HIV-1 Receptor Binding Site-Directed Antibodies Using a VH1-2 Gene Segment Orthologue Are Activated by Env Trimer Immunization

PLoS Pathogens

Volumn 10, Issue 8, 2014, Pages

  Navis, Marjon ^a   Tran, Karen ^b   Bale, Shridhar ^b   Phad, Ganesh E ^a   Guenaga, Javier ^b   Wilson, Richard ^b   Soldemo, Martina ^a   McKee, Krisha ^c   Sundling, Christopher ^a   Mascola, John ^c   Li, Yuxing ^b   Wyatt, Richard T ^b   Karlsson Hedestam, Gunilla B ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD20 ANTIGEN; CD27 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; ENVELOPE PROTEIN; GLYCOPROTEIN GP 120; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN VARIABLE REGION; VIRUS ENVELOPE PROTEIN;

AFFINITY CHROMATOGRAPHY; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY COMBINING SITE; ARTICLE; BIOTINYLATION; BLOOD SAMPLING; CELL SELECTION; COMPLEMENTARITY DETERMINING REGION; CRYSTALLIZATION; DNA ISOLATION; EPITOPE MAPPING; FLOW CYTOMETRY; GEL FILTRATION CHROMATOGRAPHY; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNIZATION; MOLECULAR CLONING; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; SOMATIC HYPERMUTATION; VH1 2 GENE; VIRUS GENE; VIRUS NEUTRALIZATION; AMINO ACID SEQUENCE; ANIMAL; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; MOLECULAR GENETICS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, NEUTRALIZING; B-LYMPHOCYTES; BINDING SITES, ANTIBODY; CD4-POSITIVE T-LYMPHOCYTES; FLOW CYTOMETRY; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN VARIABLE REGION; MACACA MULATTA; MOLECULAR SEQUENCE DATA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRAL ENVELOPE PROTEINS;

EID: 84911462885     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004337     Document Type: Article

References (67)

