Eliciting neutralizing antibodies with gp120 outer domain constructs based on M-group consensus sequence

Virology

Volumn 462-463, Issue , 2014, Pages 363-376

  Qin, Yali ^a   Banasik, Marisa ^a   Kim, SoonJeung ^d   Penn Nicholson, Adam ^e   Habte, Habtom H ^a   LaBranche, Celia ^c   Montefiori, David C ^c   Wang, Chong ^a,b   Cho, Michael W ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b Department of Statistics Center for Statistics and Applications in Forensic Evidence Iowa State University 2438 Osborn Dr Ames   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

gp120; HIV 1; Neutralizing antibody; Outer domain; V3; Vaccine

Indexed keywords

EPITOPE; GLYCOPROTEIN GP 120; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; NEUTRALIZING ANTIBODY; VACCINE;

ANIMAL; ARTICLE; BLOOD; CONSENSUS SEQUENCE; EPITOPE MAPPING; FEMALE; GENETICS; GP120; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; OUTER DOMAIN; RABBIT; V3;

GP120; HIV-1; NEUTRALIZING ANTIBODY; OUTER DOMAIN; V3; VACCINE;

ANIMALS; ANTIBODIES, NEUTRALIZING; CONSENSUS SEQUENCE; EPITOPE MAPPING; EPITOPES; FEMALE; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV-1; RABBITS;

EID: 84907284878     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2014.06.006     Document Type: Article

References (80)

