High-resolution longitudinal study of HIV-1 env vaccine-elicited b cell responses to the virus primary receptor binding site reveals affinity maturation and clonal persistence

Journal of Immunology

Volumn 196, Issue 9, 2016, Pages 3729-3743

  Wang, Yimeng ^a,b   Sundling, Christopher ^c,d   Wilson, Richard ^a   O'Dell, Sijy ^e   Chen, Yajing ^a   Dai, Kaifan ^a   Phad, Ganesh E ^c   Zhu, Jiang ^a,f   Xiao, Yongli ^e   Mascola, John R ^e   Karlsson Hedestam, Gunilla B ^c   Wyatt, Richard T ^a,f   Li, Yuxing ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

^d GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

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

^f Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOGLOBULIN; CD4 ANTIGEN; COMPLEMENTARITY DETERMINING REGION; PROTEIN BINDING; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ANTIGENICITY; ARTICLE; BINDING AFFINITY; BINDING SITE; CLONAL VARIATION; CONTROLLED STUDY; GENETIC ANALYSIS; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HYDROPHOBICITY; LONGITUDINAL STUDY; MEMORY CELL; NONHUMAN; PHYLOGENY; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY; SOMATIC HYPERMUTATION; STATIC ELECTRICITY; THERMOSTABILITY; TIME TO TREATMENT; VIRUS NEUTRALIZATION; ANIMAL; ANTIBODY AFFINITY; ANTIBODY COMBINING SITE; BIOLOGY; BLOOD; CELL CLONE; CELL SURVIVAL; COMPLEMENTARITY DETERMINING REGION; GENETICS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; SINGLE CELL ANALYSIS;

AIDS VACCINES; ANIMALS; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ANTIGENS, CD4; BINDING SITES, ANTIBODY; CELL SURVIVAL; CLONE CELLS; COMPLEMENTARITY DETERMINING REGIONS; COMPUTATIONAL BIOLOGY; ENV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, HUMORAL; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MACACA MULATTA; PROTEIN BINDING; SINGLE-CELL ANALYSIS;

EID: 84974851790     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502543     Document Type: Article

References (53)

