CD4 binding determinant mimicry for HIV vaccine design

Frontiers in Immunology

Volumn 3, Issue DEC, 2012, Pages

  Nishiyama, Yasuhiro ^a   Planque, Stephanie ^a   Hanson, Carl V ^b   Massey, Richard J ^c   Paul, Sudhir ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b VIRAL AND RICKETTSIAL DISEASE LABORATORY   (United States)

^c Covalent Bioscience Inc ^*  (United States)

Author keywords

B cell superantigen; Catalytic antibody; CD4 binding determinant; Human immunodeficiency virus; Neutralizing antibody; Vaccine

Indexed keywords

EID: 84874222809     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00383     Document Type: Review

References (96)

1. Berberian, L., Goodglick, L., Kipps, T. J., and Braun, J. (1993). Immunoglobulin VH3 gene products: natural ligands for HIV gp120. Science 261, 1588-1591.
2. Bialuk, I., Whitney, S., Andresen, V., Florese, R. H., Nacsa, J., Cecchinato, V., et al. (2011). Vaccine induced antibodies to the first variable loop of human immunodeficiency virus type 1 gp120, mediate antibody-dependent virus inhibition in macaques. Vaccine 30, 78-94.
3. Binley, J. M., Wrin, T., Korber, B., Zwick, M. B., Wang, M., Chappey, C., et al. (2004). Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78, 13232-13252.
4. Boudet, F., Girard, M., Theze, J., and Zouali, M. (1992). Antibodies of HIV-1 positive subjects and experimentally immunized primates and rodents bind to sequence divergent regions of the third variable domain (V3) of gp120. Int. Immunol. 4, 283-294.
5. Brown, B. K., Wieczorek, L., Sanders-Buell, E., Rosa Borges, A., Robb, M. L., Birx, D. L., et al. (2008). Cross-clade neutralization patterns among HIV-1 strains from the six major clades of the pandemic evaluated and compared in two different models. Virology 375, 529-538.
6. Burton, D. R., Pyati, J., Koduri, R., Sharp, S. J., Thornton, G. B., Parren, P. W., et al. (1994). Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266, 1024-1027.
7. Chen, B., Vogan, E. M., Gong, H., Skehel, J. J., Wiley, D. C., and Harrison, S. C. (2005). Structure of an unliganded simian immunodeficiency virus gp120 core. Nature 433, 834-841.
8. Chen, L., Kwon, Y. D., Zhou, T., Wu, X., O'Dell, S., Cavacini, L., et al. (2009). Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326, 1123-1127.
9. Cordonnier, A., Montagnier, L., and Emerman, M. (1989). Single amino-acid changes in HIV envelope affect viral tropism and receptor binding. Nature 340, 571-574.
10. Corti, D., Langedijk, J. P., Hinz, A., Seaman, M. S., Vanzetta, F., Fernandez-Rodriguez, B. M., et al. (2010). Analysis of memory B cell responses and isolation of novel monoclonal antibodies with neutralizing breadth from HIV-1-infected individuals. PLoS ONE 5:e8805. doi: 10.1371/journal.pone. 0008805
11. Dey, B., Pancera, M., Svehla, K., Shu, Y., Xiang, S. H., Vainshtein, J., et al. (2007). Characterization of human immunodeficiency virus type 1 monomeric and trimeric gp120 glycoproteins stabilized in the CD4-bound state: antigenicity, biophysics, and immunogenicity. J. Virol. 81,5579-5593.
12. Diskin, R., Scheid, J. F., Marcovecchio, P. M., West, A. P. Jr., Klein, F., Gao, H., et al. (2011). Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334, 1289-1293.
13. Falkowska, E., Ramos, A., Feng, Y., Zhou, T., Moquin, S., Walker, L. M., et al. (2012). PGV04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce confor-mational changes characteristic of CD4.J. Virol. 86, 4394-4403.
14. Feng, Y., McKee, K., Tran, K., O'Dell, S., Schmidt, S. D., Phogat, A., et al. (2012). Biochemically defined HIV-1 envelope glycoprotein variant immunogens display differential binding and neutralizing specificities to the CD4-binding site. J. Biol. Chem. 287, 5673-5686.
