Antigenicity and immunogenicity of a trimeric envelope protein from an Indian clade C HIV-1 isolate

Journal of Biological Chemistry

Volumn 290, Issue 14, 2015, Pages 9195-9208

  Sneha Priya, Rangasamy ^a   Veena, Menon ^b   Kalisz, Irene ^b   Whitney, Stephen ^b   Priyanka, Dhopeshwarkar ^b   LaBranche, Celia C ^c   Sri Teja, Mullapudi ^a   Montefiori, David C ^c   Pal, Ranajit ^b   Mahalingam, Sundarasamy ^a   Kalyanaraman, Vaniambadi S ^b  

^a INDIAN INSTITUTE OF TECHNOLOGY MADRAS   (India)

^b ADVANCED BIOSCIENCE LABORATORIES INC   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODIES; DICHROISM; EPITOPES; MONOCLONAL ANTIBODIES; PROTEINS; PURIFICATION; VACCINES; VIRUSES;

CONDITIONED MEDIUM; CONFORMATIONAL INTEGRITY; ENVELOPE PROTEINS; EPITOPE SPECIFIC ANTIBODIES; HIGH AFFINITY BINDING; HUMAN IMMUNODEFICIENCY VIRUS TYPE-1; PURIFIED PROTEIN; STABLE STRUCTURES;

DISEASES;

CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; GLYCOPROTEIN GP 145; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGENICITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CD4+ T LYMPHOCYTE; CLADISTICS; CONTROLLED STUDY; FEMALE; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNIZATION; IMMUNOGENICITY; INDIA; INFECTION PREVENTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STABILITY; RABBIT; VIRUS ISOLATION; VIRUS STRAIN; ANIMAL; CHO CELL LINE; CIRCULAR DICHROISM; CRICETULUS; ENZYME LINKED IMMUNOSORBENT ASSAY; HAMSTER; HUMAN; IMMUNOLOGY; METABOLISM;

HUMAN IMMUNODEFICIENCY VIRUS 1; ORYCTOLAGUS CUNICULUS;

ANIMALS; BINDING SITES; CHO CELLS; CIRCULAR DICHROISM; CRICETINAE; CRICETULUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEK293 CELLS; HIV ANTIGENS; HIV-1; HUMANS; VIRAL ENVELOPE PROTEINS;

EID: 84926442279     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.621185     Document Type: Article

References (67)