1. Lewis, G. K., A. L. DeVico, and R. C. Gallo. 2014. Antibody persistence and Tcell balance: two key factors confronting HIV vaccine development. Proc. Natl. Acad. Sci. USA 111: 15614-15621.
2. Burton, D. R., and J. R. Mascola. 2015. Antibody responses to envelope glycoproteins in HIV-1 infection. Nat. Immunol. 16: 571-576.
3. Kwong, P. D., J. R. Mascola, and G. J. Nabel. 2013. Broadly neutralizing antibodies and the search for an HIV-1 vaccine: the end of the beginning. Nat. Rev. Immunol. 13: 693-701.
4. Klein, F., H. Mouquet, P. Dosenovic, J. F. Scheid, L. Scharf, and M. C. Nussenzweig. 2013. Antibodies in HIV-1 vaccine development and therapy. Science 341: 1199-1204.
5. Sanders, R. W., R. Derking, A. Cupo, J. P. Julien, A. Yasmeen, N. de Val, H. J. Kim, C. Blattner, A. T. de la Peña, J. Korzun, 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: e1003618.
6. Guenaga, J., N. de Val, K. Tran, Y. Feng, K. Satchwell, A. B. Ward, and R. T. Wyatt. 2015. Well-ordered trimeric HIV-1 subtype B and C soluble spike mimetics generated by negative selection display native-like properties. PLoS Pathog. 11: e1004570.
7. Sharma, S. K., N. de Val, S. Bale, J. Guenaga, K. Tran, Y. Feng, V. Dubrovskaya, A. B. Ward, and R. T. Wyatt. 2015. Cleavage-independent HIV-1 Env trimers engineered as soluble native spike mimetics for vaccine design. Cell Reports 11: 539-550.
8. Dosenovic, P., L. von Boehmer, A. Escolano, J. Jardine, N. T. Freund, A. D. Gitlin, A. T. McGuire, D. W. Kulp, T. Oliveira, L. Scharf, et al. 2015. Immunization for HIV-1 broadly neutralizing antibodies in Human Ig knockin mice. Cell 161: 1505-1515.
9. Jardine, J. G., T. Ota, D. Sok, M. Pauthner, D. W. Kulp, O. Kalyuzhniy, P. D. Skog, T. C. Thinnes, D. Bhullar, B. Briney, et al. 2015. HIV-1 VACCINES. Priming a broadly neutralizing antibody response to HIV-1 using a germlinetargeting immunogen. Science 349: 156-161.
10. McGuire, A. T., A. M. Dreyer, S. Carbonetti, A. Lippy, J. Glenn, J. F. Scheid, H. Mouquet, and L. Stamatatos. 2014. HIV antibodies. Antigen modification regulates competition of broad and narrow neutralizing HIV antibodies. Science 346: 1380-1383.
11. Malherbe, D. C., F. Pissani, D. N. Sather, B. Guo, S. Pandey, W. F. Sutton, A. B. Stuart, H. Robins, B. Park, S. J. Krebs, et al. 2014. Envelope variants circulating as initial neutralization breadth developed in two HIV-infected subjects stimulate multiclade neutralizing antibodies in rabbits. J. Virol. 88: 12949-12967.
12. Bricault, C. A., J. M. Kovacs, J. P. Nkolola, K. Yusim, E. E. Giorgi, J. L. Shields, J. Perry, C. L. Lavine, A. Cheung, K. Ellingson-Strouss, et al. 2015. A multivalent clade C HIV-1 Env trimer cocktail elicits a higher magnitude of neutralizing antibodies than any individual component. J. Virol. 89: 2507-2519.
13. Rerks-Ngarm, S., P. Pitisuttithum, S. Nitayaphan, J. Kaewkungwal, J. Chiu, R. Paris, N. Premsri, C. Namwat, M. de Souza, E. Adams, et al; MOPH-TAVEG Investigators. 2009. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med. 361: 2209-2220.
14. Haynes, B. F., P. B. Gilbert, M. J. McElrath, S. Zolla-Pazner, G. D. Tomaras, S. M. Alam, D. T. Evans, D. C. Montefiori, C. Karnasuta, R. Sutthent, et al. 2012. Immune-correlates analysis of an HIV-1 vaccine efficacy trial. N. Engl. J. Med. 366: 1275-1286.
15. Robb, M. L., S. Rerks-Ngarm, S. Nitayaphan, P. Pitisuttithum, J. Kaewkungwal, P. Kunasol, C. Khamboonruang, P. Thongcharoen, P. Morgan, M. Benenson, et al. 2012. Risk behaviour and time as covariates for efficacy of the HIV vaccine regimen ALVAC-HIV (vCP1521) and AIDSVAX B/E: a post-hoc analysis of the Thai phase 3 efficacy trial RV 144. Lancet Infect. Dis. 12: 531-537.
16. Yates, N. L., H. X. Liao, Y. Fong, A. deCamp, N. A. Vandergrift, W. T. Williams, S. M. Alam, G. Ferrari, Z. Y. Yang, K. E. Seaton, et al. 2014. Vaccine-induced Env V1-V2 IgG3 correlates with lower HIV-1 infection risk and declines soon after vaccination. Sci. Transl. Med. 6: 228ra39.
