Mechanisms of HIV-1 subtype C resistance to GRFT, CV-N and SVN

Virology

Volumn 446, Issue 1-2, 2013, Pages 66-76

  Alexandre, Kabamba B ^a,b   Moore, Penny L ^a,b   Nonyane, Molati ^a   Gray, Elin S ^a   Ranchobe, Nthabeleng ^a   Chakauya, Ereck ^c   McMahon, James B ^d   O'Keefe, Barry R ^d   Chikwamba, Rachel ^c   Morris, Lynn ^a,b  

^a NATIONAL INSTITUTE FOR COMMUNICABLE DISEASES   (South Africa)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^c DSI CSIR Nanotechnology Innovation Centre   (South Africa)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cyanovirin N; Entry inhibitor; Glycans; Griffithsin; HIV subtype C; Microbicide; Resistance; Scytovirin; Single genome amplification

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; GLYCAN; GLYCOPROTEIN GP 120; LECTIN; MANNOSE; MANNOSE RICH GLYCAN; PROTEIN INHIBITOR; SOLUBLE CD4 ANTIGEN; UNCLASSIFIED DRUG;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE DELETION; GENE INSERTION; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 C; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIRUS CULTURE; VIRUS INHIBITION; VIRUS ISOLATION; VIRUS RESISTANCE; VIRUS STRAIN;

CYANOVIRIN-N; ENTRY INHIBITOR; GLYCANS; GRIFFITHSIN; HIV SUBTYPE C; MICROBICIDE; RESISTANCE; SCYTOVIRIN; SINGLE GENOME AMPLIFICATION;

ANTIVIRAL AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; CELL LINE; DRUG RESISTANCE, VIRAL; DRUG TOLERANCE; GLYCOSYLATION; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; INHIBITORY CONCENTRATION 50; LECTINS; MICROBIAL SENSITIVITY TESTS; MUTANT PROTEINS; MUTATION, MISSENSE; PLANT LECTINS; SEQUENCE ANALYSIS, DNA; SERIAL PASSAGE;

EID: 84884566724     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.07.019     Document Type: Article

References (54)