15. Gao, Q. S., Sun, M., Rees, A. R., and Paul, S. (1995). Site-directed muta-genesis of proteolytic antibody light chain.J. Mol. Biol. 253, 658-664.
16. Gauduin, M. C., Parren, P. W., Weir, R., Barbas, C. F., Burton, D. R., and Koup, R. A. (1997). Passive immunization with a human monoclonal antibody protects hu-PBL-SCID mice against challenge by primary isolates of HIV-1. Nat. Med. 3, 1389-1393.
17. Geonnotti, A. R., Bilska, M., Yuan, X., Ochsenbauer, C., Edmonds, T. G., Kappes, J. C., et al. (2010). Differential inhibition of human immunodeficiency virus type 1 in peripheral blood mononuclear cells and TZM-bl cells by endotoxin-mediated chemokine and gamma interferon production. AIDS Res. Hum. Retroviruses 26, 279-291.
18. Gololobov, G., Sun, M., and Paul, S. (1999). Innate antibody catalysis. Mol. Immunol. 36, 1215-1222.
19. Goodglick, L., Zevit, N., Neshat, M. S., and Braun, J. (1995). Mapping the Ig superantigen-binding site of HIV-1 gp120. J. Immunol. 155, 5151-5159.
20. Goodyear, C. S., Corr, M., Sugiyama, F., Boyle, D. L., and Silverman, G. J. (2007). Cutting edge: bim is required for superantigen-mediated B cell death. J. Immunol. 178, 2636-2640.
21. Goodyear, C. S., and Silverman, G. J. (2005). B cell superantigens: a microbe's answer to innate-like B cells and natural antibodies. Springer Semin. Immunopathol. 26, 463-484.
22. Graf Von Stosch, A., Jimenez, M. A., Kinzel, V., and Reed, J. (1995). Solvent polarity-dependent structural refolding: a CD and NMR study of a 15 residue peptide. Proteins 23, 196-203.
23. Herrera, C., Spenlehauer, C., Fung, M. S., Burton, D. R., Beddows, S., and Moore, J. P. (2003). Nonneutralizing antibodies to the CD4-binding site on the gp120 subunit of human immunodeficiency virus type 1 do not interfere with the activity of a neutralizing antibody against the same site.J. Virol. 77, 1084-1091.
24. Heyndrickx, L., Heath, A., Sheik-Khalil, E., Alcami, J., Bongertz, V., Jansson, M., et al. (2012). International network for comparison of HIV neutralization assays: the NeutNet report II. PLoS ONE 7:e36438. doi: 10.1371/journal.pone.0036438
25. Hifumi, E., Honjo, E., Fujimoto, N., Arakawa, M., Nishizono, A., and Uda, T. (2012). Highly efficient method of preparing human catalytic antibody light chains and their biological characteristics. FASEBJ. 26, 1607-1615.
26. Huang, C. C., Tang, M., Zhang, M. Y., Majeed, S., Montabana, E., Stanfield, R. L., et al. (2005). Structure of a V3-containing HIV-1 gp120 core. Science 310, 1025-1028.
27. Janeway, C., Travers, P., Walport, M., and Schlomchik, M. J. (2005). Immunologybiology: the Immune System in Health and Disease. The Generation of Lymphocyte Antigen Receptors. 6th Edn. New York and London: Garland Science Publishing, 135-168.
28. Karle, S., Nishiyama, Y., Taguchi, H., Zhou, Y X., Luo, J., Planque, S., et al. (2003). Carrier-dependent specificity of antibodies to a conserved peptide determinant of gp120. Vaccine 21, 1213-1218.
29. Karle, S., Planque, S., Nishiyama, Y., Taguchi, H., Zhou, Y X., Salas, M., et al. (2004). Cross-clade HIV-1 neutralization by an antibody fragment from a lupus phage display library.AIDS 18, 329-331.
30. Karray, S., Juompan, L., Maroun, R. C., Isenberg, D., Silverman, G. J., and Zouali, M. (1998). Structural basis of the gp120 superantigen-binding site on human immunoglobulins. J. Immunol. 161, 6681-6688.
