Antibody potency relates to the ability to recognize the closed, pre-fusion form of HIV Env

Nature Communications

Volumn 6, Issue , 2015, Pages

  Guttman, Miklos ^a   Cupo, Albert ^b   Julien, Jean Philippe ^c   Sanders, Rogier W ^b,d   Wilson, Ian A ^c   Moore, John P ^b   Lee, Kelly K ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c International AIDS Vaccine Initiative Neutralizing Antibody Center   (United States)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD4I ANTIBODY; CELL ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ENVELOPE GLYCOPROTEIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; EPITOPE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ANTIBODY; DEUTERIUM; HUMAN IMMUNODEFICIENCY VIRUS; HYDROGEN; NEUTRALIZATION; PROTEIN; REACTION KINETICS; VIRUS;

ANTIGEN BINDING; ANTIGEN RECOGNITION; ARTICLE; BINDING KINETICS; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEUTERIUM HYDROGEN EXCHANGE; ELECTRON MICROSCOPY; IC50; IMMUNOPRECIPITATION; KINETICS; NATIVE POLYACRYLAMIDE GEL ELECTROPHORESIS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SURFACE PROPERTY; ANTAGONISTS AND INHIBITORS; CHEMISTRY; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MOLECULAR MODEL; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE;

ANTIBODIES, NEUTRALIZING; BINDING SITES; DEUTERIUM EXCHANGE MEASUREMENT; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; EPITOPES; GENE EXPRESSION; HEK293 CELLS; HIV-1; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS;

EID: 84923164032     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7144     Document Type: Article

References (70)

