Human immunodeficiency virus type 1 gp41 antibodies that mask membrane proximal region epitopes: Antibody binding kinetics, induction, and potential for regulation in acute infection

Journal of Virology

Volumn 82, Issue 1, 2008, Pages 115-125

  Alam, S Munir ^a,f   Scearce, Richard M ^a   Parks, Robert J ^a   Plonk, Kelly ^a   Plonk, Steven G ^a   Sutherland, Laura L ^a   Gorny, Miroslaw K ^b   Zolla Pazner, Susan ^b   VanLeeuwen, Stacie ^a   Moody, M Anthony ^a   Xia, Shi Mao ^a   Montefiori, David C ^a   Tomaras, Georgia D ^a   Weinhold, Kent J ^a   Karim, Salim Abdool ^c   Hicks, Charles B ^a   Liao, Hua Xin ^a   Robinson, James ^d   Shaw, George M ^e   Haynes, Barton F ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KWAZULU NATAL   (South Africa)

^d TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; EPITOPE; GLYCOPROTEIN GP 41; GLYCOPROTEIN GP 41 ANTIBODY; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 13H11; MONOCLONAL ANTIBODY 2F5; MONOCLONAL ANTIBODY 4E10; MONOCLONAL ANTIBODY 5A9; PHOSPHATIDYLSERINE; PROTEIN ANTIBODY; UNCLASSIFIED DRUG; VIRUS GLYCOPROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ANTIGEN BINDING; ARTICLE; B LYMPHOCYTE ACTIVATION; BINDING KINETICS; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENVELOPE GENE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS ISOLATION;

ANIMALS; ANTIBODIES, MONOCLONAL; CROSS REACTIONS; EPITOPES; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP41; HIV INFECTIONS; HIV-1; HUMANS; KINETICS; LIPIDS; MICE; NEUTRALIZATION TESTS; PROTEIN BINDING;

HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE;

EID: 37349057483     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00927-07     Document Type: Article

References (56)