31. Karray, S., and Zouali, M. (1997). Identification of the B cell superantigen-binding site of HIV-1 gp120. Proc. Natl. Acad. Sci. U.S.A. 94, 1356-1360.
32. Kelker, H. C., Itri, V R., and Valentine, F. T. (2010). A strategy for eliciting antibodies against cryptic, conserved, conformationally dependent epitopes of HIV envelope glycoprotein. PLoS ONE 5:e8555. doi: 10.1371/journal.pone.0008555
33. Koff, W. C. (2012). HIV vaccine development: challenges and opportunities towards solving the HIV vaccine-neutralizing antibody problem. Vaccine 30, 4310-4315.
34. Kwon, Y D., Finzi, A., Wu, X., Dogo-Isonagie, C., Lee, L. K., Moore, L. R., et al. (2012). Unliganded HIV-1 gp120 core structures assume the CD4-bound conformation with regulation by quaternary interactions and variable loops. Proc. Natl. Acad. Sci. U.S.A. 109, 5663-5668.
35. Kwong, P. D., Doyle, M. L., Casper, D. J., Cicala, C., Leavitt, S. A., Majeed, S., et al. (2002). HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420, 678-682.
36. Kwong, P. D., Wyatt, R., Majeed, S., Robinson, J., Sweet, R. W., Sodroski, J., et al. (2000). Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8, 1329-1339.
37. Kwong, P. D., Wyatt, R., Robinson, J., Sweet, R. W., Sodroski, J., and Hendrickson, W. A. (1998). Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659.
38. Lasky, L. A., Nakamura, G., Smith, D. H., Fennie, C., Shimasaki, C., Patzer, E., et al. (1987). Delineation of a region of the human immunodeficiency virus type 1 gp120 glycoprotein critical for interaction with the CD4 receptor. Cell 50, 975-985.
39. Leder, L., Berger, C., Bornhauser, S., Wendt, H., Ackermann, E, Jelesarov, I., et al. (1995). Spectroscopic,calorimetric, and kinetic demonstration of conformational adaptation in peptide-antibodyrecognition. Biochemistry 34, 16509-16518.
40. Los Alamos National Laboratory Theoretical Biology and Biophysics Group. (2012). HIV Sequence Compendium 2012. Los Alamos, New Mexico: Los Alamos National Laboratory.
41. Mann, A. M., Rusert, P., Berlinger, L., Kuster, H., Gunthard, H. F., and Trkola, A. (2009). HIV sensitivity to neutralization is determined by target and virus producer cell properties. AIDS 23, 1659-1667.
42. McElrath, M. J., and Haynes, B. E (2010). Induction of immunity to human immunodeficiency virus type-1 by vaccination. Immunity 33, 542-554.
43. Mihailescu, D., Smith, J. C., and Reed, J. (2002). Solution structure of aputa-tive HIV1 immunogenic peptide: computer simulation of the principal CD4 binding domain of gp120. J. Med. Chem. 45, 1019-1025.
44. Montefiori, D. C., Graham, B. S., Zhou, J., Zhou, J., Bucco, R. A., Schwartz, D. H., et al. (1993). V3-specific neutralizing antibodies in sera from HIV-1 gp160-immunized volunteers block virus fusion and act synergistically with human monoclonal antibody to the conformation-dependentCD4 binding site of gp120. NIH-NIAID AIDS Vaccine Clinical Trials Network. J. Clin. Invest. 92, 840-847.
45. Moody, M. A., Liao, H. X., Alam, S. M., Scearce, R. M., Plonk, M. K., Kozink, D. M., et al. (2010). Anti-phospholipid human monoclonal antibodies inhibit CCR5-tropic HIV-1 and induce beta-chemokines. J. Exp. Med. 207, 763-776.
46. Moore, J. P., and Sodroski, J. (1996). Antibody cross-competition analysis of the human immunodeficiency virus type 1 gp 120 exterior envelope glycoprotein. J. Virol. 70, 1863-1872.
