Recombinant HIV envelope trimer selects for quaternary-dependent antibodies targeting the trimer apex

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages 17624-17629

  Sok, Devin ^a,b   Gils, Marit J Van ^c   Pauthner, Matthias ^a   Julien, Jean Philippe ^a,d   Saye Francisco, Karen L ^a   Hsueh, Jessica ^a   Briney, Bryan ^a   Lee, Jeong Hyun ^a   Le, Khoa M ^a   Lee, Peter S ^a   Hua, Yuanzi ^a   Seaman, Michael S ^e   Moore, John P ^f   Ward, Andrew B ^a   Wilson, Ian A ^a   Sanders, Rogier W ^c,f   Burton, Dennis R ^a,g  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b INTERNATIONAL AIDS VACCINE INITIATIVE   (United States)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^f WEILL CORNELL MEDICAL COLLEGE   (United States)

^g HARVARD UNIVERSITY   (United States)

Author keywords

B cell; BG505 SOSIP; Broadly neutralizing antibodies; HIV; Vaccine

Indexed keywords

GLYCOPROTEIN GP 140; NEUTRALIZING ANTIBODY; PGDM1400; PGDM1412; PGT121; PGT145; REAGENT; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; EPITOPE; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; PEPTIDE LIBRARY;

ANTIBODY RESPONSE; ARTICLE; BINDING KINETICS; BIOTINYLATION; CONJUGATION; DRUG ISOLATION; DRUG POTENCY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IC50; IMMUNOTHERAPY; PERIPHERAL BLOOD MONONUCLEAR CELL; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; B LYMPHOCYTE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CROSS REACTION; CYTOLOGY; GENETIC VARIABILITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; MOLECULAR GENETICS; MONONUCLEAR CELL; NUCLEOTIDE SEQUENCE; PEPTIDE LIBRARY; PHYLOGENY; PROTEIN FOLDING; SEQUENCE HOMOLOGY; SERODIAGNOSIS;

AMINO ACID SEQUENCE; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BASE SEQUENCE; CROSS REACTIONS; EPITOPES; GENETIC VARIATION; HIV ANTIBODIES; HIV ENVELOPE PROTEIN GP120; HIV INFECTIONS; HUMANS; IMMUNOLOGIC MEMORY; INHIBITORY CONCENTRATION 50; LEUKOCYTES, MONONUCLEAR; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PEPTIDE LIBRARY; PHYLOGENY; PROTEIN FOLDING; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84917705974     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1415789111     Document Type: Article

References (45)