17. Sundling, C., Z. Zhang, G. E. Phad, Z. Sheng, Y. Wang, J. R. Mascola, Y. Li, R. T. Wyatt, L. Shapiro, and G. B. Karlsson Hedestam. 2014. Single-cell and deep sequencing of IgG-switched macaque B cells reveal a diverse Ig repertoire following immunization. J. Immunol. 192: 3637-3644.
18. Sundling, C., Y. Li, N. Huynh, C. Poulsen, R. Wilson, S. O'Dell, Y. Feng, J. R. Mascola, R. T. Wyatt, and G. B. Karlsson Hedestam. 2012. High-resolution definition of vaccine-elicited B cell responses against the HIV primary receptor binding site. Sci. Transl. Med. 4: 142ra96.
19. Dai, K., L. He, S. N. Khan, S. O'Dell, K. McKee, K. Tran, Y. Li, C. Sundling, C. D. Morris, J. R. Mascola, et al. 2015. Rhesus Macaque B-Cell Responses to an HIV-1 Trimer Vaccine Revealed by Unbiased Longitudinal Repertoire Analysis. MBio 6: e01375-e15.
20. Sundling, C., M. N. Forsell, S. O'Dell, Y. Feng, B. Chakrabarti, S. S. Rao, K. Loré, J. R. Mascola, R. T. Wyatt, I. Douagi, and G. B. Karlsson Hedestam. 2010. Soluble HIV-1 Env trimers in adjuvant elicit potent and diverse functional B cell responses in primates. J. Exp. Med. 207: 2003-2017.
21. Wu, X., Z. Y. Yang, Y. Li, C. M. Hogerkorp, W. R. Schief, M. S. Seaman, T. Zhou, S. D. Schmidt, L. Wu, L. Xu, et al. 2010. Rational design of envelope identifies broadly neutralizing human monoclonal antibodies to HIV-1. Science 329: 856-861.
22. Sundling, C., G. Phad, I. Douagi, M. Navis, and G. B. Karlsson Hedestam. 2012. Isolation of antibody V(D)J sequences from single cell sorted rhesus macaque B cells. J. Immunol. Methods 386: 85-93.
23. Tiller, T., E. Meffre, S. Yurasov, M. Tsuiji, M. C. Nussenzweig, and H. Wardemann. 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.
24. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377.
25. Alamyar, E., V. Giudicelli, S. Li, P. Duroux, and M. P. Lefranc. 2012. IMGT/HighV-QUEST: the IMGT(R) web portal for immunoglobulin (IG) or antibody and T cell receptor (TR) analysis from NGS high throughput and deep sequencing. Immunome Res. DOI: 10.4172/1745-7580.1000056.
26. Ye, J., N. Ma, T. L. Madden, and J. M. Ostell. 2013. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res. 41: W34-W40.
27. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
28. Wu, X., T. Zhou, J. Zhu, B. Zhang, I. Georgiev, C. Wang, X. Chen, N. S. Longo, M. Louder, K. McKee, et al; NISC Comparative Sequencing Program. 2011. Focused evolution of HIV-1 neutralizing antibodies revealed by structures and deep sequencing. Science 333: 1593-1602.
29. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
30. Li, M., F. Gao, J. R. Mascola, L. Stamatatos, V. R. Polonis, M. Koutsoukos, G. Voss, P. Goepfert, P. Gilbert, K. M. Greene, 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.
31. Seaman, M. S., H. Janes, N. Hawkins, L. E. Grandpre, C. Devoy, A. Giri, R. T. Coffey, L. Harris, B. Wood, M. G. Daniels, et al. 2010. Tiered categorization of a diverse panel of HIV-1 Env pseudoviruses for assessment of neutralizing antibodies. J. Virol. 84: 1439-1452.
32. Wu, X., T. Zhou, S. O'Dell, R. T. Wyatt, P. D. Kwong, and J. R. Mascola. 2009. Mechanism of human immunodeficiency virus type 1 resistance to monoclonal antibody B12 that effectively targets the site of CD4 attachment. J. Virol. 83: 10892-10907.
33. Pantophlet, R., E. Ollmann Saphire, P. Poignard, P. W. Parren, I. A. Wilson, and D. R. Burton. 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.
34. Zhou, T., L. Xu, B. Dey, A. J. Hessell, D. Van Ryk, S. H. Xiang, X. Yang, M. Y. Zhang, M. B. Zwick, J. Arthos, et al. 2007. Structural definition of a conserved neutralization epitope on HIV-1 gp120. Nature 445: 732-737.
35. Saphire, E. O., P. W. Parren, R. Pantophlet, M. B. Zwick, G. M. Morris, P. M. Rudd, R. A. Dwek, R. L. Stanfield, D. R. Burton, and I. A. Wilson. 2001. Crystal structure of a neutralizing human IGG against HIV-1: a template for vaccine design. Science 293: 1155-1159.