1. Alexandre K.B., Gray E.S., Lambson B.E., Moore P.L., Choge I.A., Mlisana K., Karim S.S., McMahon J., O'Keefe B., Chikwamba R., Morris L. Mannose-rich glycosylation patterns on HIV-1 subtype C gp120 and sensitivity to the lectins, Griffithsin, Cyanovirin-N and Scytovirin. Virology 2010, 402:187-196.
2. Alexandre K.B., Gray E.S., Pantophlet R., Moore P.L., McMahon J.B., Chakauya E., O'Keefe B.R., Chikwamba R., Morris L. Binding of the mannose-specific lectin, griffithsin, to HIV-1 gp120 exposes the CD4-binding site. J. Virol. 2011, 85:9039-9050.
3. Balzarini J. Targeting the glycans of gp120: a novel approach aimed at the Achilles heel of HIV. Lancet Infect. Dis. 2005, 5:726-731.
4. Balzarini J., Van Laethem K., Hatse S., Froeyen M., Van Damme E., Bolmstedt A., Peumans W., De Clercq E., Schols D. Marked depletion of glycosylation sites in HIV-1 gp120 under selection pressure by the mannose-specific plant lectins of Hippeastrum hybrid and Galanthus nivalis. Mol. Pharmacol. 2005, 67:1556-1565.
5. Balzarini J., Van Laethem K., Hatse S., Vermeire K., De Clercq E., Peumans W., Van Damme E., Vandamme A.M., Bolmstedt A., Schols D. Profile of resistance of human immunodeficiency virus to mannose-specific plant lectins. J. Virol. 2004, 78:10617-10627.
6. Balzarini J., Van Laethem K., Peumans W.J., Van Damme E.J., Bolmstedt A., Gago F., Schols D. Mutational pathways, resistance profile, and side effects of cyanovirin relative to human immunodeficiency virus type 1 strains with N-glycan deletions in their gp120 envelopes. J. Virol. 2006, 80:8411-8421.
7. Binley J.M., Wrin T., Korber B., Zwick M.B., Wang M., Chappey C., Stiegler G., Kunert R., Zolla-Pazner S., Katinger H., Petropoulos C.J., Burton D.R. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 2004, 78:13232-13252.
8. Bokesch H.R., O'Keefe B.R., McKee T.C., Pannell L.K., Patterson G.M., Gardella R.S., Sowder R.C., Turpin J., Watson K., Buckheit R.W., Boyd M.R. A potent novel anti-HIV protein from the cultured cyanobacterium Scytonema varium. Biochemistry 2003, 42:2578-2584.
9. Bonomelli, C., Doores, K.J., Dunlop, D.C., Thaney, V., Dwek, R.A., Burton, D.R., Crispin, M., Scanlan, C.N., 2011. The glycan shield of HIV is predominantly oligomannose independently of production system or viral clade. PLoS One 6, e23521.
10. Boyd M.R., Gustafson K.R., McMahon J.B., Shoemaker R.H., O'Keefe B.R., Mori T., Gulakowski R.J., Wu L., Rivera M.I., Laurencot C.M., Currens M.J., Cardellina J.H., Buckheit R.W., Nara P.L., Pannell L.K., Sowder R.C., Henderson L.E. Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob. Agents Chemother. 1997, 41:1521-1530.
11. Bures R., Gaitan A., Zhu T., Graziosi C., McGrath K.M., Tartaglia J., Caudrelier P., El Habib R., Klein M., Lazzarin A., Stablein D.M., Deers M., Corey L., Greenberg M.L., Schwartz D.H., Montefiori D.C. Immunization with recombinant canarypox vectors expressing membrane-anchored glycoprotein 120 followed by glycoprotein 160 boosting fails to generate antibodies that neutralize R5 primary isolates of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 2000, 16:2019-2035.
12. Bures R., Morris L., Williamson C., Ramjee G., Deers M., Fiscus S.A., Abdool-Karim S., Montefiori D.C. Regional clustering of shared neutralization determinants on primary isolates of clade C human immunodeficiency virus type 1 from South Africa. J. Virol. 2002, 76:2233-2244.
13. Chen H., Xu X., Bishop A., Jones I.M. Reintroduction of the 2G12 epitope in an HIV-1 clade C gp120. Aids 2005, 19:833-835.
14. Choge I., Cilliers T., Walker P., Taylor N., Phoswa M., Meyers T., Viljoen J., Violari A., Gray G., Moore P.L., Papathanosopoulos M., Morris L. Genotypic and phenotypic characterization of viral isolates from HIV-1 subtype C-infected children with slow and rapid disease progression. AIDS Res. Hum. Retroviruses 2006, 22:458-465.
15. Cilliers T., Nhlapo J., Coetzer M., Orlovic D., Ketas T., Olson W.C., Moore J.P., Trkola A., Morris L. The CCR5 and CXCR4 coreceptors are both used by human immunodeficiency virus type 1 primary isolates from subtype C. J. Virol. 2003, 77:4449-4456.
16. 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, 23:316-321.
17. Coetzer M., Nedellec R., Cilliers T., Meyers T., Morris L., Mosier D.E. Extreme genetic divergence is required for coreceptor switching in HIV-1 subtype C. J. Acquir. Immune Defic. Syndr. 2011, 56:9-15.
18. Doores, K.J., Bonomelli, C., Harvey, D.J., Vasiljevic, S., Dwek, R.A., Burton, D.R., Crispin, M., Scanlan, C.N., 2010. Envelope glycans of immunodeficiency virions are almost entirely oligomannose antigens. Proc. Natl. Acad. Sci. USA 107, pp. 13800-13805.