1. Alam, S. M., C. A. Paleos, H-X. Liao, R. M. Scearce, J. Robinson, and B. F. Haynes. 2004. An inducible HIV-1 gp41 HR-2 peptide binding site on HIV-1 envelope gp120. AIDS Res. Hum. Retrovir. 20:836-845.
2. Alam, S. M., M. McAdam, 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 gp41 membrane proximal envelope epitopes. J. Immunol. 178:4424-4435.
3. Barin, F., M. F. McLane, J. S. Allan, T. H. Lee, J. E. Groopman, and M. Essex. 1985. Virus envelope protein of HTLV-III represents major target antigen for antibodies in AIDS patients. Science 228:1094-1096.
4. Bowman, J. M. 1988. The prevention of Rh immunization. Transfus. Med. Rev. 2:129-150.
5. + T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J. Exp. Med. 200:749-759.
6. 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.
7. Buchacher, A., R. Predl, K. Strutzenberger, W. Steinfellner, A. Trkola, M. Purtscher, G. Gruber, C. Tauer, F. Steindl, and A. Jungbauer. 1994. Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retrovir. 10:359-369.
8. Burton, D. R., R. L. Stanfield, and I. A. Wilson. 2005. Antibody vs. HIV in a clash of evolutionary titans. Proc. Natl. Acad. Sci. USA 102:14943-14948.
9. Calarota, S., M. Janssen, M. Levi, K. Broliden, O. Libonatti, H. Wigzell, and B. Wahren. 1996. Immunodominant glycoprotein 41 epitope identified by seroreactivity in HIV type 1-infected individuals. AIDS Res. Hum. Retrovir. 12:705-713.
10. Cardoso, R. M., M. B. Zwick, R. L. Stanfield, R. Kunert, J. M. Binley, H. Katinger, D. R. Burton, and I. A. Wilson. 2005. Broadly neutralizing anti-HIV antibody 4E10 recognizes a helical conformation of a highly conserved fusion-associated motif in gp41. Immunity 22:163-173.
11. Choudhry, V., M. Y. Zhang, I. Harris, I. A. Sidorov, B. Vu, A. S. Dimitrov, T. fouts, and D. S. Dimitrov. 2006. Increased efficacy of HIV-1 neutralization by antibodies at low CCR5 surface concentration. Biochem. Biophys. Res. Commun. 348:1107-1115.
12. Clarke, C. A., W. T. A. Donohoe, J. C. Woodrow, R. Finn, J. R. Krevans, W. Kulke, D. Lehane, and P. M. Sheppard. 1963. Further experimental studies on the prevention of Rh haemolytic disease. Br. Med. J. 1:979-984.
13. Cleghorn, F. R., N. Jack, J. K. Carr, J. Edwards, B. Mahabir, A. Sill, C. B. McDanal, S. M. Connolly, D. Goodman, R. Q. Bennetts, T. R. O'Brien, K. J. Weinhold, C. Bartholomew, W. A. Blattner, and M. L. Greenberg. 2000. A distinctive clade B HIV type 1 is heterosexually transmitted in Trinidad and Tobago. Proc. Natl. Acad. Sci. USA 97:10523-10537.
14. Cleveland, S. M., E. Buratti, T. D. Jones, P. North, F. Baralle, L. McLain, T. Mclnerney, Z. Durrani, and N. J. Dimmock. 2000. Immunogenic and anitgenic dominance of a neutralizing epitope over a highly conserved neutralizing epitope in the gp41 envelope glycoprotein of human immunodeficiency virus type 1: its deletion leads to a strong neutralizing response. Virology 266:66-78.
15. Dintzis, R., Z. M. H. Middleton, and H. M. Dintzis. 1983. Studies on the immunogenicity and tolerogenicity of T-independent antigens. J. Immunol. 131:2196-2203.
16. Dintzis, R. Z., M. Okajima, M. H. Middleton, and H. M. Dintzis. 1990. Inhibition of antibody formation by receptor crosslinking: the molecular characteristics of inhibitory haptenated polymers. Eur. J. Immunol. 20:229-232.
17. Garrity, R. R., G. Rimmelzwaan, A. Minassian, W. P. Tsai, G. Lin, J. J. de Jong, J. Goudsmit, and P. L. Nara. 1997. Refocusing neutralizing antibody response by targeted dampening of an immunodominant epitope. J. Immunol. 159:279-289.
18. Gorny, M. K., and S. Zolla-Pazner. 2000. Recognition of human monoclonal antibodies of free and complexed peptides representing the prefusogenic and fusogenic forms of human immunodeficiency virus type I gp41. J. Virol. 74:6186-6192.
19. Goudsmit, J., R. H. Meloen, and R. Brasseur. 1990. Map of sequential B cell epitopes of the HIV-1 transmembrane protein using human antibodies as probe. Intervirology 31:327-338.
