Cross-reactive human immunodeficiency virus type 1-neutralizing human monoclonal antibody that recognizes a novel conformational epitope on gp41 and lacks reactivity against self-antigens

Journal of Virology

Volumn 82, Issue 14, 2008, Pages 6869-6879

  Zhang, Mei Yun ^a,b   Vu, Bang K ^a   Choudhary, Anil ^c   Lu, Hong ^d   Humbert, Michael ^e,f   Ong, Helena ^e   Alam, Munir ^g   Ruprecht, Ruth M ^e,f   Quinnan, Gerald ^c   Jiang, Shibo ^d   Montefiori, David C ^g   Mascola, John R ^h   Broder, Christopher C ^c   Haynes, Barton F ^g   Dimitrov, Dimiter S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d NEW YORK BLOOD CENTER   (United States)

^e DANA FARBER CANCER INSTITUTE   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g DUKE UNIVERSITY MEDICAL CENTER   (United States)

^h NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; CROSS REACTING ANTIBODY; EPITOPE; GLYCOPROTEIN GP 140; GLYCOPROTEIN GP 41; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; MONOCLONAL ANTIBODY M44; MONOCLONAL ANTIBODY M46; MONOCLONAL ANTIBODY M48; MONOCLONAL ANTIBODY Z13; NEUTRALIZING ANTIBODY; PHOSPHATIDYLSERINE; VIRUS GLYCOPROTEIN; AUTOANTIGEN; DNA; GP41 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; VIRUS ANTIBODY;

ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ARTICLE; CLADISTICS; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; CELL CULTURE; CELL LINE; CROSS REACTION; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; PROTEIN BINDING; SERODIAGNOSIS; SURFACE PLASMON RESONANCE; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; REPLICATION COMPETENT VIRUSES;

ANTIBODIES, MONOCLONAL; ANTIBODIES, VIRAL; AUTOANTIGENS; CARDIOLIPINS; CELL LINE; CELLS, CULTURED; CROSS REACTIONS; DNA; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; HIV ENVELOPE PROTEIN GP41; HIV-1; HUMANS; LEUKOCYTES, MONONUCLEAR; NEUTRALIZATION TESTS; PHOSPHATIDYLSERINES; PROTEIN BINDING; SURFACE PLASMON RESONANCE;

EID: 47049130702     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00033-08     Document Type: Article

References (52)