19. Fenyo E.M., Heath A., Dispinseri S., Holmes H., Lusso P., Zolla-Pazner S., Donners H., Heyndrickx L., Alcami J., Bongertz V., Jassoy C., Malnati M., Montefiori D., Moog C., Morris L., Osmanov S., Polonis V., Sattentau Q., Schuitemaker H., Sutthent R., Wrin T., Scarlatti G. International network for comparison of HIV neutralization assays: the NeutNet report. PLoS One 2009, 4:e4505.
20. Ferir G., Huskens D., Palmer K.E., Boudreaux D.M., Swanson M.D., Markovitz D.M., Balzarini J., Schols D. Combinations of griffithsin with other carbohydrate-binding agents demonstrate superior activity against HIV Type 1, HIV Type 2, and selected carbohydrate-binding agent-resistant HIV Type 1 strains. AIDS Res. Hum. Retroviruses 2012, 28:1513-1523.
21. Geijtenbeek T.B., Gringhuis S.I. Signalling through C-type lectin receptors: shaping immune responses. Nat. Rev. Immunol. 2009, 9:465-479.
22. Gray E.S., Moore P.L., Pantophlet R.A., Morris L. N-linked glycan modifications in gp120 of human immunodeficiency virus type 1 subtype C render partial sensitivity to 2G12 antibody neutralization. J. Virol. 2007, 81:10769-10776.
23. Hu Q., Mahmood N., Shattock R.J. High-mannose-specific deglycosylation of HIV-1 gp120 induced by resistance to cyanovirin-N and the impact on antibody neutralization. Virology 2007, 368:145-154.
24. Huang X., Jin W., Griffin G.E., Shattock R.J., Hu Q. Removal of two high-mannose N-linked glycans on gp120 renders human immunodeficiency virus 1 largely resistant to the carbohydrate-binding agent griffithsin. J. Gen. Virol. 2011, 92:2367-2373.
25. Johnson V.A., Byington R.E. Quantitative assays for virus infectivity. Tech. HIV Res. 1990, 71-76. Stockton Press, New York. A. Aldovini, B.D. Walker (Eds.).
26. Kwong P.D., Wyatt R., Robinson J., Sweet R.W., Sodroski J., Hendrickson W.A. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 1998, 393:648-659.
27. Leonard C.K., Spellman M.W., Riddle L., Harris R.J., Thomas J.N., Gregory T.J. Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J. Biol. Chem. 1990, 265:10373-10382.
28. Li Y., Luo L., Rasool N., Kang C.Y. Glycosylation is necessary for the correct folding of human immunodeficiency virus gp120 in CD4 binding. J. Virol. 1993, 67:584-588.
29. Li Y., O'Dell S., Walker L.M., Wu X., Guenaga J., Feng Y., Schmidt S.D., McKee K., Louder M.K., Ledgerwood J.E., Graham B.S., Haynes B.F., Burton D.R., Wyatt R.T., Mascola J.R. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 2011, 85:8954-8967.
30. Lin G., Simmons G., Pohlmann S., Baribaud F., Ni H., Leslie G.J., Haggarty B.S., Bates P., Weissman D., Hoxie J.A., Doms R.W. Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR. J. Virol. 2003, 77:1337-1346.
31. Liu Y., Liu H., Kim B.O., Gattone V.H., Li J., Nath A., Blum J., He J.J. CD4-independent infection of astrocytes by human immunodeficiency virus type 1: requirement for the human mannose receptor. J. Virol. 2004, 78:4120-4133.
32. Losman B., Bolmstedt A., Schonning K., Bjorndal A., Westin C., Fenyo E.M., Olofsson S. Protection of neutralization epitopes in the V3 loop of oligomeric human immunodeficiency virus type 1 glycoprotein 120 by N-linked oligosaccharides in the V1 region. AIDS Res. Hum. Retroviruses 2001, 17:1067-1076.
33. Lue J., Hsu M., Yang D., Marx P., Chen Z., Cheng-Mayer C. Addition of a single gp120 glycan confers increased binding to dendritic cell-specific ICAM-3-grabbing nonintegrin and neutralization escape to human immunodeficiency virus type 1. J. Virol. 2002, 76:10299-10306.
34. Manrique A., Rusert P., Joos B., Fischer M., Kuster H., Leemann C., Niederost B., Weber R., Stiegler G., Katinger H., Gunthard H.F., Trkola A. In vivo and in vitro escape from neutralizing antibodies 2G12, 2F5, and 4E10. J. Virol. 2007, 81:8793-8808.
35. McCaffrey R.A., Saunders C., Hensel M., Stamatatos L. N-linked glycosylation of the V3 loop and the immunologically silent face of gp120 protects human immunodeficiency virus type 1 SF162 from neutralization by anti-gp120 and anti-gp41 antibodies. J. Virol. 2004, 78:3279-3295.
36. Montefiori D.C. Evaluating neutralizing antibodies againts HIV, SIV and SHIV in luciferase reporter gene assays. Current Protocols in Immunology 2004, 12.11.11-12.11.15. John Wiley & Sons. J.E. Coligan, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, W. Strober, R. Coico (Eds.).
37. Mori T., O'Keefe B.R., Sowder R.C., Bringans S., Gardella R., Berg S., Cochran P., Turpin J.A., Buckheit R.W., McMahon J.B., Boyd M.R. Isolation and characterization of griffithsin, a novel HIV-inactivating protein, from the red alga Griffithsia sp. J. Biol. Chem. 2005, 280:9345-9353.