47. Morrow, W. J., Williams, W. M., Whalley, A. S., Ryskamp, T., Newman, R., Kang, C. Y., et al. (1992). Synthetic peptides from a conserved region of gp120 induce broadly reactive anti-HIV responses. Immunology 75, 557-564.
48. Munier, C. M., Andersen, C. R., and Kelleher, A. D. (2011). HIV vaccines: progress to date. Drugs 71, 387-414.
49. Neshat, M. N., Goodglick, L., Lim, K., and Braun, J. (2000). Mapping the B cell superantigen binding site for HIV-1 gp120 on a V(H)3 Ig. Int. Immunol. 12,305-312.
50. Neurath, A. R., Strick, N., and Lee, E. S. (1990). B cell epitope mapping of human immunodeficiency virus envelope glycoproteins with long (19- to 36-residue) synthetic peptides. J. Gen. Virol. 71(Pt 1), 85-95.
51. Nishiyama, Y., Karle, S., Mitsuda, Y., Taguchi, H., Planque, S., Salas, M., et al. (2006). Towards irreversible HIV inactivation: stable gp120 binding by nucleophilic antibodies. J. Mol. Recognit. 19, 423-431.
52. Nishiyama, Y., Mitsuda, Y., Taguchi, H., Planque, S., Hara, M., Karle, S., et al. (2005). Broadly distributed nucleophilic reactivity of proteins coordinated with specific ligand binding activity. J. Mol. Recognit. 18, 295-306.
53. Nishiyama, Y., Planque, S., Mitsuda, Y., Nitti, G., Taguchi, H., Jin, L., et al. (2009). Toward effective HIV vaccination: induction of binary epitope reactive antibodies with broad HIV neutralizing activity. J. Biol Chem. 284,30627-30642.
54. Olshevsky, U., Helseth, E., Furman, C., Li, J., Haseltine, W., and Sodroski, J. (1990). Identification of individual human immunodeficiency virus type 1 gp120 amino acids important for CD4 receptor binding. J. Virol. 64, 5701-5707.
55. Pancera, M., and Wyatt, R. (2005). Selective recognition of oligomeric HIV-1 primary isolate envelope glycoproteins by potently neutralizing ligands requires efficient precursor cleavage. Virology 332, 145-156.
56. Pantophlet, R., and Burton, D. R. (2006). GP120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24, 739-769.
57. Pantophlet, R., Ollmann Saphire, E., Poignard, P., Parren, P. W., Wilson, I. A., and Burton, D. R. (2003). Fine mapping of the interaction of neutralizing and nonneutralizing monoclonal antibodies with the CD4 binding site of human immunodeficiency virus type 1 gp120. J. Virol. 77, 642-658.
58. Parren, P. W., Marx, P. A., Hessell, A. J., Luckay, A., Harouse, J., Cheng-Mayer, C., 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.
59. Paul, S., Karle, S., Planque, S., Taguchi, H., Salas, M., Nishiyama, Y., et al. (2004). Naturally occurring proteolytic antibodies: selective immunoglobulinM-catalyzed hydrolysis of HIV gp120. J. Biol. Chem. 279,39611-39619.
60. Paul, S., Planque, S., Nishiyama, Y., Escobar, M., and Hanson, C. (2010). Back to the future: covalent epitope-based HIV vaccine development. Expert Rev. Vaccines 9, 1027-1043.
61. Paul, S., Planque, S., Zhou, Y X., Taguchi, H., Bhatia, G., Karle, S., et al. (2003). Specific HIV gp120-cleaving antibodies induced by covalently reactive analog of gp120. J. Biol. Chem. 278, 20429-20435.
62. Planque, S., Mitsuda, Y., Taguchi, H., Salas, M., Morris, M. K., Nishiyama, Y., et al. (2007). Characterization of gp120 hydrolysis by IgA antibodies from humans without HIV infection. AIDS Res. Hum. Retroviruses 23, 1541-1554.
63. Planque, S., Nishiyama, Y., Mitsuda, Y., Taniguchi, R., Watanabe, K., Hanson, C. V., et al. (2012a). "Broad HIV neutralization by constitutive antibodies and their amplification by covalent HIV vaccination," in 19th International AIDS Conference (AIDS2012) (Washington, DC).