1. Rosenberg, E. S., Billingsley, J. M., Caliendo, A. M., Boswell, S. L., Sax, P. E., Kalams, S. A., and Walker, B. D. (1997) Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia. Science 278, 1447-1450
2. Matano, T., Kobayashi, M., Igarashi, H., Takeda, A., Nakamura, H., Kano, M., Sugimoto, C., Mori, K., Iida, A., Hirata, T., Hasegawa, M., Yuasa, T., Miyazawa, M., Takahashi, Y., Yasunami, M., Kimura, A., O'Connor, D. H., Watkins, D. I., and Nagai, Y. (2004) Cytotoxic T lymphocyte-based control of simian immunodeficiency virus replication in a preclinical AIDS vaccine trial. J. Exp. Med. 199, 1709-1718
3. Amara, R. R., Sharma, S., Patel, M., Smith, J. M., Chennareddi, L., Herndon, J. G., and Robinson, H. L. (2005) Studies on the cross-clade and cross-species conservation of HIV-1 Gag-specific CD8 and CD4 T cell responses elicited by a clade B DNA/MVA vaccine in macaques. Virology 334, 124-133
4. Pitisuttithum, P., Gilbert, P., Gurwith, M., Heyward, W., Martin, M., van Griensven, F., Hu, D., Tappero, J. W., and Choopanya, K. (2006) Randomized, double-blind, placebo-controlled efficacy trial of a bivalent recombinant glycoprotein 120 HIV-1 vaccine among injection drug users in Bangkok, Thailand. J. Infect. Dis. 194, 1661-1671
5. Gilbert, P. B., Peterson, M. L., Follmann, D., Hudgens, M. G., Francis, D. P., Gurwith, M., Heyward, W. L., Jobes, D. V., Popovic, V., Self, S. G., Sinangil, F., Burke, D., and Berman, P. W. (2005) Correlation between immunologic responses to a recombinant glycoprotein 120 vaccine and incidence of HIV-1 infection in a phase 3 HIV-1 preventive vaccine trial. J. Infect. Dis. 191, 666-677
6. Walker, L. M., and Burton, D. R. (2010) Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr. Opin. Immunol. 22, 358-366
7. Kwong, P. D., Mascola, J. R., and Nabel, G. J. (2011) Rational design of vaccines to elicit broadly neutralizing antibodies to HIV-1. Cold Spring Harb. Perspect. Med. 1, a007278
8. Stamatatos, L., Morris, L., Burton, D. R., and Mascola, J. R. (2009) Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15, 866-870
9. Mascola, J. R., Lewis, M. G., Stiegler, G., Harris, D., VanCott, T. C., Hayes, D., Louder, M. K., Brown, C. R., Sapan, C. V., Frankel, S. S., Lu, Y., Robb, M. L., Katinger, H., and Birx, D. L. (1999) Protection of macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73, 4009-4018
10. Shibata, R., Igarashi, T., Haigwood, N., Buckler-White, A., Ogert, R., Ross, W., Willey, R., Cho, M. W., and Martin, M. A. (1999) Neutralizing antibody directed against the HIV-1 envelope glycoprotein can completely block HIV-1/SIV chimeric virus infections of macaque monkeys. Nat. Med. 5, 204-210
11. Baba, T. W., Liska, V., Hofmann-Lehmann, R., Vlasak, J., Xu, W., Ayehunie, S., Cavacini, L. A., Posner, M. R., Katinger, H., Stiegler, G., Bernacky, B. J., Rizvi, T. A., Schmidt, R., Hill, L. R., Keeling, M. E., Lu, Y., Wright, J. E., Chou, T. C., and Ruprecht, R. M. (2000) Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat. Med. 6, 200-206
12. Mascola, J. R., Stiegler, G., VanCott, T. C., Katinger, H., Carpenter, C. B., Hanson, C. E., Beary, H., Hayes, D., Frankel, S. S., Birx, D. L., and Lewis, M. G. (2000) Protection of macaques against vaginal transmission of a pathogenic HIV-1/SIV chimeric virus by passive infusion of neutralizing antibodies. Nat. Med. 6, 207-210
13. Parren, P. W., Marx, P. A., Hessell, A. J., Luckay, A., Harouse, J., Cheng-Mayer, C., Moore, J. P., and Burton, D. R. (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
14. Mascola, J. R. (2003) Defining the protective antibody response for HIV-1. Curr. Mol. Med. 3, 209-216
15. Hessell, A. J., Poignard, P., Hunter, M., Hangartner, L., Tehrani, D. M., Bleeker, W. K., Parren, P. W., Marx, P. A., and Burton, D. R. (2009) Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat. Med. 15, 951-954