1. Barbas, C.F., Björling, E., Chiodi, F., Dunlop, N., Cababa, D., Jones, T.M., Zebedee, S.L., Persson, M.A., Nara, P.L., Norrby, E., Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc. Natl. Acad. Sci. U.S.A. 89 (1992), 9339–9343.
2. Bhattacharyya, S., Rajan, R.E., Swarupa, Y., Rathore, U., Verma, A., Udaykumar, R., Varadarajan, R., Design of a non-glycosylated outer domain-derived HIV-1 gp120 immunogen that binds to CD4 and induces neutralizing antibodies. zJ. Biol. Chem. 285 (2010), 27100–27110.
3. Blattner, C., Lee, J.H., Sliepen, K., Derking, R., Falkowska, E., la Peña, de, A.T., Cupo, A., Julien, J.-P., van Gils, M., Lee, P.S., Peng, W., Paulson, J.C., Poignard, P., Burton, D.R., Moore, J.P., Sanders, R.W., Wilson, I.A., Ward, A.B., Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env Trimers. Immunity 40 (2014), 669–680.
4. Buchacher, A., Predl, R., Strutzenberger, K., Steinfellner, W., Trkola, A., Purtscher, M., Gruber, G., Tauer, C., Steindl, F., Jungbauer, A., 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 (1994), 359–369.
5. Burton, D.R., Barbas, C.F., Persson, M.A., Koenig, S., Chanock, R.M., Lerner, R.A., 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 (1991), 10134–10137.
6. Burton, D.R., Pyati, J., Koduri, R., Sharp, S.J., Thornton, G.B., Parren, P.W., Sawyer, L.S., Hendry, R.M., Dunlop, N., Nara, P.L., Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266 (1994), 1024–1027.
7. Center, R.J., Leapman, R.D., Lebowitz, J., Arthur, L.O., Earl, P.L., Moss, B., Oligomeric structure of the human immunodeficiency virus type 1 envelope protein on the virion surface. J. Virol. 76 (2002), 7863–7867.
8. Center, R.J., Schuck, P., Leapman, R.D., Arthur, L.O., Earl, P.L., Moss, B., Lebowitz, J., Oligomeric structure of virion-associated and soluble forms of the simian immunodeficiency virus envelope protein in the prefusion activated conformation. Proc. Natl. Acad. Sci. U.S.A. 98 (2001), 14877–14882.
9. Chen, H., Xu, X., Jones, I.M., Immunogenicity of the outer domain of a HIV-1 clade C gp120. Retrovirology, 4, 2007, 33.
10. Chen, H., Xu, X., Lin, H.-H., Chen, S.-H., Forsman, A., Aasa-Chapman, M., Jones, I.M., Mapping the immune response to the outer domain of a human immunodeficiency virus-1 clade C gp120. J. Gen. Virol. 89 (2008), 2597–2604.
11. Cho, M.W., Teterina, N., Egger, D., Bienz, K., Ehrenfeld, E., Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology 202 (1994), 129–145.
12. Conley, A.J., Gorny, M.K., Kessler, J.A., Boots, L.J., Ossorio-Castro, M., Koenig, S., Lineberger, D.W., Emini, E.A., Williams, C., Zolla-Pazner, S., Neutralization of primary human immunodeficiency virus type 1 isolates by the broadly reactive anti-V3 monoclonal antibody, 447-52D. J. Virol. 68 (1994), 6994–7000.
13. Crawford, J.M., Earl, P.L., Moss, B., Reimann, K.A., Wyand, M.S., Manson, K.H., Bilska, M., Zhou, J.T., Pauza, C.D., Parren, P.W., Burton, D.R., Sodroski, J.G., Letvin, N.L., Montefiori, D.C., Characterization of primary isolate-like variants of simian-human immunodeficiency virus. J. Virol. 73 (1999), 10199–10207.
14. Diskin, R., Scheid, J.F., Marcovecchio, P.M., West, A.P., Klein, F., Gao, H., Gnanapragasam, P.N.P., Abadir, A., Seaman, M.S., Nussenzweig, M.C., Bjorkman, P.J., Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334 (2011), 1289–1293.
15. Etemad-Moghadam, B., Sun, Y., Nicholson, E.K., Karlsson, G.B., Schenten, D., Sodroski, J., Determinants of neutralization resistance in the envelope glycoproteins of a simian-human immunodeficiency virus passaged in vivo. J. Virol. 73 (1999), 8873–8879.
16. Falkowska, E., Le, K.M., Ramos, A., Doores, K.J., Lee, J.H., Blattner, C., Ramirez, A., Derking, R., van Gils, M.J., Liang, C.-H., McBride, R., Bredow, von, B., Shivatare, S.S., Wu, C.-Y., Chan-Hui, P.-Y., Liu, Y., Feizi, T., Zwick, M.B., Koff, W.C., Seaman, M.S., Swiderek, K., Moore, J.P., Evans, D., Paulson, J.C., Wong, C.-H., Ward, A.B., Wilson, I.A., Sanders, R.W., Poignard, P., Burton, D.R., Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on Cleaved Envelope Trimers. Immunity 40 (2014), 657–668.
17. Gao, F., Korber, B.T., Weaver, E., Liao, H.-X., Hahn, B.H., Haynes, B.F., Centralized immunogens as a vaccine strategy to overcome HIV-1 diversity. Expert Rev. Vaccines 3 (2004), S161–8.