1. Alam, S. M., M. McAdams, D. Boren, M. Rak, R. M. Scearce, F. Gao, Z. T. Camacho, D. Gewirth, G. Kelsoe, P. Chen, and B. F. Haynes. 2007. The role of antibody polyspecificity and lipid reactivity in binding of broadly neutralizing anti-HIV-1 envelope human monoclonal antibodies 2F5 and 4E10 to glycoprotein 41 membrane proximal envelope epitopes. J. Immunol. 178: 4424-4435.
2. Beck, Z., N. Karasavvas, J. Tong, G. R. Matyas, M. Rao, and C. R. Alving. 2007. Calcium modulation of monoclonal antibody binding to phosphatidyl-inositol phosphate. Biochem. Biophys. Res. Commun. 354:747-751.
3. Binley, J. M., C. S. Cayanan, C. Wiley, N. Schulke, W. C. Olson, and D. R. Burton. 2003. Redox-triggered infection by disulfide-shackled human immunodeficiency virus type 1 pseudovirions. J. Virol. 77:5678-5684.
4. Binley, J. M., T. Wrin, B. Korber, M. B. Zwick, M. Wang, C. Chappey, G. Stiegler, R. Kunert, S. Zolla-Pazner, H. Katinger, C. J. Petropoulos, and D. R. Burton. 2004. Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78:13232-13252.
5. Broder, C. C, P. L. Earl, D. Long, S. T. Abedon, B. Moss, and R. W. Doms. 1994. Antigenic implications of human immunodeficiency virus type 1 envelope quaternary structure: oligomer-specific and -sensitive monoclonal antibodies. Proc. Natl. Acad. Sci. USA 91:11699-11703.
6. Broder, C. C., P. E. Kennedy, F. Michaels, and E. A. Berger. 1994. Expression of foreign genes in cultured human primary macrophages using recombinant vaccinia virus vectors. Gene 142:167-174.
7. Brown, B. K., N. Karasawas, Z. Beck, G. R. Matyas, D. L. Birx, V. R. Polonis, and C. R. Alving. 2007. Monoclonal antibodies to phosphatidylinositol phosphate neutralize human immunodeficiency virus type 1: role of phosphate-binding subsites. J. Virol. 81:2087-2091.
8. Burton, D. R., J. Pyati, R. Koduri, S. J. Sharp, G. B. Thornton, P. W. Parren, L. S. Sawyer, R. M. Hendry, N. Dunlop, P. L. Nara, et al. 1994. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266:1024-1027.
9. Burton, D. R., E. O. Saphire, and P. W. Parren. 2001. A model for neutralization of viruses based on antibody coating of the virion surface. Curr. Top. Microbiol. Immunol. 260:109-143.
10. Choudhry, V., M. Y. Zhang, I. A. Sidorov, J. M. Louis, I. Harris, A. S. Dimitrov, P. Bouma, F. Cham, A. Choudhary, S. M. Rybak, T. Fouts, D. C. Montefiori, C. C. Broder, G. V. Quinnan, Jr., and D. S. Dimitrov. 2007. Cross-reactive HIV-1 neutralizing monoclonal antibodies selected by screening of an immune human phage library against an envelope glycoprotein (gp140) isolated from a patient (R2) with broadly HIV-1 neutralizing anti-bodies. Virology 363:79-90.
11. Coëffier, E., J. M. Clement, V. Cussac, N. Khodaei-Boorane, M. Jehanno, M. Rojas, A. Dridi, M. Latour, R. El Habib, F. Barre-Sinoussi, M. Hofnung, and C. Leclerc. 2000. Antigenicity and immunogenicity of the HIV-1 gp41 epitope ELDKWA inserted into permissive sites of the MalE protein. Vaccine 19:684-693.
12. Cotropia, J., K. E. Ugen, S. Kliks, K. Broliden, P. A. Broliden, J. A. Hoxie, V. Srikantan, W. V. Williams, and D. B. Weiner. 1996. A human monoclonal antibody to HIV-1 gp41 with neutralizing activity against diverse laboratory isolates. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 12:221-232.
13. Dimitrov, D. S. 2004. Virus entry: molecular mechanisms and biomedical applications. Nat. Rev. Microbiol. 2:109-122.
14. Dimitrov, D. S., R. L. Willey, H. Sato, L. J. Chang, R. Blumenthal, and M. A. Martin. 1993. Quantitation of human immunodeficiency virus type 1 infection kinetics. J. Virol. 67:2182-2190.