20. Gray, E. S., P. L. Moore, I. A. Choge, F. Bibollet-Ruche, H. Li, N. Leseka, F. Treurnicht, K. Milsana, G. M. Shaw, S. S. Abdool Karim, C. Williamson, and L. Morris. 4 April 2007. Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J. Virol. doi:10.1128/JVI.00239-07. (Subsequently published, J. Virol. 81:6187-6196, 2007.)
21. Grundner, C., T. Mirzabekov, J. Sodroski, and R. Wyatt. 2002. Solid-phase proteoliposomes containing human immunodeficiency virus envelope glyco-proteins. J. Virol. 76:3511-3521.
22. + T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J. Virol. 77:11708-11717.
23. Haynes, B. F., and D. C. Montefiori. 2006. Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev. Vaccines 5:347-363.
24. 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.
25. Haynes, B. F., M. A. Moody, L. Verkoczy, G. Kelsoe, and S. M. Alam. 2005. Antibody polyspecificity and neutralization of HIV-1: a hypothesis. Hum. Antibodies 14:59-67.
26. Hjelm, F., F. Carlsson, A. Getahun, and B. Heyman. 2006. Antibody-mediated regulation of the immune response. Scand. J. Immunol. 64:177-184.
27. Ioannou, X. P., S. M. Gomis, B. Karvonen, R. Hecker, L. A. Babiuk, and S. van Drunen Littel-van den Hurk. 2002. CpG-containing oligodeoxynucleotides, in combination with conventional adjuvants, enhance the magnitude and change the bias of the immune responses to a herpesvirus glycoprotein. Vaccine 21:127-137.
28. Kim, M., Z. Qiao, J. Yu, D. Montefiori, and E. L. Reinherz. 9 October 2006. Immunogenicity of recombinant human immunodeficiency virus type 1-like particles expressing gp41 derivatives in a pre-fusion state. Vaccine 25:5102-5114. [Epub ahead of print.]
29. Klasse, P. J., R. Pipkorn, and J. Blomberg. 1988. Presence of antibodies to a putatively immunosuppressive part of human immunodeficiency virus (HIV) envelope glycoprotein gp41 is strongly associated with health among HIV-positive subjects. Proc. Natl. Acad. Sci. USA 85:5225-5229.
30. Kwong, P. D., M. L. Doyle, DJ Casper, C. Cicala, S. A. Leavitt S. Majeed, T. D. Steenbeke, M. Venturi, I. Chaiken, M. Fung, H. Katinge, P. W. Parren, J. Robinson, D. Van Ryk, L. Wang, D. R. Burton, E. Freire, R. Wyatt, J. Sodroski, W. A. Hendrickson, and J. Arthos. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682.
31. Lee, S. J., R. Arora, L. M. Bull, R. C. Arduino, L. Garza, J. Allan, J. T. Kimata, and P. Zhou. 2006. A nonneutralizing anti-HIV type 1 antibody turns into a broad neutralizing antibody when expressed on the surface of HIV type 1-susceptible cells. II. Inhibition of HIV type 1 captured and transferred by DC-SIGN. AIDS Res. Hum. Retrovir. 22:874-883.
32. Li, H., Y. Jiang, H. Cao, M. Radic, E. L. Prak, and M. Weigert. 2003. Regulation of anti-phosphatidylserine antibodies. Immunity 18:185-192.
33. Li, M., J. F. Salazar-Gonzalez, C. A. Derdeyn, L. Morris, C. Williamson, J. E. Robinson, J. M. Decker, Y. Li, M. G. Salazar, V. R. Polonis, K. Mlisana, S. A. Karim, K. Hong, K. M., Greene, M. Bilska, J. Zhou, S. Allen, E. Chomba, J. Mulenga, C. Vwalika, F. Gao, M. Zhang, B. T. Korber, E. Hunter, B. H. Hahn, and D. C. Montefiori. 2006. Genetic and neutralization properties of subtype C human immunodeficiency virus type 1 molecular env clones from acute and early heterosexually acquired infections in Southern Africa. J. Virol. 80:11776-11790.
34. Liao, H.X., L. L. Sutherland, S-M Xia, M. E. Brock, R. M. Scearce, S. Vanleeuwen, M-S. Alam, M. McAdams, E. A. Weaver, Z. T. Camacho, B-J. Ma, Y. Li, J. M. Decker, G. J. Nabel, D. C. Montefiori, B. H. Hahn, B. T. Korber, F. Gao, and B. F. Haynes. 2006. A group M consensus envelope glycoprotein induces antibodies that neutralize subsets of subtype B and C HIV-1 primary viruses. Virology 353:268-282.
35. + T cells in multiple tissues during acute SIV infection. Nature 434:1093-1097.
36. McGaughey, G. B., G. Barbato, E. Bianchi, R. M. Freidinger, V. M. Garsky, W. M. Hurni, J. G. Joyce, X. Liang, M. D. Miller, A. Pessi, J. W. Shiver, and M. J. Bogusky. 2004. Progress towards the development of a HIV-1 gp41-directed vaccine. Curr. HIV Res. 2:193-204.