16. Feng, Y., McKee, K., Tran, K., O'Dell, S., Schmidt, S. D., Phogat, A., Forsell, M. N., Karlsson Hedestam, G. B., Mascola, J. R., and Wyatt, R. T. (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
17. Bhattacharyya, S., Rajan, R. E., Swarupa, Y., Rathore, U., Verma, A., Udaykumar, R., and Varadarajan, R. (2010) Design of a non-glycosylated outer domain-derived HIV-1 gp120 immunogen that binds to CD4 and induces neutralizing antibodies. J. Biol. Chem. 285, 27100-27110
18. McGuire, A. T., Hoot, S., Dreyer, A. M., Lippy, A., Stuart, A., Cohen, K. W., Jardine, J., Menis, S., Scheid, J. F., West, A. P., Schief, W. R., and Stamatatos, L. (2013) Engineering HIV envelope protein to activate germline B cell receptors of broadly neutralizing anti-CD4 binding site antibodies. J. Exp. Med. 210, 655-663
19. Kovacs, J. M., Nkolola, J. P., Peng, H., Cheung, A., Perry, J., Miller, C. A., Seaman, M. S., Barouch, D. H., and Chen, B. (2012) HIV-1 envelope trimer elicits more potent neutralizing antibody responses than monomeric gp120. Proc. Natl. Acad. Sci. U.S.A. 109, 12111-12116
20. Sanders, R. W., Derking, R., Cupo, A., Julien, J.-P., Yasmeen, A., de Val, N., Kim, H. J., Blattner, C., de la Peña, A. T., Korzun, J., Golabek, M., de Los Reyes, K., Ketas, T. J., van Gils, M. J., King, C. R., Wilson, I. A., Ward, A. B., Klasse, P. J., and Moore, J. P. (2013) A next-generation cleaved, soluble HIV-1 Env trimer, BG505 SOSIP.664 gp140, expresses multiple epitopes for broadly neutralizing but not non-neutralizing antibodies. PLoS Pathog. 9, e1003618
21. Rerks-Ngarm, S., Pitisuttithum, P., Nitayaphan, S., Kaewkungwal, J., Chiu, J., Paris, R., Premsri, N., Namwat, C., de Souza, M., Adams, E., Benenson, M., Gurunathan, S., Tartaglia, J., McNeil, J. G., Francis, D. P., Stablein, D., Birx, D. L., Chunsuttiwat, S., Khamboonruang, C., Thongcharoen, P., Robb, M. L., Michael, N. L., Kunasol, P., and Kim, J. H. (2009) Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361, 2209-2220
22. Haynes, B. F., Gilbert, P. B., McElrath, M. J., Zolla-Pazner, S., Tomaras, G. D., Alam, S. M., Evans, D. T., Montefiori, D. C., Karnasuta, C., Sutthent, R., Liao, H.-X., DeVico, A. L., Lewis, G. K., Williams, C., Pinter, A., Fong, Y., Janes, H., DeCamp, A., Huang, Y., Rao, M., Billings, E., Karasavvas, N., Robb, M. L., Ngauy, V., de Souza, M. S., Paris, R., Ferrari, G., Bailer, R. T., Soderberg, K. A., Andrews, C., Berman, P. W., Frahm, N., De Rosa, S. C., Alpert, M. D., Yates, N. L., Shen, X., Koup, R. A., Pitisuttithum, P., Kaewkungwal, J., Nitayaphan, S., Rerks-Ngarm, S., Michael, N. L., Kim, J. H., Rosa, S. C. De, and Alam, M. (2012) Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366, 1275-1286
23. Gottardo, R., Bailer, R. T., Korber, B. T., Gnanakaran, S., Phillips, J., Shen, X., Tomaras, G. D., Turk, E., Imholte, G., Eckler, L., Wenschuh, H., Zerweck, J., Greene, K., Gao, H., Berman, P. W., Francis, D., Sinangil, F., Lee, C., Nitayaphan, S., Rerks-Ngarm, S., Kaewkungwal, J., Pitisuttithum, P., Tartaglia, J., Robb, M. L., Michael, N. L., Kim, J. H., Zolla-Pazner, S., Haynes, B. F., Mascola, J. R., Self, S., Gilbert, P., and Montefiori, D. C. (2013) Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One 8, e75665
24. VanCott, T. C., Veit, S. C., Kalyanaraman, V., Earl, P., and Birx, D. L. (1995) Characterization of a soluble, oligomeric HIV-1 gp160 protein as a potential immunogen. J. Immunol. Methods 183, 103-117
25. Selvarajah, S., Puffer, B., Pantophlet, R., Law, M., Doms, R. W., and Burton, D. R. (2005) Comparing antigenicity and immunogenicity of engineered gp120. J. Virol. 79, 12148-12163
26. Kang, Y. K., Andjelic, S., Binley, J. M., Crooks, E. T., Franti, M., Iyer, S. P., Donovan, G. P., Dey, A. K., Zhu, P., Roux, K. H., Durso, R. J., Parsons, T. F., Maddon, P. J., Moore, J. P., and Olson, W. C. (2009) Structural and immunogenicity studies of a cleaved, stabilized envelope trimer derived from subtype A HIV-1. Vaccine 27, 5120-5132