15. Dreyer, K., E. G. Kallas, V. Planelles, D. Montefiori, M. P. McDermott, M. S. Hasan, and T. G. Evans. 1999. Primary isolate neutralization by HIV type 1-infected patient sera in the era of highly active antiretroviral therapy. AIDS Res. Hum. Retrovir. 15:1563-1571.
16. Earl, P. L., C. C. Broder, R. W. Doms, and B. Moss. 1997. Epitope map of human immunodeficiency virus type 1 gp41 derived from 47 monoclonal antibodies produced by immunization with oligomeric envelope protein. J. Virol. 71:2674-2684.
17. Follis, K. E., S. J. Larson, M. Lu, and J. H. Nunberg. 2002. Genetic evidence that interhelical packing interactions in the gp41 core are critical for transition of the human immunodeficiency virus type 1 envelope glycoprotein to the fusion-active state. J. Virol. 76:7356-7362.
18. Giles, I., N. Lambrianides, N. Pattni, D. Faulkes, D. Latchman, P. Chen, S. Pierangeli, D. Isenberg, and A. Rahman. 2006. Arginine residues are important in determining the binding of human monoclonal antiphospholipid antibodies to clinically relevant antigens. J. Immunol. 177:1729-1736.
19. Gustchina, E., J. M. Louis, S. N. Lam, C. A. Bewley, and G. M. Clore. 2007. A monoclonal Fab derived from a human nonimmune phage library reveals a new epitope on gp41 and neutralizes diverse human immunodeficiency virus type 1 strains. J. Virol. 81:12946-12953.
20. Haynes, B. F., J. Fleming, E. W. St. Clair, H. Katinger, G. Stiegler, R. Kunert, J. Robinson, R. M. Scearce, K. Plonk, H. F. Staats, T. L. Ortel, H. X. Liao, and S. M. Alam. 2005. Cardiolipin polyspecific autoreactivity in two broadly neutralizing HIV-1 antibodies. Science 308:1906-1908.
21. Jacobs, A., J. Sen, L. Rong, and M. Caffrey. 2005. Alanine scanning mutants of the HIV gp41 loop. J. Biol. Chem. 280:27284-27288.
22. Jiang, S., K. Lin, and M. Lu. 1998. A conformation-specific monoclonal antibody reacting with fusion-active gp41 from the human immunodeficiency virus type 1 envelope glycoprotein. J. Virol. 72:10213-10217.
23. Jiang, S., H. Lu, S. Liu, Q. Zhao, Y. He, and A. K. Debnath. 2004. N-substituted pyrrole derivatives as novel human immunodeficiency virus type 1 entry inhibitors that interfere with the gp41 six-helix bundle formation and block virus fusion. Antimicrob. Agents Chemother. 48:4349-4359.
24. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, M. Bilska, D. L. Kothe, J. F. Salazar-Gonzalez, X. Wei, J. M. Decker, B. H. Hahn, and D. C. Montefiori. 2005. Human immunodeficiency virus type 1 env clones from acute and early subtype B infections for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 79:10108-10125.
25. Li, Y., S. A. Migueles, B. Welcher, K. Svehla, A. Phogat, M. K. Louder, X. Wu, G. M. Shaw, M. Connors, R. T. Wyatt, and J. R. Mascola. 2007. Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat. Med. 13:1032-1034.
26. Louder, M. K., A. Sambor, E. Chertova, T. Hunte, S. Barrett, F. Ojong, E. Sanders-Buell, S. Zolla-Pazner, F. E. McCutchan, J. D. Roser, D. Gabuzda, J. D. Lifson, and J. R. Mascola. 2005. HIV-1 envelope pseudotyped viral vectors and infectious molecular clones expressing the same envelope glycoprotein have a similar neutralization phenotype, but culture in peripheral blood mononuclear cells is associated with decreased neutralization sensitivity. Virology 339:226-238.
27. Louis, J. M., C. A. Bewley, and G. M. Clore. 2001. Design and properties of N(CCG)-gp41, a chimeric gp41 molecule with nanomolar HIV fusion inhibitory activity. J. Biol. Chem. 276:29485-29489.