38. Moulaei T., Botos I., Ziolkowska N.E., Bokesch H.R., Krumpe L.R., McKee T.C., O'Keefe B.R., Dauter Z., Wlodawer A. Atomic-resolution crystal structure of the antiviral lectin scytovirin. Protein Sci. 2007, 16:2756-2760.
39. Moulaei T., Shenoy S.R., Giomarelli B., Thomas C., McMahon J.B., Dauter Z., O'Keefe B.R., Wlodawer A. Monomerization of viral entry inhibitor griffithsin elucidates the relationship between multivalent binding to carbohydrates and anti-HIV activity. Structure 2010, 18:1104-1115.
40. O'Keefe B.R., Vojdani F., Buffa V., Shattock R.J., Montefiori D.C., Bakke J., Mirsalis J., d'Andrea A.L., Hume S.D., Bratcher B., Saucedo C.J., McMahon J.B., Pogue G.P., Palmer K.E. Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl. Acad. Sci. USA 2009, 106:6099-6104.
41. Salazar-Gonzalez J.F., Bailes E., Pham K.T., Salazar M.G., Guffey M.B., Keele B.F., Derdeyn C.A., Farmer P., Hunter E., Allen S., Manigart O., Mulenga J., Anderson J.A., Swanstrom R., Haynes B.F., Athreya G.S., Korber B.T., Sharp P.M., Shaw G.M., Hahn B.H. Deciphering human immunodeficiency virus type 1 transmission and early envelope diversification by single-genome amplification and sequencing. J. Virol. 2008, 82:3952-3970.
42. Tsai C.C., Emau P., Jiang Y., Agy M.B., Shattock R.J., Schmidt A., Morton W.R., Gustafson K.R., Boyd M.R. Cyanovirin-N inhibits AIDS virus infections in vaginal transmission models. AIDS Res. Hum. Retroviruses 2004, 20:11-18.
43. Tsai C.C., Emau P., Jiang Y., Tian B., Morton W.R., Gustafson K.R., Boyd M.R. Cyanovirin-N gel as a topical microbicide prevents rectal transmission of SHIV89.6P in macaques. AIDS Res. Hum. Retroviruses 2003, 19:535-541.
44. Walker L.M., Huber M., Doores K.J., Falkowska E., Pejchal R., Julien J.P., Wang S.K., Ramos A., Chan-Hui P.Y., Moyle M., Mitcham J.L., Hammond P.W., Olsen O.A., Phung P., Fling S., Wong C.H., Phogat S., Wrin T., Simek M.D., Koff W.C., Wilson I.A., Burton D.R., Poignard P. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 2011, 477:466-470.
45. Wei X., Decker J.M., Wang S., Hui H., Kappes J.C., Wu X., Salazar-Gonzalez J.F., Salazar M.G., Kilby J.M., Saag M.S., Komarova N.L., Nowak M.A., Hahn B.H., Kwong P.D., Shaw G.M. Antibody neutralization and escape by HIV-1. Nature 2003, 422:307-312.
46. Williamson C., Morris L., Maughan M.F., Ping L.H., Dryga S.A., Thomas R., Reap E.A., Cilliers T., van Harmelen J., Pascual A., Ramjee G., Gray G., Johnston R., Karim S.A., Swanstrom R. Characterization and selection of HIV-1 subtype C isolates for use in vaccine development. AIDS Res. Hum. Retroviruses 2003, 19:133-144.
47. Witvrouw M., Fikkert V., Hantson A., Pannecouque C., O'Keefe B R., McMahon J., Stamatatos L., de Clercq E., Bolmstedt A. Resistance of human immunodeficiency virus type 1 to the high-mannose binding agents cyanovirin N and concanavalin A. J. Virol. 2005, 79:7777-7784.
48. Zhang M., Gaschen B., Blay W., Foley B., Haigwood N., Kuiken C., Korber B. Tracking global patterns of N-linked glycosylation site variation in highly variable viral glycoproteins: HIV, SIV, and HCV envelopes and influenza hemagglutinin. Glycobiology 2004, 14:1229-1246.
49. Zhou J.Y., Montefiori D.C. Antibody-mediated neutralization of primary isolates of human immunodeficiency virus type 1 in peripheral blood mononuclear cells is not affected by the initial activation state of the cells. J. Virol. 1997, 71:2512-2517.
50. Zhou T., Georgiev I., Wu X., Yang Z.Y., Dai K., Finzi A., Kwon Y.D., Scheid J.F., Shi W., Xu L., Yang Y., Zhu J., Nussenzweig M.C., Sodroski J., Shapiro L., Nabel G.J., Mascola J.R., Kwong P.D. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 2010, 329:811-817.
51. Zhou T., Xu L., Dey B., Hessell A.J., Van Ryk D., Xiang S.H., Yang X., Zhang M.Y., Zwick M.B., Arthos J., Burton D.R., Dimitrov D.S., Sodroski J., Wyatt R., Nabel G.J., Kwong P.D. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 2007, 445:732-737.
52. Zhu X., Borchers C., Bienstock R.J., Tomer K.B. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells. Biochemistry 2000, 39:11194-11204.
53. Ziolkowska N.E., O'Keefe B.R., Mori T., Zhu C., Giomarelli B., Vojdani F., Palmer K.E., McMahon J.B., Wlodawer A. Domain-swapped structure of the potent antiviral protein griffithsin and its mode of carbohydrate binding. Structure 2006, 14:1127-1135.
54. Ziolkowska N.E., Wlodawer A. Structural studies of algal lectins with anti-HIV activity. Acta Biochim. Pol. 2006, 53:617-626.