37. McGaughey, G. B., M. Citron, R. C. Danziesen, R. M. Freidinger, V. M. Garsky, W. M. Hurni, J. G. Joyce, X. Liang, M. D. Miller, J. W. Shiver, and M. J. Bogusky. 2003. HIV-1 vaccine development: constrained peptide immunogens show improved binding to the anti-HIV-1 gp41 MAb. Biochemistry 42:3214-3223.
38. 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.
39. + T lymphocytes from effector sites in the gastrointestinal tract. J. Exp. Med. 200:761-770.
40. Moore, P. L., E. T. Crooks, L. Porter, P. Zhu, C. S. Cayanan, H. Grise, P. Corcoran, M. B. Zwick, M. Franti, L. Morris, K. H. Roux, D. R. Burton, and J. M. Binley. 2006. Nature of nonfunctional envelope proteins on the surface of human immunodeficiency virus type 1. J. Virol. 80:2515-2528.
41. Neurath, A. R., N, Strick, P. Taylor, P. Rubinstein, and C. E. Stevens. 1990. Search for epitope-specific antibody responses to the human immunodeficiency virus (HIV-1) envelope glycoproteins signifying resistance to disease development. AIDS Res. Hum. Retrovir. 6:1183-1192.
42. 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.
43. Opalka, D., A. Pessi, E. Bianchi, G. Ciliberto, W. Schleif, M. McElhaugh, R. Danzeisen, R. Geleziunas, R. Miller, M. Eckert, D. M. Bramhill, J. Joyce, J. Cook, W. Magilton, J. Shiver, E. Emini, and M. T. Esser. 2004. Analysis of the HIV-1 gp41 specific immune response using a multiplexed antibody detection assay. J. Immunol. Methods 287:49-65.
44. Pantophlet, R., I. A. Wilson, and D. R. Burton. 2003. Hyperglycosylated mutants of human immunodeficiency virus (HIV) type 1 monomeric gpl20 as novel antigens for HIV vaccine design. J. Virol. 77:5889-5901.
45. Parker, C. E., L. J. Deterding, C. Hager-Braun, J. M. Binley, N. Schulke, H. Katinger, J. P. Moore, and K. B. Tomer. 2001. Fine definition of the epitope on the gp41 glycoprotein of human immunodeficiency virus type 1 for the neutralizing monoclonal antibody 2F5. J. Virol. 75:10906-10911.
46. Parren, P. W., D. R. Burton, and Q. J. Sattentau. 1997. HIV-1 antibody: debris or virion? Nat. Med. 3:366-367.
47. Purtscher, M., A. Trkola, G. Gruber, A. Buchacher, R. Predl, F. Steindl, C. Tauer, R. Berger, N. Barrett, and A. Jungbauer. 1994. A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retrovir. 10:1651-1658.
48. Richman, D. D., T. Wrin, S. J. Little, and C. J. Petropoulos. 2003. Rapid evolution of the neutralizing antibody response to HIV type 1 infection. Proc. Natl. Acad. Sci. USA. 100:4144-4149.
49. Sanchez-Martinez, S., M. Lorizate, H. Katinger, R. Kunerte, 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.
50. 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.
51. Tran, T. T., C. F. Reich III, M. Alam, and D. S. Pisetsky. 2003. Specificity and immunochemical properties of anti-DNA antibodies induced in normal mice by immunization with mammalian DNA with a CpG oligonucleotide as adjuvant. Clin. Immunol. 109:278-287.
52. Tyler, D. S., S. D. Stanley, S. Zolla-Pazner, M. K. Gorny, P. P. Shadduck, A. J. Langlois, T. J., Matthews, D. P. Bolognesi, T. J. Palker, and K. J. Weinhold. 1990. Identification of sites within gp41 that serve as targets for antibody-dependent cellular cytotoxicity by using human monoclonal anti-bodies. J. Immunol. 145:3276-3282.
53. + T cell depletion and viral replication in SIV infection. Science 280:427-431.
54. Wei, X., J. M. Decker, S. Wang, H. Hui, J. C. Kappes, X. Wu, J. F. Salazar-Gonzalez, M. G. Salazar, J. M. Kilby, M. S. Saag, N. L. Komarova, M. A. Nowak, B. H. Hahn, P. D. Kwong, and G. M. Shaw. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307-312.
55. Xu, J. Y, M. K. Gorny, T. Palker, S. Karwowska, and S. Zolla-Pazner. 1991. Epitope mapping of two immunodominant domains of gp41, the transmembrane protein of human immunodeficiency virus type 1, using ten human monoclonal antibodies. J. Virol. 65:4832-4838.
56. 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.