18. Gao, F., Weaver, E.A., Lu, Z., Li, Y., Liao, H.-X., Ma, B., Alam, S.M., Scearce, R.M., Sutherland, L.L., Yu, J.-S., Decker, J.M., Shaw, G.M., Montefiori, D.C., Korber, B.T., Hahn, B.H., Haynes, B.F., Antigenicity and immunogenicity of a synthetic human immunodeficiency virus type 1 group m consensus envelope glycoprotein. J. Virol. 79 (2005), 1154–1163.
19. Gaschen, B., Taylor, J., Yusim, K., Foley, B., Gao, F., Lang, D., Novitsky, V., Haynes, B., Hahn, B.H., Bhattacharya, T., Korber, B., Diversity considerations in HIV-1 vaccine selection. Science 296 (2002), 2354–2360.
20. Gorny, M.K., Conley, A.J., Karwowska, S., Buchbinder, A., Xu, J.Y., Emini, E.A., Koenig, S., Zolla-Pazner, S., Neutralization of diverse human immunodeficiency virus type 1 variants by an anti-V3 human monoclonal antibody. J. Virol. 66 (1992), 7538–7542.
21. Gorny, M.K., VanCott, T.C., Hioe, C., Israel, Z.R., Michael, N.L., Conley, A.J., Williams, C., Kessler, J.A., Chigurupati, P., Burda, S., Zolla-Pazner, S., Human monoclonal antibodies to the V3 loop of HIV-1 with intra- and interclade cross-reactivity. J. Immunol. 159 (1997), 5114–5122.
22. Gorny, M.K., Xu, J.Y., Karwowska, S., Buchbinder, A., Zolla-Pazner, S., Repertoire of neutralizing human monoclonal antibodies specific for the V3 domain of HIV-1 gp120. J. Immunol. 150 (1993), 635–643.
23. Haynes, B.F., Montefiori, D.C., Aiming to induce broadly reactive neutralizing antibody responses with HIV-1 vaccine candidates. Expert Rev. Vaccines 5 (2006), 579–595.
24. Hoxie, J.A., Toward an antibody-based HIV-1 vaccine. Annu. Rev. Med. 61 (2010), 135–152.
25. 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., Connors, M., Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491 (2012), 406–412.
26. Jardine, J., Julien, J.-P., Menis, S., Ota, T., Kalyuzhniy, O., McGuire, A., Sok, D., Huang, P.-S., Macpherson, S., Jones, M., Nieusma, T., Mathison, J., Baker, D., Ward, A.B., Burton, D.R., Stamatatos, L., Nemazee, D., Wilson, I.A., Schief, W.R., Rational HIV immunogen design to target specific Germline B cell receptors. Science 340 (2013), 711–716.
27. Joyce, M.G., Kanekiyo, M., Xu, L., Biertümpfel, C., Boyington, J.C., Moquin, S., Shi, W., Wu, X., Yang, Y., Yang, Z.-Y., Zhang, B., Zheng, A., Zhou, T., Zhu, J., Mascola, J.R., Kwong, P.D., Nabel, G.J., Outer domain of HIV-1 gp120: antigenic optimization, structural malleability, and crystal structure with antibody VRC-PG04. J. Virol. 87 (2013), 2294–2306.
28. Julien, J.-P., Cupo, A., Sok, D., Stanfield, R.L., Lyumkis, D., Deller, M.C., Klasse, P.J., Burton, D.R., Sanders, R.W., Moore, J.P., Ward, A.B., Wilson, I.A., Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342 (2013), 1477–1483.
29. Karlsson Hedestam, G.B., Fouchier, R.A.M., Phogat, S., Burton, D.R., Sodroski, J., Wyatt, R.T., The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6 (2008), 143–155.
30. Khayat, R., Lee, J.H., Julien, J.-P., Cupo, A., Klasse, P.J., Sanders, R.W., Moore, J.P., Wilson, I.A., Ward, A.B., Structural characterization of cleaved, soluble HIV-1 envelope glycoprotein trimers. J. Virol. 87 (2013), 9865–9872.
31. Klein, F., Gaebler, C., Mouquet, H., Sather, D.N., Lehmann, C., Scheid, J.F., Kraft, Z., Liu, Y., Pietzsch, J., Hurley, A., Poignard, P., Feizi, T., Morris, L., Walker, B.D., Fätkenheuer, G., Seaman, M.S., Stamatatos, L., Nussenzweig, M.C., Broad neutralization by a combination of antibodies recognizing the CD4 binding site and a new conformational epitope on the HIV-1 envelope protein. J. Exp. Med. 209 (2012), 1469–1479.
32. Klein, J.S., Bjorkman, P.J., Few and far between: how HIV may be evading antibody avidity. PLoS Pathog., 6, 2010, e1000908.
33. Klein, J.S., Gnanapragasam, P.N.P., Galimidi, R.P., Foglesong, C.P., West, A.P., Bjorkman, P.J., Examination of the contributions of size and avidity to the neutralization mechanisms of the anti-HIV antibodies b12 and 4E10. PNAS 106 (2009), 7385–7390.
34. Kwong, P.D., Mascola, J.R., Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37 (2012), 412–425.
35. Kwong, P.D., Mascola, J.R., Nabel, G.J., Rational design of vaccines to elicit broadly neutralizing antibodies to HIV-1. Cold Spring Harb. Perspect. Med., 1, 2011, a007278.
36. Kwong, P.D., Mascola, J.R., Nabel, G.J., Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13 (2013), 693–701.
37. Kwong, P.D., Wyatt, R., Robinson, J., Sweet, R.W., Sodroski, J., Hendrickson, W.A., Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393 (1998), 648–659.
