang S.H., Pacheco B., Wang L., Haight J., Kassa A., Danek B., Pancera M., Kwong P.D., Sodroski J. Topological layers in the HIV-1 gp120 inner domain regulate gp41 interaction and CD4-triggered conformational transitions. Mol. Cell 2010, 37(5):656-667.
10. Forssmann W.G., Stoll Y.H., Adermann M., Albrecht K., Barlos U., Busmann K., Canales-Mayordomo A., Gimenez-Gallego A., Hirsch G., Jimenez-Barbero J., Meyer-Olson J., Munch D., Perez-Castells J., Standker J., Kirchhoff L., Schmidt, R.E.F. Short-term monotherapy in HIV-infected patients with a virus entry inhibitor against the gp41 fusion peptide. Sci. Transl. Med. 2010, 2(63). 63re63.
11. Gonzalez E., Ballana E., Clotet B., Este J.A. Development of resistance to VIR-353 with cross-resistance to the natural HIV-1 entry virus inhibitory peptide (VIRIP). AIDS 2011, 25(13):1557-1583.
12. Gonzalez-Ortega E., Ballana E., Badia R., Clotet B., Este J.A. Compensatory mutations rescue the virus replicative capacity of VIRIP-resistant HIV-1. Antivir. Res. 2011, 92(3):479-483.
13. Hartley O., Klasse P.J., Sattentau Q.J., Moore J.P. V3: HIV's switch-hitter. AIDS Res. Hum. Retroviruses 2005, 21(2):171-189.
14. Helseth E., Olshevsky U., Furman C., Sodroski J. Human immunodeficiency virus type 1 gp120 envelope glycoprotein regions important for association with the gp41 transmembrane glycoprotein. J. Virol. 1991, 65(4):2119-2123.
15. Huang W., Toma J., Fransen S., Stawiski E., Reeves J.D., Whitcomb J.M., Parkin N., Petropoulos C.J. Coreceptor tropism can be influenced by amino acid substitutions in the gp41 transmembrane subunit of human immunodeficiency virus type 1 envelope protein. J. Virol. 2008, 82(11):5584-5593.
16. Ketas T.J., Holuigue S., Matthews K., Moore J.P., Klasse P.J. Env-glycoprotein heterogeneity as a source of apparent synergy and enhanced cooperativity in inhibition of HIV-1 infection by neutralizing antibodies and entry inhibitors. Virology 2012, 422(1):22-36.
17. Ketas T.J., Kuhmann S.E., Palmer A., Zurita J., He W., Ahuja S.K., Klasse P.J., Moore J.P. Cell surface expression of CCR5 and other host factors influence the inhibition of HIV-1 infection of human lymphocytes by CCR5 ligands. Virology 2007, 364(2):281-290.
18. Kitrinos K.M., Amrine-Madsen H., Irlbeck D.M., Word J.M., Demarest J.F. Virologic failure in therapy-naive subjects on aplaviroc plus lopinavir-ritonavir: detection of aplaviroc resistance requires clonal analysis of envelope. Antimicrob. Agents Chemother. 2009, 53(3):1124-1131.
19. Klasse P.J. Modeling how many envelope glycoprotein trimers per virion participate in human immunodeficiency virus infectivity and its neutralization by antibody. Virology 2007, 369(2):245-262.
20. Kuhmann S.E., Hartley O. Targeting chemokine receptors in HIV: a status report. Annu. Rev. Pharmacol. Toxicol. 2008, 48:425-461.
21. Kuhmann S.E., Pugach P., Kunstman K.J., Taylor J., Stanfield R.L., Snyder A., Strizki J.M., Riley J., Baroudy B.M., Wilson I.A., Korber B.T., Wolinsky S.M., Moore J.P. Genetic and phenotypic analyses of human immunodeficiency virus type 1 escape from a small-molecule CCR5 inhibitor. J. Virol. 2004, 78(6):2790-2807.
22. 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., Doms R.W. V3 loop truncations in HIV-1 envelope impart resistance to coreceptor inhibitors and enhanced sensitivity to neutralizing antibodies. PLoS Pathog. 2007, 3(8):e117.
23. MacArthur R.D., Novak R.M. Reviews of anti-infective agents: maraviroc: the first of a new class of antiretroviral agents. Clin. Infect. Dis. 2008, 47(2):236-241.