1. Walker LM, et al.; Protocol G Principal Investigators (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326 (5950):285-289.
2. Doria-Rose NA, et al.; NISC Comparative Sequencing Program (2014) Developmental pathway for potent V1V2-directed HIV-neutralizing antibodies. Nature 509 (7498):55-62.
3. Walker LM, et al.; Protocol G Principal Investigators (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477 (7365):466-470.
4. Bonsignori M, et al. (2011) Analysis of a clonal lineage of HIV-1 envelope V2/V3 conformational epitope-specific broadly neutralizing antibodies and their inferred unmutated common ancestors. J Virol 85(19):9998-10009.
5. Burton DR, et al. (2012) A blueprint for HIV vaccine discovery. Cell Host Microbe 12(4): 396-407.
6. Wu X, et al. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329 (5993):856-861.
7. Huang J, et al. (2012) Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491 (7424):406-412.
8. Scheid JF, et al. (2011) Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333 (6049):1633-1637.
9. Mouquet H, et al. (2012) Complex-type N-glycan recognition by potent broadly neutralizing HIV antibodies. Proc Natl Acad Sci USA 109(47):E3268-E3277.
10. Klein F, et al. (2012) 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(8):1469-1479.
11. Falkowska E, et al. (2014) Broadly neutralizing HIV antibodies define a glycan-dependent epitope on the prefusion conformation of gp41 on cleaved envelope trimers. Immunity 40(5):657-668.
12. Blattner C, et al. (2014) Structural delineation of a quaternary, cleavage-dependent epitope at the gp41-gp120 interface on intact HIV-1 Env trimers. Immunity 40(5):669-680.
13. Burton DR, et al. (1994) Efficient neutralization of primary isolates of HIV-1 by a recombinant human monoclonal antibody. Science 266 (5187):1024-1027.
14. Muster T, et al. (1994) Cross-neutralizing activity against divergent human immunodeficiency virus type 1 isolates induced by the gp41 sequence ELDKWAS. J Virol 68(6):4031-4034.
15. Burton DR, et al. (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 USA 88(22):10134-10137.
16. Zwick MB, et al. (2001) Broadly neutralizing antibodies targeted to the membrane-proximal external region of human immunodeficiency virus type 1 glycoprotein gp41. J Virol 75(22):10892-10905.
17. Barbas CF, 3rd, et al. (1992) Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc Natl Acad Sci USA 89(19):9339-9343.
18. Trkola A, et al. (1996) Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70(2):1100-1108.
19. Conley AJ, et al. (1994) Neutralization of divergent human immunodeficiency virus type 1 variants and primary isolates by IAM-41-2F5, an anti-gp41 human monoclonal antibody. Proc Natl Acad Sci USA 91(8):3348-3352.
20. Buchacher A, et al. (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(4):359-369.
21. Simek MD, et al. (2009) Human immunodeficiency virus type 1 elite neutralizers: Individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm. J Virol 83(14):7337-7348.
22. Gray ES, et al.; CAPRISA002 Study Team (2011) The neutralization breadth of HIV-1 develops incrementally over four years and is associated with CD4+ T cell decline and high viral load during acute infection. J Virol 85(10):4828-4840.
23. Wardemann H, et al. (2003) Predominant autoantibody production by early human B cell precursors. Science 301 (5638):1374-1377.
24. Scheid JF, et al. (2009) Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458 (7238):636-640.
25. Gaebler C, et al. (2013) Isolation of HIV-1-reactive antibodies using cell surface-expressed gp160Δc(BaL.). J Immunol Methods 397(1-2):47-54.
26. Sanders RW, et al. (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(9):e1003618.
27. Tiller T, et al. (2008) Efficient generation of monoclonal antibodies from single human B cells by single cell RT-PCR and expression vector cloning. J Immunol Methods 329(1-2):112-124.
28. Zhu J, et al.; NISC Comparative Sequencing Program (2013) Mining the antibodyome for HIV-1-neutralizing antibodies with next-generation sequencing and phylogenetic pairing of heavy/light chains. Proc Natl Acad Sci USA 110(16):6470-6475.
29. McLellan JS, et al. (2011) Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480 (7377):336-343.
30. Pancera M, et al. (2013) Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat Struct Mol Biol 20(7):804-813.
31. Julien J-P, et al. (2013) Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc Natl Acad Sci USA 110(11):4351-4356.
32. Yasmeen A, et al. (2014) Differential binding of neutralizing and non-neutralizing antibodies to native-like soluble HIV-1 Env trimers, uncleaved Env proteins, and monomeric subunits. Retrovirology 11:41.
33. Lyumkis D, et al. (2013) Cryo-EM structure of a fully glycosylated soluble cleaved HIV-1 envelope trimer. Science 342 (6165):1484-1490.
34. Tran K, et al. (2014) Vaccine-elicited primate antibodies use a distinct approach to the HIV-1 primary receptor binding site informing vaccine redesign. Proc Natl Acad Sci USA 111(7):E738-E747.
35. Kong L, et al. (2013) Supersite of immune vulnerability on the glycosylated face of HIV-1 envelope glycoprotein gp120. Nat Struct Mol Biol 20(7):796-803.
36. Julien J-P, et al. (2013) Crystal structure of a soluble cleaved HIV-1 envelope trimer. Science 342 (6165):1477-1483.
37. Sok D, et al. (2013) The effects of somatic hypermutation on neutralization and binding in the PGT121 family of broadly neutralizing HIV antibodies. PLoS Pathog 9(11):e1003754.
38. Liao H-X, et al.; NISC Comparative Sequencing Program (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496 (7446):469-476.
39. Scharf L, et al. (2014) Antibody 8ANC195 reveals a site of broad vulnerability on the HIV-1 envelope spike. Cell Reports 7(3):785-795.
40. Gray ES, et al.; CAPRISA 002 Study Team (2007) Neutralizing antibody responses in acute human immunodeficiency virus type 1 subtype C infection. J Virol 81(12): 6187-6196.
41. Walker LM, et al. (2010) A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6(8): e1001028.
42. Li M, et al. (2005) 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(16):10108-10125.
43. Sievers F, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539.
44. Schrodinger, LLC (2010) The PyMOL molecular graphics system, version 1.3r1. Available at www.pymol.org.
45. Pettersen EF, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605-1612.