1. Burton DR, Desrosiers RC, Doms RW, Koff WC, Kwong PD, et al. (2004) HIV vaccine design and the neutralizing antibody problem. Nat Immunol 5: 233–236.
2. Burton DR, Stanfield RL, Wilson IA, (2005) Antibody vs. HIV in a clash of evolutionary titans. Proc Natl Acad Sci U S A 102: 14943–14948.
3. Kwong PD, Doyle ML, Casper DJ, Cicala C, Leavitt SA, et al. (2002) HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420: 678–682.
4. Wyatt R, Sodroski J, (1998) The HIV-1 envelope glycoproteins: fusogens, antigens, and immunogens. Science 280: 1884–1888.
5. Stamatatos L, Morris L, Burton DR, Mascola JR, (2009) Neutralizing antibodies generated during natural HIV-1 infection: good news for an HIV-1 vaccine? Nat Med 15: 866–870.
6. Binley JM, Lybarger EA, Crooks ET, Seaman MS, Gray E, et al. (2008) Profiling the specificity of neutralizing antibodies in a large panel of plasmas from patients chronically infected with human immunodeficiency virus type 1 subtypes B and C. J Virol 82: 11651–11668.
7. Li Y, Migueles SA, Welcher B, Svehla K, Phogat A, et al. (2007) Broad HIV-1 neutralization mediated by CD4-binding site antibodies. Nat Med 13: 1032–1034.
8. Walker LM, Simek MD, Priddy F, Gach JS, Wagner D, et al. (2010) A limited number of antibody specificities mediate broad and potent serum neutralization in selected HIV-1 infected individuals. PLoS Pathog 6: e1001028.
9. Scheid JF, Mouquet H, Ueberheide B, Diskin R, Klein F, et al. (2011) Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333: 1633–1637.
10. Walker LM, Huber M, Doores KJ, Falkowska E, Pejchal R, et al. (2011) Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466–470.
11. Walker LM, Phogat SK, Chan-Hui PY, Wagner D, Phung P, et al. (2009) Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target. Science 326: 285–289.
12. Wu X, Yang ZY, Li Y, Hogerkorp CM, Schief WR, et al. (2010) Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856–861.
13. Wu X, Zhou T, Zhu J, Zhang B, Georgiev I, et al. (2011) Focused Evolution of HIV-1 Neutralizing Antibodies Revealed by Structures and Deep Sequencing. Science 333: 1593–1602.
14. Baba TW, Liska V, Hofmann-Lehmann R, Vlasak J, Xu W, et al. (2000) Human neutralizing monoclonal antibodies of the IgG1 subtype protect against mucosal simian-human immunodeficiency virus infection. Nat Med 6: 200–206.
15. Hessell AJ, Poignard P, Hunter M, Hangartner L, Tehrani DM, et al. (2009) Effective, low-titer antibody protection against low-dose repeated mucosal SHIV challenge in macaques. Nat Med 15: 951–954.
16. Hessell AJ, Rakasz EG, Poignard P, Hangartner L, Landucci G, et al. (2009) Broadly neutralizing human anti-HIV antibody 2G12 is effective in protection against mucosal SHIV challenge even at low serum neutralizing titers. PLoS Pathog 5: e1000433.
17. Hessell AJ, Rakasz EG, Tehrani DM, Huber M, Weisgrau KL, et al. (2010) Broadly neutralizing monoclonal antibodies 2F5 and 4E10 directed against the human immunodeficiency virus type 1 gp41 membrane-proximal external region protect against mucosal challenge by simian-human immunodeficiency virus SHIVBa-L. J Virol 84: 1302–1313.
18. Mascola JR, Stiegler G, VanCott TC, Katinger H, Carpenter CB, et al. (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.
19. Moldt B, Rakasz EG, Schultz N, Chan-Hui PY, Swiderek K, et al. (2012) Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc Natl Acad Sci U S A 109: 18921–18925.
20. Parren PW, Marx PA, Hessell AJ, Luckay A, Harouse J, 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.
21. Barouch DH, Whitney JB, Moldt B, Klein F, Oliveira TY, et al. (2013) Therapeutic efficacy of potent neutralizing HIV-1-specific monoclonal antibodies in SHIV-infected rhesus monkeys. Nature 503: 224–228.
22. Shingai M, Nishimura Y, Klein F, Mouquet H, Donau OK, et al. (2013) Antibody-mediated immunotherapy of macaques chronically infected with SHIV suppresses viraemia. Nature 503: 277–280.
23. Klein F, Halper-Stromberg A, Horwitz JA, Gruell H, Scheid JF, et al. (2012) HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492: 118–122.
24. Klein F, Mouquet H, Dosenovic P, Scheid JF, Scharf L, et al. (2013) Antibodies in HIV-1 vaccine development and therapy. Science 341: 1199–1204.
25. Corti D, Langedijk JP, Hinz A, Seaman MS, Vanzetta F, 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.
26. Zhou T, Georgiev I, Wu X, Yang ZY, Dai K, et al. (2010) Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811–817.
27. West AP, JrDiskin R, Nussenzweig MC, Bjorkman PJ, (2012) Structural basis for germ-line gene usage of a potent class of antibodies targeting the CD4-binding site of HIV-1 gp120. Proc Natl Acad Sci U S A 109: E2083–2090.
28. Diskin R, Scheid JF, Marcovecchio PM, West AP, JrKlein F, et al. (2011) Increasing the potency and breadth of an HIV antibody by using structure-based rational design. Science 334: 1289–1293.
29. Zhou T, Zhu J, Wu X, Moquin S, Zhang B, et al. (2013) Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39: 245–258.
30. Sundling C, Li Y, Huynh N, Poulsen C, Wilson R, et al. (2012) High-Resolution Definition of Vaccine-Elicited B Cell Responses Against the HIV Primary Receptor Binding Site. Sci Transl Med 4: 142ra196.
31. McCoy LE, Quigley AF, Strokappe NM, Bulmer-Thomas B, Seaman MS, et al. (2012) Potent and broad neutralization of HIV-1 by a llama antibody elicited by immunization. J Exp Med 209: 1091–1103.