64. Planque, S. A., Mitsuda, Y., Nishiyama, Y., Karle, S., Boivin, S., Salas, M., et al. (2012b). Antibodies to asuper-antigenic gp120 epitope as the basis for developing an HIV vaccine. J. Immunol. 189, 5367-5381.
65. Planque, S., Nishiyama, Y., Taguchi, H., Salas, M., Hanson, C., and Paul, S. (2008). Catalytic antibodies to HIV: physiological role and potential clinical utility. Autoimmun. Rev. 7, 473-479.
66. Planque, S., Salas, M., Mitsuda, Y., Sienczyk, M., Escobar, M. A., Mooney, J. P., et al. (2010). Neutralization of genetically diverse HIV-1 strains by IgA antibodies to the gp120-CD4-binding site from long-term survivors of HIV infection. AIDS 24, 875-884.
67. Planque, S., Taguchi, H., Burr, G., Bhatia, G., Karle, S., Zhou, Y X., et al. (2003). Broadly distributed chemical reactivity of natural antibodies expressed in coordination with specific antigen binding activity.J. Biol. Chem. 278,20436-20443.
68. Reed, J., and Kinzel, V (1991). A conformational switch is associated with receptor affinity in peptides derived from the CD4-binding domain of gp120 from HIV I. Biochemistry 30, 4521-4528.
69. Reed, J., and Kinzel, V (1993). Primary structure elements responsible for the conformational switch in the envelope glycoprotein gp120 from human immunodeficiency virus type 1: LPCR is a motif governing folding. Proc. Natl. Acad. Sci. U.S.A. 90, 6761-6765.
70. Rerks-Ngarm, S., Pitisuttithum, P., Nitayaphan, S., Kaewkungwal, J., Chiu, J., Paris, R., et al. (2009). Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361, 2209-2220.
71. Reshetnyak, A. V., Armentano, M. F., Ponomarenko, N. A., Vizzuso, D., Durova, O. M., Ziganshin, R., et al. (2007). Routes to covalent catalysis by reactive selection for nascent protein nucleophiles. J. Am. Chem. Soc. 129,16175-16182.
72. Robey, F. A., Harris-Kelson, T., Robert-Guroff, M., Batinic, D., Ivanov, B., Lewis, M. S., et al. (1996). A synthetic conformational epitope from the C4 domain of HIV Gp120 that binds CD4. J. Biol. Chem. 271, 17990-17995.
73. Rusert, P., Mann, A., Huber, M., Von Wyl, V., Gunthard, H. F., and Trkola, A. (2009). Divergent effects of cell environment on HIV entry inhibitor activity. AIDS 23, 1319-1327.
74. Saphire, E. O., Montero, M., Menendez, A., Van Houten, N. E., Irving, M. B., Pantophlet, R., et al. (2007). Structure of a high-affinity "mimo-tope" peptide bound to HIV-1-neutralizing antibody b12 explains its inability to elicit gp120 cross-reactive antibodies. J. Mol. Biol. 369, 696-709.
75. Sapparapu, G., Planque, S., Mitsuda, Y., McLean, G., Nishiyama, Y., and Paul, S. (2012). Constant domain-regulated antibody catalysis. J. Biol. Chem. 287, 36096-36104.
76. Scheid, J. F., Mouquet, H., Ueberheide, B., Diskin, R., Klein, F., Oliveira, T. Y., et al. (2011). Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333, 1633-1637.
77. Sharma, V., Heriot, W., Trisler, K., and Smider, V. (2009). A human germ line antibody light chain with hydrolytic properties associated with multimerization status. J. Biol Chem. 284, 33079-33087.
78. Silverman, G. J., and Goodyear, C. S. (2006). Confounding B-cell defences: lessons from a staphy-lococcal superantigen. Nat. Rev. Immunol. 6, 465-475.
79. Sun, N. C., Ho, D. D., Sun, C. R., Liou, R. S., Gordon, W., Fung, M. S., et al. (1989). Generation and characterization of monoclonal antibodies to the putative CD4-binding domain of human immunodeficiency virus type 1 gp120. J. Virol. 63,3579-3585.