28. Louis, J. M., C. A. Bewley, E. Gustchina, A. Aniana, and G. M. Clore. 2005. Characterization and HIV-1 fusion inhibitory properties of monoclonal Fabs obtained from a human non-immune phage library selected against diverse epitopes of the ectodomain of HIV-1 gp41. J. Mol. Biol. 353:945-951.
29. Louis, J. M., I. Nesheiwat, L. Chang, G. M. Clore, and C. A. Bewley. 2003. Covalent trimers of the internal N-terminal trimeric coiled-coil of gp41 and antibodies directed against them are potent inhibitors of HIV envelope-mediated cell fusion. J. Biol. Chem. 278:20278-20285.
30. Meffre, E., M. Milili, C. Blanco-Betancourt, H. Antunes, M. C. Nussenzweig, and C. Schiff. 2001. Immunoglobulin heavy chain expression shapes the B cell receptor repertoire in human B cell development. J. Clin. Investig. 108:879-886.
31. Miller, M. D., R. Geleziunas, E. Bianchi, S. Lennard, R. Hrin, H. Zhang, M. Lu, Z. An, P. Ingallinella, M. Finotto, M. Mattu, A. C. Finnefrock, D. Bramhill, J. Cook, D. M. Eckert, R. Hampton, M. Patel, S. Jarantow, J. Joyce, G. Ciliberto, R. Cortese, P. Lu, W. Strohl, W. Schleif, M. McElhaugh, S. Lane, C. Lloyd, D. Lowe, J. Osbourn, T. Vaughan, E. Emini, G. Barbato, P. S. Kim, D. J. Hazuda, J. W. Shiver, and A. Pessi. 2005. A human monoclonal antibody neutralizes diverse HIV-1 isolates by binding a critical gp41 epitope. Proc. Natl. Acad. Sci. USA 102:14759-14764.
32. Montefiori, D. C., G. Pantaleo, L. M. Fink, J. T. Zhou, J. Y. Zhou, M. Bilska, G. D. Miralles, and A. S. Fauci. 1996. Neutralizing and infection-enhancing antibody responses to human immunodeficiency virus type 1 in long-term nonprogressors. J. Infect. Dis. 173:60-67.
33. Moulard, M., S. K. Phogat, Y. Shu, A. F. Labrijn, X. Xiao, J. M. Binley, M. Y. Zhang, I. A. Sidorov, C. C. Broder, J. Robinson, P. W. Parren, D. R. Burton, and D. S. Dimitrov. 2002. Broadly cross-reactive HIV-1-neutralizing human monoclonal Fab selected for binding to gp120-CD4-CCR5 complexes. Proc. Natl. Acad. Sci. USA 99:6913-6918.
34. Muster, T., F. Steindl, M. Purtscher, A. Trkola, A. Klima, G. Himmler, F. Ruker, and H. Katinger. 1993. A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J. Virol. 67:6642-6647.
35. Nelson, J. D., F. M. Brunei, R. Jensen, E. T. Crooks, R. M. Cardoso, M. Wang, A. Hessell, I. A. Wilson, J. M. Binley, P. E. Dawson, D. R. Burton, and M. B. Zwick. 2007. An affinity-enhanced neutralizing antibody against the membrane-proximal external region of human immunodeficiency virus type 1 gp41 recognizes an epitope between those of 2F5 and 4E10. J. Virol. 81:4033-4043.
36. Ofek, G., M. Tang, A. Sambor, H. Katinger, J. R. Mascola, R. Wyatt, and P. D. Kwong. 2004. Structure and mechanistic analysis of the anti-human immunodeficiency virus type 1 antibody 2F5 in complex with its gp41 epitope. J. Virol. 78:10724-10737.
37. Parren, P. W., I. Mondor, D. Naniche, H. J. Ditzel, P. J. Klasse, D. R. Burton, and Q. J. Sattentau. 1998. Neutralization of human immunodeficiency virus type 1 by antibody to gp120 is determined primarily by occupancy of sites on the virion irrespective of epitope specificity. J. Virol. 72:3512-3519.
38. Polonis, V. R., B. K. Brown, A. Rosa Borges, S. Zolla-Pazner, D. S. Dimitrov, M.-Y. Zhang, S. W. Barnett, R. M. Ruprecht, G. Scarlatti, E. Maria Fenyo, D. C. Montefiori, F. E. McCutchan, and N. L. Michael. 25 March 2008. Recent advances in the characterization of HIV-1 neutralization assays for standardized evaluation of newly developed or vaccine-induced antibodies. Virology doi:10.1016/j.virol.2008.02.007.