32. Sundling C, Forsell MN, O'Dell S, Feng Y, Chakrabarti B, et al. (2010) Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J Exp Med 207: 2003–2017.
33. Tran K, Poulsen C, Guenega J, de Val N, Wilson R, 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: E738–747.
34. Yang X, Lee J, Mahony EM, Kwong PD, Wyatt R, et al. (2002) Highly stable trimers formed by human immunodeficiency virus type 1 envelope glycoproteins fused with the trimeric motif of T4 bacteriophage fibritin. J Virol 76: 4634–4642.
35. Forsell MN, Dey B, Morner A, Svehla K, O'Dell S, et al. (2008) B cell recognition of the conserved HIV-1 co-receptor binding site is altered by endogenous primate CD4. PLoS Pathog 4: e1000171.
36. Dey B, Svehla K, Xu L, Wycuff D, Zhou T, et al. (2009) Structure-based stabilization of HIV-1 gp120 enhances humoral immune responses to the induced co-receptor binding site. PLoS Pathog 5: e1000445.
37. Doria-Rose NA, Klein RM, Manion MM, O'Dell S, Phogat A, et al. (2009) Frequency and phenotype of human immunodeficiency virus envelope-specific B cells from patients with broadly cross-neutralizing antibodies. J Virol 83: 188–199.
38. Tiller T, Meffre E, Yurasov S, Tsuiji M, Nussenzweig MC, 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: 112–124.
39. Sundling C, Phad G, Douagi I, Navis M, Karlsson Hedestam GB, (2012) Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J Immunol Methods 386: 85–93.
40. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, et al. (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 1: W465–469.
41. Huson DH, Richter DC, Rausch C, Dezulian T, Franz M, et al. (2007) Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8: 460–465.
42. Gibbs RA, Rogers J, Katze MG, Bumgarner R, Weinstock GM, et al. (2007) Evolutionary and biomedical insights from the rhesus macaque genome. Science 316: 222–234.
43. Li M, Gao F, Mascola JR, Stamatatos L, Polonis VR, 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: 10108–10125.
44. Pantophlet R, Ollmann Saphire E, Poignard P, Parren PW, Wilson IA, et al. (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.
45. Li Y, O'Dell S, Walker LM, Wu X, Guenaga J, et al. (2011) Mechanism of Neutralization by the Broadly Neutralizing HIV-1 Monoclonal Antibody VRC01. J Virol 85: 8954–8967.
46. Otwinowski Z, Minor W, (1997) Processing of X-ray Diffraction Data Collected in Oscillation Mode. Methods in Enzymology 276A: 307–326.
47. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr D58: 1948–1954.
48. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ, (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61: 458–464.
49. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr D60: 2126–2132.
50. Vagin AA, Steiner RA, Lebedev AA, Potterton L, McNicholas S, et al. (2004) REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr D Biol Crystallogr 60: 2184–2195.
51. Comeau SR, Gatchell DW, Vajda S, Camacho CJ, (2004) ClusPro: a fully automated algorithm for protein-protein docking. Nucleic acids research 32: W96–99.
52. Comeau SR, Gatchell DW, Vajda S, Camacho CJ, (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20: 45–50.
53. Kozakov D, Beglov D, Bohnuud T, Mottarella SE, Xia B, et al. (2013) How good is automated protein docking? Proteins 81: 2159–2166.
54. Kozakov D, Brenke R, Comeau SR, Vajda S, (2006) PIPER: an FFT-based protein docking program with pairwise potentials. Proteins 65: 392–406.
55. Brenke R, Hall DR, Chuang GY, Comeau SR, Bohnuud T, et al. (2012) Application of asymmetric statistical potentials to antibody-protein docking. Bioinformatics 28: 2608–2614.
56. Jardine J, Julien JP, Menis S, Ota T, Kalyuzhniy O, et al. (2013) Rational HIV immunogen design to target specific germline B cell receptors. Science 340: 711–716.
57. Xiang SH, Kwong PD, Gupta R, Rizzuto CD, Casper DJ, 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.
58. Douagi I, Forsell MN, Sundling C, O'Dell S, Feng Y, et al. (2010) Influence of novel CD4 binding-defective HIV-1 envelope glycoprotein immunogens on neutralizing antibody and T-cell responses in nonhuman primates. J Virol 84: 1683–1695.
59. Chen L, Kwon YD, Zhou T, Wu X, O'Dell S, et al. (2009) Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326: 1123–1127.
60. Kwong PD, Wyatt R, Robinson J, Sweet RW, Sodroski J, et al. (1998) Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648–659.
61. Zhou T, Xu L, Dey B, Hessell AJ, Van Ryk D, et al. (2007) Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732–737.
62. Julien JP, Cupo A, Sok D, Stanfield RL, Lyumkis D, et al. (2013) Crystal Structure of a Soluble Cleaved HIV-1 Envelope Trimer. Science 342: 1477–1483.
63. Kwong PD, Mascola JR, (2012) Human antibodies that neutralize HIV-1: identification, structures, and B cell ontogenies. Immunity 37: 412–425.
64. Klein F, Diskin R, Scheid JF, Gaebler C, Mouquet H, et al. (2013) Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153: 126–138.
65. McGuire AT, Hoot S, Dreyer AM, Lippy A, Stuart A, et al. (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.
66. Liao HX, Lynch R, Zhou T, Gao F, Alam SM, et al. (2013) Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469–476.
67. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109–113.