24. Marozsan A.J., Kuhmann S.E., Morgan T., Herrera C., Rivera-Troche E., Xu S., Baroudy B.M., Strizki J., 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 2005, 338(1):182-199.
25. Moore J.P., Kuritzkes D.R. A piece de resistance: how HIV-1 escapes small molecule CCR5 inhibitors. Curr. Opin. HIV AIDS 2009, 4(2):118-124.
26. Munch J., Standker L., Adermann K., Schulz A., Schindler M., Chinnadurai R., Pohlmann S., Chaipan C., Biet T., Peters T., Meyer B., Wilhelm D., Lu H., Jing W., Jiang S., Forssmann W.G., Kirchhoff F. Discovery and optimization of a natural HIV-1 entry inhibitor targeting the gp41 fusion peptide. Cell 2007, 129(2):263-275.
27. Ogert R.A., Hou Y., Ba L., Wojcik L., Qiu P., Murgolo N., Duca J., Dunkle L.M., Ralston R., Howe J.A. 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 2010, 400(1):145-155.
28. Ogert R.A., Wojcik L., Buontempo C., Ba L., Buontempo P., Ralston R., Strizki J., 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 2008, 373(2):387-399.
29. Pancera M., Majeed S., Ban Y.E., Chen L., Huang C.C., Kong L., Kwon Y.D., Stuckey J., Zhou T., Robinson J.E., Schief W.R., Sodroski J., Wyatt R., Kwong P.D. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl. Acad. Sci. USA 2010, 107(3):1166-1171.
30. Pugach P., Marozsan A.J., Ketas T.J., Landes E.L., Moore J.P., Kuhmann S.E. HIV-1 clones resistant to a small molecule CCR5 inhibitor use the inhibitor-bound form of CCR5 for entry. Virology 2007, 361(1):212-228.
31. Putcharoen O., Lee S.H., Henrich T.J., Hu Z., Vanichanan J., Coakley E., Greaves W., Gulick R.M., Kuritzkes D.R., Tsibris A.M. HIV-1 clinical isolates resistant to CCR5 antagonists exhibit delayed entry kinetics that are corrected in the presence of drug. J. Virol. 2012, 86(2):1119-1128.
32. Roche M., Jakobsen M.R., Ellett A., Salimiseyedabad H., Jubb B., Westby M., Lee B., Lewin S.R., Churchill M.J., Gorry P.R. 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.
33. Trkola A., Kuhmann S.E., Strizki J.M., Maxwell E., Ketas T., Morgan T., Pugach P., Xu S., Wojcik L., Tagat J., Palani A., Shapiro S., Clader J.W., McCombie S., Reyes G.R., Baroudy B.M., Moore J.P. HIV-1 escape from a small molecule, CCR5-specific entry inhibitor does not involve CXCR4 use. Proc. Natl. Acad. Sci. USA 2002, 99(1):395-400.
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., Kuritzkes D.R. In vivo emergence of vicriviroc resistance in a human immunodeficiency virus type 1 subtype C-infected subject. J. Virol. 2008, 82(16):8210-8214.
35. Westby M., Lewis M., Whitcomb J., Youle M., Pozniak A.L., James I.T., Jenkins T.M., Perros M., van der Ryst E. Emergence of CXCR4-using human immunodeficiency virus type 1 (HIV-1) variants in a minority of HIV-1-infected patients following treatment with the CCR5 antagonist maraviroc is from a pretreatment CXCR4-using virus reservoir. J. Virol. 2006, 80(10):4909-4920.
36. 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(5):2359-2371.
37. Wood N., Bhattacharya T., Keele B.F., Giorgi E., Liu M., Gaschen B., Daniels M., Ferrari G., Haynes B.F., McMichael A., Shaw G.M., Hahn B.H., Korber B., Seoighe C. HIV evolution in early infection: selection pressures, patterns of insertion and deletion, and the impact of APOBEC. PLoS Pathog. 2009, 5(5):e1000414.
38. Yang X., Mahony E., Holm G.H., Kassa A., Sodroski J. Role of the gp120 inner domain beta-sandwich in the interaction between the human immunodeficiency virus envelope glycoprotein subunits. Virology 2003, 313(1):117-125.