27. Kong, L., and Sattentau, Q. J. (2012) Antigenicity and immunogenicity in HIV-1 antibody-based vaccine design. J. AIDS Clin. Res. S8, 3
28. Visciano, M. L., Tagliamonte, M., Stewart-Jones, G., Heyndrickx, L., Vanham, G., Jansson, M., Fomsgaard, A., Grevstad, B., Ramaswamy, M., Buonaguro, F. M., Tornesello, M. L., Biswas, P., Scarlatti, G., and Buonaguro, L. (2013) Characterization of humoral responses to soluble trimeric HIV gp140 from a clade A Ugandan field isolate. J. Transl. Med. 11, 165
29. Liao, H.-X., Tsao, C.-Y., Alam, S. M., Muldoon, M., Vandergrift, N., Ma, B.-J., Lu, X., Sutherland, L. L., Scearce, R. M., Bowman, C., Parks, R., Chen, H., Blinn, J. H., Lapedes, A., Watson, S., Xia, S.-M., Foulger, A., Hahn, B. H., Shaw, G. M., Swanstrom, R., Montefiori, D. C., Gao, F., Haynes, B. F., and Korber, B. (2013) Antigenicity and immunogenicity of transmitted/founder, consensus, and chronic envelope glycoproteins of human immunodeficiency virus type 1. J. Virol. 87, 4185-4201
30. Polonis, V., Wieczorek, L., Kalyanaraman, V., Matyas, G., Whitney, S., Williams, C., Tovanabutra, S., Sanders-buell, E., Wesberry, M., Ochsenbauer, C., Chenine, A., Rao, M., Tong, T., Alving, C., Cheng, H., Zollapazner, S., Michael, N., Vancott, T., and Marovich, M. (2012) Antigenicity and immunogenicity of a novel, acute HIV-1 Tanzanian Subtype C gp145 envelope protein for clinical development. Retrovirology 9, Suppl. 2, P323
31. Dietrich, U., Grez, M., von Briesen, H., Panhans, B., Geissendörfer, M., Kudie;hnel, H., Maniar, J., Mahambre, G., Becker, W. B., and Becker, M. L. (1993) HIV-1 strains from India are highly divergent from prototypic African and US/European strains, but are linked to a South African isolate. AIDS 7, 23-27
32. Kulkarni, S. S., Lapedes, A., Tang, H., Gnanakaran, S., Daniels, M. G., Zhang, M., Bhattacharya, T., Li, M., Polonis, V. R., McCutchan, F. E., Morris, L., Ellenberger, D., Butera, S. T., Bollinger, R. C., Korber, B. T., Paranjape, R. S., and Montefiori, D. C. (2009) Highly complex neutralization determinants on a monophyletic lineage of newly transmitted subtype C HIV-1 Env clones from India. Virology 385, 505-520
33. Shen, C., Craigo, J., Ding, M., Chen, Y., and Gupta, P. (2011) Origin and dynamics of HIV-1 subtype C infection in India. PLoS One 6, e25956
34. Seaman, M. S., Janes, H., Hawkins, N., Grandpre, L. E., Devoy, C., Giri, A., Coffey, R. T., Harris, L., Wood, B., Daniels, M. G., Bhattacharya, T., Lapedes, A., Polonis, V. R., McCutchan, F. E., Gilbert, P. B., Self, S. G., Korber, B. T., Montefiori, D. C., and Mascola, J. R. (2010) Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84, 1439-1452
35. 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., and Burton, D. R. (2004) Comprehensive cross-clade neutralization analysis of a panel of anti-human immunodeficiency virus type 1 monoclonal antibodies. J. Virol. 78, 13232-13252
36. Ringe, R., Thakar, M., and Bhattacharya, J. (2010) Variations in autologous neutralization and CD4 dependence of b12 resistant HIV-1 clade C env clones obtained at different time points from antiretroviral naïve Indian patients with recent infection. Retrovirology 7, 76
37. Gharu, L., Ringe, R., and Bhattacharya, J. (2011) HIV-1 clade C envelopes obtained from late stage symptomatic Indian patients varied in their ability towards relative CD4 usages and sensitivity to CCR5 antagonist TAK-779. Virus Res. 158, 216-224
38. Huang, J., Ofek, G., Laub, L., Louder, M. K., Doria-Rose, N. A., Longo, N. S., Imamichi, H., Bailer, R. T., Chakrabarti, B., Sharma, S. K., Alam, S. M., Wang, T., Yang, Y., Zhang, B., Migueles, S. A., Wyatt, R., Haynes, B. F., Kwong, P. D., Mascola, J. R., and Connors, M. (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491, 406-412
39. Mochizuki, N., Otsuka, N., Matsuo, K., Shiino, T., Kojima, A., Kurata, T., Sakai, K., Yamamoto, N., Isomura, S., Dhole, T. N., Takebe, Y., Matsuda, M., and Tatsumi, M. (1999) An infectious DNA clone of HIV type 1 subtype C. AIDS Res. Hum. Retroviruses 15, 1321-1324