80. Takeda, A., Tuazon, C. U., and Ennis, F. A. (1988). Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science 242, 580-583.
81. Townsley-Fuchs, J., Kam, L., Fairhurst, R., Gange, S. J., Goodglick, L., Giorgi, J. V., et al. (1996). Human immunodeficiency virus-1 (HIV-1) gp120 superantigen-binding serum antibodies. A host factor in homosexual HIV-1 transmission. J. Clin. Invest. 98, 1794-1801.
82. Townsley-Fuchs, J., Neshat, M. S., Margolin, D. H., Braun, J., and Goodglick, L. (1997). HIV-1 gp120: a novel viral B cell superantigen. Int. Rev. Immunol. 14, 325-338.
83. Walker, L. M., Phogat, S. K., Chan-Hui, P. Y., Wagner, D., Phung, P., mimic CD4 binding. Science 333, 1633-1637.
84. Sharma, V., Heriot, W., Trisler, K., and Smider, V. (2009). A human germ line antibody light chain with hydrolytic properties associated with multimerization status. J. Biol Chem. 284, 33079-33087.
85. Silverman, G. J., and Goodyear, C. S. (2006). Confounding B-cell defences: lessons from a staphy-lococcal superantigen. Nat. Rev. Immunol. 6, 465-475.
86. Sun, N. C., Ho, D. D., Sun, C. R., Liou, R. S., Gordon, W., Fung, M. S., et al. (1989). Generation and characterization of monoclonal antibodies to the putative CD4-binding domain of human immunodeficiency virus type 1 gp120. J. Virol. 63,3579-3585.
87. Takeda, A., Tuazon, C. U., and Ennis, F. A. (1988). Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science 242, 580-583.
88. Townsley-Fuchs, J., Kam, L., Fairhurst, R., Gange, S. J., Goodglick, L., Giorgi, J. V., et al. (1996). Human immunodeficiency virus-1 (HIV-1) gp120 superantigen-binding serum antibodies. A host factor in homosexual HIV-1 transmission. J. Clin. Invest. 98, 1794-1801.
89. Townsley-Fuchs, J., Neshat, M. S., Margolin, D. H., Braun, J., and Goodglick, L. (1997). HIV-1 gp120: a novel viral B cell superantigen. Int. Rev. Immunol. 14, 325-338.
90. Walker, L. M., Phogat, S. K., Chan-Hui, P. Y., Wagner, D., Phung, P., Wu, X., Zhou, T., Zhu, J., Zhang, B., Georgiev, I., Wang, C., et al. (2011). Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333, 1593-1602.
91. Wyatt, R., Kwong, P. D., Desjardins, E., Sweet, R. W., Robinson, J., Hendrickson, W. A., et al. (1998). The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705-711.
92. Xiang, S. H., Kwong, P. D., Gupta, R., Rizzuto, C. D., Casper, D. J., Wyatt, R., et al. (2002). Mutagenic stabilization and/or disruption of a CD4-bound state reveals distinct conformations of the human immunodeficiency virus type 1 gp120 envelope glycoprotein. J. Virol. 76, 9888-9899.
93. Xiao, X., Chen, W., Feng, Y., Zhu, Z., Prabakaran, P., Wang, Y., et al. (2009). Germline-like predecessors of broadly neutralizing antibodies lack measurable binding to HIV-1 envelope glycoproteins: implications for evasion of immune responses and design of vaccine immunogens. Biochem. Biophys. Res. Commun. 390, 404-409.
94. Zhou, T., Georgiev, I., Wu, X., Yang, Z. Y., Dai, K., Finzi, A., et al. (2010). Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817.
95. Zhou, T., Xu, L., Dey, B., Hessell, A. J., Van Ryk, D., Xiang, S. H., et al. (2007). Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445, 732-737.
96. Zwick, M. B., Bonnycastle, L. L., Menendez, A., Irving, M. B., Barbas, C. F. 3rd., Parren, P. W., et al. (2001). Identification and characterization of a peptide that specifically binds the human, broadly neutralizing anti-human immunodeficiency virus type 1 antibody b12. J. Virol. 75, 6692-6699.