1. Walker, L. M. & Burton, D. R. Rational antibody-based HIV-1 vaccine design: current approaches and future directions. Curr. Opin. Immunol. 22, 358-366 (2010).
2. Walker, L. M. et al. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477, 466-470 (2011).
3. Mascola, J. R. & Haynes, B. F. HIV-1 neutralizing antibodies: understanding nature's pathways. Immunol. Rev. 254, 225-244 (2013).
4. Wyatt, R. et al. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705-711 (1998).
5. Kwong, P. D. et al. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420, 678-682 (2002).
6. Wei, X. et al. Antibody neutralization and escape by HIV-1. Nature 422, 307-312 (2003).
7. Pantophlet, R. et al. 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 (2003).
8. Wu, X. et al. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333, 1593-1602 (2011).
9. Liu, J., Bartesaghi, A., Borgnia, M. J., Sapiro, G. & Subramaniam, S. Molecular architecture of native HIV-1 gp120 trimers. Nature 455, 109-113 (2008).
10. Julien, J. P. et al. Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342, 1477-1483 (2013).
11. Lyumkis, D. et al. Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342, 1484-1490 (2013).
12. Pancera, M. et al. Structure and immune recognition of trimeric pre-fusion HIV-1 Env. Nature 514, 455-461 (2014).
13. Wu, L. et al. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature 384, 179-183 (1996).
14. Trkola, A. et al. CD4-dependent, antibody-sensitive interactions between HIV- 1 and its co-receptor CCR-5. Nature 384, 184-187 (1996).
15. Rizzuto, C. D. et al. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280, 1949-1953 (1998).
16. White, T. A. et al. Molecular architectures of trimeric SIV and HIV-1 envelope glycoproteins on intact viruses: strain-dependent variation in quaternary structure. PLoS Pathog. 6, e1001249 (2010).
17. Tran, E. E. et al. Structural mechanism of trimeric HIV-1 envelope glycoprotein activation. PLoS Pathog. 8, e1002797 (2012).
18. Harris, A. et al. Trimeric HIV-1 glycoprotein gp140 immunogens and native HIV-1 envelope glycoproteins display the same closed and open quaternary molecular architectures. Proc. Natl Acad. Sci. USA 108, 11440-11445 (2011).
19. Guttman, M. et al. CD4-induced activation in a soluble HIV-1 Env trimer. Structure 22, 974-984 (2014).
20. Burton, D. R. et al. Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266, 1024-1027 (1994).
21. Zhou, T. et al. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445, 732-737 (2007).
22. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
23. Thali, M. et al. Characterization of conserved human immunodeficiency virus type 1 gp120 neutralization epitopes exposed upon gp120-CD4 binding. J. Virol. 67, 3978-3988 (1993).
24. Kwong, P. D. et al. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393, 648-659 (1998).
25. Salzwedel, K., Smith, E. D., Dey, B. & Berger, E. A. Sequential CD4-coreceptor interactions in human immunodeficiency virus type 1 Env function: soluble CD4 activates Env for coreceptor-dependent fusion and reveals blocking activities of antibodies against cryptic conserved epitopes on gp120. J. Virol. 74, 326-333 (2000).
26. Seaman, M. S. et al. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84, 1439-1452 (2010).
27. Trkola, A. et al. Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J. Virol. 70, 1100-1108 (1996).
28. Sanders, R. W. et al. The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J. Virol. 76, 7293-7305 (2002).
29. Murin, C. D. et al. Structure of 2G12 Fab2 in complex with soluble and fully glycosylated HIV-1 Env by negative-stain single particle electron microscopy. J. Virol. 88, 10177-10188 (2014).
30. Walker, L. M. et al. Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326, 285-289 (2009).
31. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
32. Julien, J. P. et al. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc. Natl Acad. Sci. USA 110, 4351-4356 (2013).
33. Bartesaghi, A., Merk, A., Borgnia, M. J., Milne, J. L. & Subramaniam, S. Prefusion structure of trimeric HIV-1 envelope glycoprotein determined by cryo-electron microscopy. Nat. Struct. Mol. Biol. 20, 1352-1357 (2013).
34. Blattner, C. et al. Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40, 669-680 (2014).
35. Klasse, P. J. & Sattentau, Q. J. Occupancy and mechanism in antibody-mediated neutralization of animal viruses. J. Gen. Virol. 83, 2091-2108 (2002).
36. Reading, S. A. & Dimmock, N. J. Neutralization of animal virus infectivity by antibody. Arch. Virol. 152, 1047-1059 (2007).
37. Sanders, R. W. et al. 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 (2013).
38. Marcsisin, S. R. & Engen, J. R. Hydrogen exchange mass spectrometry: what is it and what can it tell us? Anal. Bioanal. Chem. 397, 967-972 (2010).
39. Eroshkin, A. M. et al. bNAber: database of broadly neutralizing HIV antibodies. Nucleic Acids Res. 42, D1133-D1139 (2014).
40. Ringe, R. P. et al. Cleavage strongly influences whether soluble HIV-1 envelope glycoprotein trimers adopt a native-like conformation. Proc. Natl Acad. Sci. USA 110, 18256-18261 (2013).
41. Julien, J. P. et al. Broadly neutralizing antibody PGT121 allosterically modulates CD4 binding via recognition of the HIV-1 gp120 V3 base and multiple surrounding glycans. PLoS Pathog. 9, e1003342 (2013).