40. Walker, L. M., Phogat, S. K., Chan-Hui, P.-Y., Wagner, D., Phung, P., Goss, J. L., Wrin, T., Simek, M. D., Fling, S., Mitcham, J. L., Lehrman, J. K., Priddy, F. H., Olsen, O. A., Frey, S. M., Hammond, P. W., Protocol G Principal Investigators, Kaminsky, S., Zamb, T., Moyle, M., Koff, W. C., Poignard, P., and Burton, D. R. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289
41. Stiegler, G., Kunert, R., Purtscher, M., Wolbank, S., Voglauer, R., Steindl, F., and Katinger, H. (2001) A potent cross-clade neutralizing human monoclonal antibody against a novel epitope on gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 17, 1757-1765
42. Purtscher, M., Trkola, A., Gruber, G., Buchacher, A., Predl, R., Steindl, F., Tauer, C., Berger, R., Barrett, N., and Jungbauer, A. (1994) A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 10, 1651-1658
43. Thali, M., Moore, J. P., Furman, C., Charles, M., Ho, D. D., Robinson, J., and Sodroski, J. (1993) Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 67, 3978-3988
44. Buchacher, A., Predl, R., Strutzenberger, K., Steinfellner, W., Trkola, A., Purtscher, M., Gruber, G., Tauer, C., Steindl, F., and Jungbauer, A. (1994) Generation of human monoclonal antibodies against HIV-1 proteins; electrofusion and Epstein-Barr virus transformation for peripheral blood lymphocyte immortalization. AIDS Res. Hum. Retroviruses 10, 359-369
45. Burton, D. R., Barbas, C. F., 3rd, Persson, M. A., Koenig, S., Chanock, R. M., and Lerner, R. A. (1991) A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc. Natl. Acad. Sci. U.S.A. 88, 10134-10137
46. Wu, X., Yang, Z.-Y., Li, Y., Hogerkorp, C.-M., Schief, W. R., Seaman, M. S., Zhou, T., Schmidt, S. D., Wu, L., Xu, L., Longo, N. S., McKee, K., O'Dell, S., Louder, M. K., Wycuff, D. L., Feng, Y., Nason, M., Doria-Rose, N., Connors, M., Kwong, P. D., Roederer, M., Wyatt, R. T., Nabel, G. J., and Mascola, J. R. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861
47. Diskin, R., Scheid, J. F., Marcovecchio, P. M., West, A. P., Jr., Klein, F., Gao, H., Gnanapragasam, P. N., Abadir, A., Seaman, M. S., Nussenzweig, M. C., and Bjorkman, P. J. (2011) Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334, 1289-1293
48. Stamatatos, L., Lim, M., and Cheng-Mayer, C. (2000) Generation and structural analysis of soluble oligomeric gp140 envelope proteins derived from neutralization-resistant and neutralization-susceptible primary HIV type 1 isolates. AIDS Res. Hum. Retroviruses 16, 981-994
49. Platt, E. J., Wehrly, K., Kuhmann, S. E., Chesebro, B., and 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
50. Brown, B. K., Darden, J. M., Tovanabutra, S., Oblander, T., Frost, J., Sanders-Buell, E., de Souza, M. S., Birx, D. L., McCutchan, F. E., and Polonis, V. R. (2005) Biologic and genetic characterization of a panel of 60 human immunodeficiency virus type 1 isolates, representing clades A, B, C, D, CRF01-AE, and CRF02-AG, for the development and assessment of candidate vaccines. J. Virol. 79, 6089-6101
51. Chung, H. K., Suschak, J., Galmin, L., Rose, N., and Pal, R. (2010) Characterization of a SHIV162P3 variant evolved in an infected rhesus macaque with persistent plasma viremia. Virus Res. 151, 229-234
52. Sellhorn, G., Kraft, Z., Caldwell, Z., Ellingson, K., Mineart, C., Seaman, M. S., Montefiori, D. C., Lagerquist, E., and Stamatatos, L. (2012) Engineering, expression, purification, and characterization of stable clade A/B recombinant soluble heterotrimeric gp140 proteins. J. Virol. 86, 128-142
53. Chen, B., Zhou, G., Kim, M., Chishti, Y., Hussey, R. E., Ely, B., Skehel, J. J., Reinherz, E. L., Harrison, S. C., and Wiley, D. C. (2000) Expression, purification, and characterization of gp160e, the soluble, trimeric ectodomain of the simian immunodeficiency virus envelope glycoprotein, gp160. J. Biol. Chem. 275, 34946-34953
