Kinetic mechanism for HIV-1 neutralization by antibody 2G12 entails reversible glycan binding that slows cell entry

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 20, 2012, Pages 7829-7834

  Platt, Emily J ^a   Gomes, Michelle M ^a   Kabat, David ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; GLYCAN; GLYCOPROTEIN GP 120; MANNOSE; NEUTRALIZING ANTIBODY; TYROSINE SULFATE;

ADSORPTION; ANTIGEN BINDING; ARTICLE; CATALYSIS; CELL JUNCTION; COMPLEX FORMATION; DISSOCIATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; VIRION; VIRUS ACTIVATION; VIRUS REPLICATION;

ANTIBODIES, MONOCLONAL; ANTIBODIES, NEUTRALIZING; CRYSTALLOGRAPHY; HELA CELLS; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; KINETICS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; PROTEIN BINDING; VIRUS INTERNALIZATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84861208332     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1109728109     Document Type: Article

References (41)

1. Pantophlet R, Burton DR (2006) GP120: Target for neutralizing HIV-1 antibodies. Annu Rev Immunol 24:739-769.
2. Pejchal R, et al. (2011) A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334:1097-1103.
3. Tang H, et al. (2011) Epitopes immediately below the base of the V3 loop of gp120 as targets for the initial autologous neutralizing antibody response in two HIV-1 subtype B-infected individuals. J Virol 85:9286-9299.
4. Walker LM, et al.; Protocol G Principal Investigators (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477:466-470.
5. Brower ET, Schön A, Klein JC, Freire E (2009) Binding thermodynamics of the N-terminal peptide of the CCR5 coreceptor to HIV-1 envelope glycoprotein gp120. Biochemistry 48:779-785.
6. Trkola A, et al. (1996) CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384:184-187. (Pubitemid 26386476)
7. Beirnaert E, De Zutter S, Janssens W, van der Groen G (2001) Potent broad cross-neutralizing sera inhibit attachment of primary HIV-1 isolates (groups M and O) to peripheral blood mononuclear cells. Virology 281:305-314. (Pubitemid 32881146)
8. Klasse PJ, Sattentau QJ (2002) Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J Gen Virol 83:2091-2108. (Pubitemid 34993714)
9. Ruprecht CR, et al. (2011) MPER-specific antibodies induce gp120 shedding and irreversibly neutralize HIV-1. J Exp Med 208:439-454.
10. Ugolini S, et al. (1997) Inhibition of virus attachment to CD4+ target cells is a major mechanism of T cell line-adapted HIV-1 neutralization. J Exp Med 186:1287-1298. (Pubitemid 27469024)
11. Fenyö EM, et al. (2009) International network for comparison of HIV neutralization assays: The NeutNet report. PLoS ONE 4:e4505.
12. Mann AM, et al. (2009) HIV sensitivity to neutralization is determined by target and virus producer cell properties. AIDS 23:1659-1667.
13. Polonis VR, et al. (2008) Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of the antibody response to infection and vaccination. Virology 375:315-320.
14. Eckert DM, Kim PS (2001) Mechanisms of viral membrane fusion and its inhibition. Annu Rev Biochem 70:777-810. (Pubitemid 32662225)
15. Pancera M, et al. (2010) Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc Natl Acad Sci USA 107:1166-1171.
16. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455:109-113.
17. Moscoso CG, et al. (2011) Quaternary structures of HIV Env immunogen exhibit conformational vicissitudes and interface diminution elicited by ligand binding. Proc Natl Acad Sci USA 108:6091-6096.
18. Platt EJ, Durnin JP, Shinde U, Kabat D (2007) An allosteric rheostat in HIV-1 gp120 reduces CCR5 stoichiometry required for membrane fusion and overcomes diverse entry limitations. J Mol Biol 374:64-79. (Pubitemid 47600236)
19. Xiang SH, et al. (2010) A V3 loop-dependent gp120 element disrupted by CD4 binding stabilizes the human immunodeficiency virus envelope glycoprotein trimer. J Virol 84:3147-3161.
20. Wei X, et al. (2003) Antibody neutralization and escape by HIV-1. Nature 422:307-312. (Pubitemid 36378357)