42. Calarese, D. A. et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300, 2065-2071 (2003).
43. Schon, A. et al. Thermodynamics of binding of a low-molecular-weight CD4 mimetic to HIV-1 gp120. Biochemistry 45, 10973-10980 (2006).
44. Mo, H. et al. Human immunodeficiency virus type 1 mutants that escape neutralization by human monoclonal antibody IgG1b12. J. Virol. 71, 6869-6874 (1997).
45. Li, Y. et al. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 85, 8954-8967 (2011).
46. Falkowska, E. et al. PGV04, an HIV-1 gp120 CD4 binding site antibody, is broad and potent in neutralization but does not induce conformational changes characteristic of CD4. J. Virol. 86, 4394-4403 (2012).
47. Guttman, M., Kahn, M., Garcia, N. K., Hu, S. L. & Lee, K. K. Solution structure, conformational dynamics, and CD4-induced activation in full-length, glycosylated, monomeric HIV gp120. J. Virol. 86, 8750-8764 (2012).
48. Munro, J. B. et al. Conformational dynamics of single HIV-1 envelope trimers on the surface of native virions. Science 346, 759-763 (2014).
49. Moore, J. P., Trkola, A., Sattentau, Q. J., Cao, Y. & Ho, D. D. Studies on the interactions of monoclonal antibodies with HIV-1 isolates from clades A-F. Proceedings of IX Colloque des Cent Gardes 151-155 (1994).
50. Moore, J. P., Sattentau, Q. J., Wyatt, R. & Sodroski, J. Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J. Virol. 68, 469-484 (1994).
51. Sullivan, N., Sun, Y., Li, J., Hofmann, W. & Sodroski, J. Replicative function and neutralization sensitivity of envelope glycoproteins from primary and T-cell line-passaged human immunodeficiency virus type 1 isolates. J. Virol. 69, 4413-4422 (1995).
52. Sattentau, Q. J. & Moore, J. P. Human immunodeficiency virus type 1 neutralization is determined by epitope exposure on the gp120 oligomer. J. Exp. Med. 182, 185-196 (1995).
53. Fouts, T. R., Binley, J. M., Trkola, A., Robinson, J. E. & Moore, J. P. Neutralization of the human immunodeficiency virus type 1 primary isolate JRFL by human monoclonal antibodies correlates with antibody binding to the oligomeric form of the envelope glycoprotein complex. J. Virol. 71, 2779-2785 (1997).
54. Kwong, P. D. et al. Structures of HIV-1 gp120 envelope glycoproteins from laboratory-adapted and primary isolates. Structure 8, 1329-1339 (2000).
55. Brandenberg, O. F. et al. Partial rescue of V1V2 mutant infectivity by HIV-1 cell-cell transmission supports the domain's exceptional capacity for sequence variation. Retrovirology 11, 75 (2014).
56. Kolchinsky, P., Kiprilov, E. & Sodroski, J. Increased neutralization sensitivity of CD4-independent human immunodeficiency virus variants. J. Virol. 75, 2041-2050 (2001).
57. Kabat, D., Kozak, S. L., Wehrly, K. & Chesebro, B. Differences in CD4 dependence for infectivity of laboratory-adapted and primary patient isolates of human immunodeficiency virus type 1. J. Virol. 68, 2570-2577 (1994).
58. Hoffman, T. L. et al. Stable exposure of the coreceptor-binding site in a CD4- independent HIV-1 envelope protein. Proc. Natl Acad. Sci. USA 96, 6359-6364 (1999).
59. Edwards, T. G. et al. Relationships between CD4 independence, neutralization sensitivity, and exposure of a CD4-induced epitope in a human immunodeficiency virus type 1 envelope protein. J. Virol. 75, 5230-5239 (2001).
60. Haim, H. et al. Contribution of intrinsic reactivity of the HIV-1 envelope glycoproteins to CD4-independent infection and global inhibitor sensitivity. PLoS Pathog. 7, e1002101 (2011).
61. Weis, D. D., Wales, T. E., Engen, J. R., Hotchko, M. & Ten Eyck, L. F. Identification and characterization of EX1 kinetics in H/D exchange mass spectrometry by peak width analysis. J. Am. Soc. Mass Spectrom. 17, 1498-1509 (2006).
62. Stamatatos, L., Morris, L., Burton, D. R. & Mascola, J. R. Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat. Med. 15, 866-870 (2009).
63. Iyer, S. P. et al. Purified, proteolytically mature HIV type 1 SOSIP gp140 envelope trimers. AIDS Res. Hum. Retroviruses 23, 817-828 (2007).
64. Garlick, R. L., Kirschner, R. J., Eckenrode, F. M., Tarpley, W. G. & Tomich, C. S. Escherichia coli expression, purification, and biological activity of a truncated soluble CD4. AIDS Res. Hum. Retroviruses 6, 465-479 (1990).
65. Burton, D. R. et al. A large array of human monoclonal antibodies to type 1 human immunodeficiency virus from combinatorial libraries of asymptomatic seropositive individuals. Proc. Natl Acad. Sci. USA 88, 10134-10137 (1991).
66. Barbas, 3rd C. F. et al. Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc. Natl Acad. Sci. USA 89, 9339-9343 (1992).
67. Buchacher, A. et al. 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 (1994).
68. Wu, X. et al. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329, 856-861 (2010).
69. Pejchal, R. et al. Structure and function of broadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc. Natl Acad. Sci. USA 107, 11483-11488 (2010).
70. Pancera, M. et al. Structure of HIV-1 gp120 with gp41-interactive region reveals layered envelope architecture and basis of conformational mobility. Proc. Natl Acad. Sci. USA 107, 1166-1171 (2010).