38. Kwong, P.D., Wyatt, R., Sattentau, Q.J., Sodroski, J., Hendrickson, W.A., Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus. J. Virol. 74 (2000), 1961–1972.
39. LaBranche, C.C., Galasso, G., Moore, J.P., Bolognesi, D.P., Hirsch, M.S., Hammer, S.M., HIV fusion and its inhibition. Antivir. Res. 50 (2001), 95–115.
40. Li, M., Gao, F., Mascola, J.R., Stamatatos, L., Polonis, V.R., Koutsoukos, M., Voss, G., Goepfert, P., Gilbert, P., Greene, K.M., Bilska, M., Kothe, D.L., Salazar-Gonzalez, J.F., Wei, X., Decker, J.M., Hahn, B.H., Montefiori, D.C., 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 (2005), 10108–10125.
41. Lyumkis, D., Julien, J.P., de Val, N., Cupo, A., Potter, C.S., Klasse, P.J., Burton, D.R., Sanders, R.W., Moore, J.P., Carragher, B., Wilson, I.A., Ward, A.B., Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 Envelope Trimer. Science 342 (2013), 1484–1490.
42. Marchal, I., Jarvis, D.L., Cacan, R., Verbert, A., Glycoproteins from insect cells: sialylated or not?. Biol. Chem. 382 (2001), 151–159.
43. Marcinkiewicz, J., Polewska, A., Knapczyk, J., Immunoadjuvant properties of chitosan. Arch. Immunol. Ther. Exp. (Warsz.) 39 (1991), 127–132.
44. 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., Birx, D.L., Protection of Macaques against pathogenic simian/human immunodeficiency virus 89.6PD by passive transfer of neutralizing antibodies. J. Virol. 73 (1999), 4009–4018.
45. Mascola, J.R., Montefiori, D.C., The role of antibodies in HIV vaccines. Annu. Rev. Immunol. 28 (2010), 413–444.
46. + T-lymphoblastoid cell assay system. PLoS ONE, 8, 2013, e77756.
47. Montefiori, D.C., Evaluating neutralizing antibodies against HIV, SIV, and SHIV in luciferase reporter gene assays. (Chapter 12, Unit) Curr. Protoc. Immunol., 12, 2005, 11.
48. Muster, T., Guinea, R., Trkola, A., Purtscher, M., Klima, A., Steindl, F., Palese, P., Katinger, H., Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J. Virol. 68 (1994), 4031–4034.
49. Nabel, G.J., Kwong, P.D., Mascola, J.R., Progress in the rational design of an AIDS vaccine. Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci. 366 (2011), 2759–2765.
50. Nickle, D.C., Consensus and ancestral state HIV vaccines. Science 299 (2003), 1515c–1518.
51. Nyambi, P.N., Gorny, M.K., Bastiani, L., van der Groen, G., Williams, C., Zolla-Pazner, S., Mapping of epitopes exposed on intact human immunodeficiency virus type 1 (HIV-1) virions: a new strategy for studying the immunologic relatedness of HIV-1. J. Virol. 72 (1998), 9384–9391.
52. Pantophlet, R., Burton, D.R., GP120: target for neutralizing HIV-1 antibodies. Annu. Rev. Immunol. 24 (2006), 739–769.
53. Purtscher, M., Trkola, A., Gruber, G., Buchacher, A., Predl, R., Steindl, F., Tauer, C., Berger, R., Barrett, N., Jungbauer, A., A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res. Hum. Retroviruses 10 (1994), 1651–1658.
54. Roben, P., Moore, J.P., Thali, M., Sodroski, J., Barbas, C.F., Burton, D.R., 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 (1994), 4821–4828.
55. Ross, A.L., Bråve, A., Scarlatti, G., Manrique, A., Buonaguro, L., Progress towards development of an HIV vaccine: report of the AIDS Vaccine 2009 Conference. Lancet Infect. Dis.(10), 2010, 305–316.
56. Scharf, L., Scheid, J.F., Lee, J.H., West, A.P., Chen, C., Gao, H., Gnanapragasam, P.N.P., Mares, R., Seaman, M.S., Ward, A.B., Nussenzweig, M.C., Bjorkman, P.J., Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 Envelope Spike. Cell Rep. 7 (2014), 785–795.
57. Scheid, J.F., Mouquet, H., Ueberheide, B., Diskin, R., Klein, F., Oliveira, T.Y.K., Pietzsch, J., Fenyo, D., Abadir, A., Velinzon, K., Hurley, A., Myung, S., Boulad, F., Poignard, P., Burton, D.R., Pereyra, F., Ho, D.D., Walker, B.D., Seaman, M.S., Bjorkman, P.J., Chait, B.T., Nussenzweig, M.C., Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333 (2011), 1633–1637.
58. Seferian, P.G., Martinez, M.L., Immune stimulating activity of two new chitosan containing adjuvant formulations. Vaccine 19 (2000), 661–668.
59. Singla, A.K., Chawla, M., Chitosan: some pharmaceutical and biological aspects–an update. J. Pharm. Pharmacol. 53 (2001), 1047–1067.
60. Stiegler, G., Kunert, R., Purtscher, M., Wolbank, S., Voglauer, R., Steindl, F., Katinger, H., 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 (2001), 1757–1765.
61. Sullivan, N., Sun, Y., Sattentau, Q., Thali, M., Wu, D., Denisova, G., Gershoni, J., Robinson, J., Moore, J., Sodroski, J., CD4-Induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization. J. Virol. 72 (1998), 4694–4703.