21. Platt EJ, Wehrly K, Kuhmann SE, Chesebro B, Kabat D (1998) Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J Virol 72:2855-2864. (Pubitemid 28175522)
22. Wei X, et al. (2002) Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob Agents Chemother 46:1896-1905. (Pubitemid 34535213)
23. Platt EJ, Bilska M, Kozak SL, Kabat D, Montefiori DC (2009) Evidence that ecotropic murine leukemia virus contamination in TZM-bl cells does not affect the outcome of neutralizing antibody assays with human immunodeficiency virus type 1. J Virol 83:8289-8292.
24. Platt EJ, Kozak SL, Durnin JP, Hope TJ, Kabat D (2010) Rapid dissociation of HIV-1 from cultured cells severely limits infectivity assays, causes the inactivation ascribed to entry inhibitors, and masks the inherently high level of infectivity of virions. J Virol 84:3106-3110.
25. Platt EJ, Durnin JP, Kabat D (2005) Kinetic factors control efficiencies of cell entry, efficacies of entry inhibitors, and mechanisms of adaptation of human immunodeficiency virus. J Virol 79:4347-4356. (Pubitemid 40388372)
26. Losier M, Fortin JF, Cantin R, Bergeron MG, Tremblay MJL (2003) Virion-bound ICAM-1 and activated LFA-1: A combination of factors conferring resistance to neutralization by sera from human immunodeficiency virus type 1-infected individuals independently of the disease status and phase. Clin Immunol 108:111-118. (Pubitemid 36960073)
27. Ugolini S, Mondor I, Sattentau QJ (1999) HIV-1 attachment: Another look. Trends Microbiol 7:144-149. (Pubitemid 29229899)
28. Rizzuto CD, Sodroski JG (1997) Contribution of virion ICAM-1 to human immunodeficiency virus infectivity and sensitivity to neutralization. J Virol 71:4847-4851. (Pubitemid 27204183)
29. Calarese DA, et al. (2003) Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300:2065-2071. (Pubitemid 36760127)
30. Scanlan CN, et al. (2002) The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of alpha1->2 mannose residues on the outer face of gp120. J Virol 76:7306-7321.
31. Hessell AJ, et al. (2009) Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog 5:e1000433.
32. Trkola A, et al. (2005) Delay of HIV-1 rebound after cessation of antiretroviral therapy through passive transfer of human neutralizing antibodies. Nat Med 11:615-622. (Pubitemid 40868301)
33. Poignard P, et al. (2003) Heterogeneity of envelope molecules expressed on primary human immunodeficiency virus type 1 particles as probed by the binding of neutralizing and nonneutralizing antibodies. J Virol 77:353-365. (Pubitemid 36004975)
34. Siciliano SJ, et al. (1999) A critical site in the core of the CCR5 chemokine receptor required for binding and infectivity of human immunodeficiency virus type 1. J Biol Chem 274:1905-1913.
35. Reeves JD, et al. (2002) Sensitivity of HIV-1 to entry inhibitors correlates with envelope/ coreceptor affinity, receptor density, and fusion kinetics. Proc Natl Acad Sci USA 99:16249-16254. (Pubitemid 35462781)
36. Farzan M, et al. (2002) Tyrosine-sulfated peptides functionally reconstitute a CCR5 variant lacking a critical amino-terminal region. J Biol Chem 277:40397-40402. (Pubitemid 35215614)
37. Huang CC, et al. (2007) Structures of the CCR5 N terminus and of a tyrosine-sulfated antibody with HIV-1 gp120 and CD4. Science 317:1930-1934.
38. Chaillon A, et al. (2011) The V1V2 domain and an N-linked glycosylation site in the V3 loop of the HIV-1 envelope glycoprotein modulate neutralization sensitivity to the human broadly neutralizing antibody 2G12. J Virol 85:3642-3648.
39. Walker LM, et al. (2011) Rapid development of glycan-specific, broad, and potent anti-HIV-1 gp120 neutralizing antibodies in an R5 SIV/HIV chimeric virus infected macaque. Proc Natl Acad Sci USA 108:20125-20129.
40. Balazs AB, et al. (2012) Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature 481:81-84.
41. Parren PW, et al. (2001) Antibody protects macaques against vaginal challenge with a pathogenic R5 simian/human immunodeficiency virus at serum levels giving complete neutralization in vitro. J Virol 75:8340-8347. (Pubitemid 32743706)