54. Kraus, M. H., Parrish, N. F., Shaw, K. S., Decker, J. M., Keele, B. F., Salazar-Gonzalez, J. F., Grayson, T., McPherson, D. T., Ping, L. H., Anderson, J. A., Swanstrom, R., Williamson, C., Shaw, G. M., and Hahn, B. H. (2010) A rev1-vpu polymorphism unique to HIV-1 subtype A and C strains impairs envelope glycoprotein expression from rev-vpu-env cassettes and reduces virion infectivity in pseudotyping assays. Virology 397, 346-357
55. Srivastava, I. K., Kan, E., Sun, Y., Sharma, V. A., Cisto, J., Burke, B., Lian, Y., Hilt, S., Biron, Z., Hartog, K., Stamatatos, L., Diaz-Avalos, R., Cheng, R. H., Ulmer, J. B., and Barnett, S. W. (2008) Comparative evaluation of trimeric envelope glycoproteins derived from subtype C and B HIV-1 R5 isolates. Virology 372, 273-290
56. Thali, M., Olshevsky, U., Furman, C., Gabuzda, D., Posner, M., and Sodroski, J. (1991) Characterization of a discontinuous human immunodeficiency virus type 1 gp120 epitope recognized by a broadly reactive neutralizing human monoclonal antibody. J. Virol. 65, 6188-6193
57. Sanders, R. W., Venturi, M., Schiffner, L., Kalyanaraman, R., Katinger, H., Lloyd, K. O., Kwong, P. D., and Moore, J. P. (2002) The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76, 7293-7305
58. Davenport, T. M., Friend, D., Ellingson, K., Xu, H., Caldwell, Z., Sellhorn, G., Kraft, Z., Strong, R. K., and Stamatatos, L. (2011) Binding interactions between soluble HIV envelope glycoproteins and quaternary-structurespecific monoclonal antibodies PG9 and PG16. J. Virol. 85, 7095-7107
59. Smith, D. H., Winters-Digiacinto, P., Mitiku, M., O'Rourke, S., Sinangil, F., Wrin, T., Montefiori, D. C., and Berman, P. W. (2010) Comparative immunogenicity of HIV-1 clade C envelope proteins for prime/boost studies. PLoS One 5, e12076
60. Tong, T., Crooks, E. T., Osawa, K., Robinson, J. E., Barnes, M., Apetrei, C., and Binley, J. M. (2014) Multi-parameter exploration of HIV-1 virus-like particles as neutralizing antibody immunogens in guinea pigs, rabbits and macaques. Virology 456-457, 55-69
61. Bontjer, I., Melchers, M., Tong, T., van Montfort, T., Eggink, D., Montefiori, D., Olson, W. C., Moore, J. P., Binley, J. M., Berkhout, B., and Sanders, R. W. (2013) Comparative immunogenicity of evolved V1V2-deleted HIV-1 envelope glycoprotein trimers. PLoS One 8, e67484
62. Montefiori, D. C. (2005) Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. Curr. Protoc. Immunol. Chapter 12, Unit 12.11
63. deCamp, A., Hraber, P., Bailer, R. T., Seaman, M. S., Ochsenbauer, C., Kappes, J., Gottardo, R., Edlefsen, P., Self, S., Tang, H., Greene, K., Gao, H., Daniell, X., Sarzotti-Kelsoe, M., Gorny, M. K., Zolla-Pazner, S., LaBranche, C. C., Mascola, J. R., Korber, B. T., and Montefiori, D. C. (2014) Global panel of HIV-1 Env reference strains for standardized assessments of vaccine-elicited neutralizing antibodies. J. Virol. 88, 2489-2507
64. Kim, M., Qiao, Z.-S., Montefiori, D. C., Haynes, B. F., Reinherz, E. L., and Liao, H.-X. (2005) Comparison of HIV Type 1 ADA gp120 monomers versus gp140 trimers as immunogens for the induction of neutralizing antibodies. AIDS Res. Hum. Retroviruses 21, 58-67
65. Vaine, M., Wang, S., Crooks, E. T., Jiang, P., Montefiori, D. C., Binley, J., and Lu, S. (2008) Improved induction of antibodies against key neutralizing epitopes by human immunodeficiency virus type 1 gp120 DNA primeprotein boost vaccination compared to gp120 protein-only vaccination. J. Virol. 82, 7369-7378
66. Klein, F., Diskin, R., Scheid, J. F., Gaebler, C., Mouquet, H., Georgiev, I. S., Pancera, M., Zhou, T., Incesu, R. B., Fu, B. Z., Gnanapragasam, P. N., Oliveira, T. Y., Seaman, M. S., Kwong, P. D., Bjorkman, P. J., and Nussenzweig, M. C. (2013) Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153, 126-138
67. Derdeyn, C. A., Moore, P. L., and Morris, L. (2014) Development of broadly neutralizing antibodies from autologous neutralizing antibody responses in HIV infection. Curr. Opin. HIV AIDS 9, 210-216