62. Thali, M., Moore, J.P., Furman, C., Charles, M., Ho, D.D., Robinson, J., Sodroski, J., Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 67 (1993), 3978–3988.
63. Trkola, A., Dragic, T., Arthos, J., Binley, J.M., Olson, W.C., Allaway, G.P., Cheng-Mayer, C., Robinson, J., Maddon, P.J., Moore, J.P., CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384 (1996), 184–187.
64. Trkola, A., Purtscher, M., Muster, T., Ballaun, C., Buchacher, A., Sullivan, N., Srinivasan, K., Sodroski, J., Moore, J.P., Katinger, H., Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70 (1996), 1100–1108.
65. Vaine, M., Wang, S., Crooks, E.T., Jiang, P., Montefiori, D.C., Binley, J., Lu, S., Improved induction of antibodies against key neutralizing epitopes by human immunodeficiency virus type 1 gp120 DNA prime-protein boost vaccination compared to gp120 protein-only vaccination. J. Virol. 82 (2008), 7369–7378.
66. van der Lubben, I.M., Verhoef, J.C., Borchard, G., Junginger, H.E., Chitosan and its derivatives in mucosal drug and vaccine delivery. Eur. J. Pharm. Sci. 14 (2001), 201–207.
67. Walker, L.M., Huber, M., Doores, K.J., Falkowska, E., Pejchal, R., Julien, J.-P., Wang, S.-K., Ramos, A., Chan-Hui, P.-Y., Moyle, M., Mitcham, J.L., Hammond, P.W., Olsen, O.A., Phung, P., Fling, S., Wong, C.-H., Phogat, S., Wrin, T., Simek, M.D., Protocol, G, Investigators, Principal, Koff, W.C., Wilson, I.A., Burton, D.R., Poignard, P., Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477 (2011), 466–470.
68. 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., Burton, D.R., Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (2009), 285–289.
69. Wang, L., Qin, Y., Ilchenko, S., Bohon, J., Shi, W., Cho, M.W., Takamoto, K., Chance, M.R., Structural analysis of a highly glycosylated and unliganded gp120-based antigen using mass spectrometry. Biochemistry 49 (2010), 9032–9045.
70. Wei, X., Decker, J.M., Liu, H., Zhang, Z., Arani, R.B., Kilby, J.M., Saag, M.S., Wu, X., Shaw, G.M., Kappes, J.C., Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46 (2002), 1896–1905.
71. Wu, L., Zhou, T., Yang, Z.-Y., Svehla, K., O'Dell, S., Louder, M.K., Xu, L., Mascola, J.R., Burton, D.R., Hoxie, J.A., Doms, R.W., Kwong, P.D., Nabel, G.J., Enhanced exposure of the CD4-binding site to neutralizing antibodies by structural design of a membrane-anchored human immunodeficiency virus type 1 gp120 domain. J. Virol. 83 (2009), 5077–5086.
72. 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., Mascola, J.R., Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329 (2010), 856–861.
73. Wyatt, R., Kwong, P.D., Desjardins, E., Sweet, R.W., Robinson, J., Hendrickson, W.A., Sodroski, J.G., The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393 (1998), 705–711.
74. Wyatt, R., Moore, J., Accola, M., Desjardin, E., Robinson, J., Sodroski, J., Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 69 (1995), 5723–5733.
75. Wyatt, R., Sodroski, J., The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280 (1998), 1884–1888.
76. Yang, X., Tomov, V., Kurteva, S., Wang, L., Ren, X., Gorny, M.K., Zolla-Pazner, S., Sodroski, J., Characterization of the outer domain of the gp120 glycoprotein from human immunodeficiency virus type 1. J. Virol. 78 (2004), 12975–12986.
77. Zhou, T., Xu, L., Dey, B., Hessell, A.J., Van Ryk, D., Xiang, S.-H., Yang, X., Zhang, M.-Y., Zwick, M.B., Arthos, J., Burton, D.R., Dimitrov, D.S., Sodroski, J., Wyatt, R., Nabel, G.J., Kwong, P.D., Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445 (2007), 732–737.
78. Zhu, P., Chertova, E., Bess, J., Lifson, J.D., Arthur, L.O., Liu, J., Taylor, K.A., Roux, K.H., Electron tomography analysis of envelope glycoprotein trimers on HIV and simian immunodeficiency virus virions. Proc. Natl. Acad. Sci. U.S.A. 100 (2003), 15812–15817.
79. Zolla-Pazner, S., O'Leary, J., Burda, S., Gorny, M.K., Kim, M., Mascola, J., McCutchan, F., Serotyping of primary human immunodeficiency virus type 1 isolates from diverse geographic locations by flow cytometry. J. Virol. 69 (1995), 3807–3815.
80. Zwick, M.B., Labrijn, A.F., Wang, M., Spenlehauer, C., Saphire, E.O., Binley, J.M., Moore, J.P., Stiegler, G., Katinger, H., Burton, D.R., Parren, P.W., Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J. Virol. 75 (2001), 10892–10905.