39. Roben, P., J. P. Moore, M. Thali, J. Sodroski, C. F. Barbas III, and D. R. Burton. 1994. Recognition properties of a panel of human recombinant Fab fragments to the CD4 binding site of gp120 that show differing abilities to neutralize human immunodeficiency virus type 1. J. Virol. 68:4821-4828.
40. Sanchez-Martínez, S., M. Lorizate, K. Hermann, R. Kunert, G. Basanez, and J. L. Nieva. 2006. Specific phospholipid recognition by human immunodeficiency virus type-1 neutralizing anti-gp41 2F5 antibody. FEBS Lett. 580:2395-2399.
41. Sánchez-Martínez, S., M. Lorizate, H. Katinger, R. Kunert, and J. L. Nieva. 2006. Membrane association and epitope recognition by HIV-1 neutralizing anti-gp41 2F5 and 4E10 antibodies. AIDS Res. Hum. Retrovir. 22:998-1006.
42. Sattentau, Q. J., and J. P. Moore. 1995. Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer. J. Exp. Med. 182:185-196.
43. Scherer, E. M., M. B. Zwick, L. Teyton, and D. R. Burton. 2007. Difficulties in eliciting broadly neutralizing anti-HIV antibodies are not explained by cardiolipin autoreactivity. AIDS 21:2131-2139.
44. Shu, Y., S. Winfrey, Z. Y. Yang, L. Xu, S. S. Rao, I. Srivastava, S. W. Barnett, G. J. Nabel, and J. R. Mascola. 2007. Efficient protein boosting after plasmid DNA or recombinant adenovirus immunization with HIV-1 vaccine constructs. Vaccine 25:1398-1408.
45. Song, R. J., A. L. Chenine, R. A. Rasmussen, C. R. Ruprecht, S. Mirshahidi, R. D. Glisson, W. Xu, J. B. Whitney, L. M. Goins, H. Ong, P. L. Li, E. Shai-Kobiler, T. Wang, C. M. McCann, H. Zhang, C. Wood, C. Kankasa, W. E. Secor, H. M. McClure, E. Strobert, J. G. Else, and R. M. Ruprecht. 2006. Molecularly cloned SHIV-1157ipd3N4: a highly replication-competent, mucosally transmissible R5 simian-human immunodeficiency virus encoding HIV clade C Env. J. Virol. 80:8729-8738.
46. Stiegler, G., R. Kunert, M. Purtscher, S. Wolbank, R. Voglauer, F. Steindl, and H. Katinger. 2001. A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 17:1757-1765.
47. Wyatt, R., and J. Sodroski. 1998. The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280:1884-1888.
48. Zhang, M. Y., V. Choudhry, I. A. Sidorov, V. Tenev, B. K. Vu, A. Choudhary, H. Lu, G. M. Stiegler, H. W. Katinger, S. Jiang, C. C. Broder, and D. S. Dimitrov. 2006. Selection of a novel gp41-specific HIV-1 neutralizing human antibody by competitive antigen panning. J. Immunol. Methods 317:21-30.
49. Zhang, M. Y., Y. Shu, S. Phogat, X. Xiao, F. Cham, P. Bouma, A. Choudhary, Y. R. Feng, I. Sanz, S. Rybak, C. C. Broder, G. V. Quinnan, T. Evans, and D. S. Dimitrov. 2003. Broadly cross-reactive HIV neutralizing human monoclonal antibody Fab selected by sequential antigen panning of a phage display library. J. Immunol. Methods 283:17-25.
50. Zhang, M. Y., X. Xiao, I. A. Sidorov, V. Choudhry, F. Cham, P. F. Zhang, P. Bouma, M. Zwick, A. Choudhary, D. C. Montefiori, C. C. Broder, D. R. Burton, G. V. Quinnan, Jr., and D. S. Dimitrov. 2004. Identification and characterization of a new cross-reactive human immunodeficiency virus type 1-neutralizing human monoclonal antibody. J. Virol. 78:9233-9242.
51. Zolla-Pazner, S. 2004. Identifying epitopes of HIV-1 that induce protective antibodies. Nat. Rev. Immunol. 4:199-210.
52. Zwick, M. B., A. F. Labrijn, M. Wang, C. Spenlehauer, E. O. Saphire, J. M. Binley, J. P. Moore, G. Stiegler, H. Katinger, D. R. Burton, and P. W. Parren. 2001. Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75:10892-10905.