36. Breden, F., C. Lepik, N. S. Longo, M. Montero, P. E. Lipsky, and J. K. Scott. 2011. Comparison of antibody repertoires produced by HIV-1 infection, other chronic and acute infections, and systemic autoimmune disease. PLoS One 6: e16857.
37. Zhou, T., R. M. Lynch, L. Chen, P. Acharya, X. Wu, N. A. Doria-Rose, M. G. Joyce, D. Lingwood, C. Soto, R. T. Bailer, et al; NISC Comparative Sequencing Program. 2015. Structural Repertoire of HIV-1-Neutralizing Antibodies Targeting the CD4 Supersite in 14 Donors. Cell 161: 1280-1292.
38. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393: 648-659.
39. Chen, L., Y. D. Kwon, T. Zhou, X. Wu, S. O'Dell, L. Cavacini, A. J. Hessell, M. Pancera, M. Tang, L. Xu, et al. 2009. Structural basis of immune evasion at the site of CD4 attachment on HIV-1 gp120. Science 326: 1123-1127.
40. Poulsen, T. R., A. Jensen, J. S. Haurum, and P. S. Andersen. 2011. Limits for antibody affinity maturation and repertoire diversification in hypervaccinated humans. J. Immunol. 187: 4229-4235.
41. Davis, M. M., and Chien, Y.H. 1999. T Cell Antigen Receptors. Lippincott-Raven, Philidelphia.
42. Moody, M. A., N. L. Yates, J. D. Amos, M. S. Drinker, J. A. Eudailey, T. C. Gurley, D. J. Marshall, J. F. Whitesides, X. Chen, A. Foulger, et al. 2012. HIV-1 gp120 vaccine induces affinity maturation in both new and persistent antibody clonal lineages. J. Virol. 86: 7496-7507.
43. Choi, Y.W., A. Herman, D. DiGiusto, T. Wade, P. Marrack, and J. Kappler. 1990. Residues of the variable region of the T-cell-receptor beta-chain that interact with S. aureus toxin superantigens. Nature 346: 471-473.
44. Garcia, K. C., M. Degano, R. L. Stanfield, A. Brunmark, M. R. Jackson, P. A. Peterson, L. Teyton, and I. A. Wilson. 1996. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex. Science 274: 209-219.
45. Li, H., A. Llera, and R. A. Mariuzza. 1998. Structure-function studies of T-cell receptor-superantigen interactions. Immunol. Rev. 163: 177-186.
46. Potter, K. N., Y. Li, and J. D. Capra. 1996. Staphylococcal protein A simultaneously interacts with framework region 1, complementarity-determining region 2, and framework region 3 on human VH3-encoded Igs. J. Immunol. 157: 2982-2988.
47. Throsby, M., E. van den Brink, M. Jongeneelen, L. L. Poon, P. Alard, L. Cornelissen, A. Bakker, F. Cox, E. van Deventer, Y. Guan, et al. 2008. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One 3: e3942.
48. Ekiert, D. C., G. Bhabha, M. A. Elsliger, R. H. Friesen, M. Jongeneelen, M. Throsby, J. Goudsmit, and I. A. Wilson. 2009. Antibody recognition of a highly conserved influenza virus epitope. Science 324: 246-251.
49. Li, Y., S. O'Dell, L. M. Walker, X. Wu, J. Guenaga, Y. Feng, S. D. Schmidt, K. McKee, M. K. Louder, J. E. Ledgerwood, et al. 2011. Mechanism of neutralization by the broadly neutralizing HIV-1 monoclonal antibody VRC01. J. Virol. 85: 8954-8967.
50. Wang, Y., P. Kapoor, R. Parks, A. Silva-Sanchez, S. M. Alam, L. Verkoczy, H. X. Liao, Y. Zhuang, P. Burrows, M. Levinson, et al. 2016. HIV-1 gp140 epitope recognition is influenced by immunoglobulin DH gene segment sequence. Immunogenetics 68: 145-155.
51. Tran, K., C. Poulsen, J. Guenaga, N. de Val, R. Wilson, C. Sundling, Y. Li, R. L. Stanfield, I. A. Wilson, A. B. Ward, et al. 2014. Vaccine-elicited primate antibodies use a distinct approach to the HIV-1 primary receptor binding site informing vaccine redesign. [Published erratum appears in 2014 Proc Natl Acad Sci U S A. 111: E1159.] Proc. Natl. Acad. Sci. USA 111: E738-E747.
52. Sanders, R. W., M. J. van Gils, R. Derking, D. Sok, T. J. Ketas, J. A. Burger, G. Ozorowski, A. Cupo, C. Simonich, L. Goo, et al. 2015. HIV-1 VACCINES. HIV-1 neutralizing antibodies induced by native-like envelope trimers. Science 349: aac4223.
53. Klein, F., R. Diskin, J. F. Scheid, C. Gaebler, H. Mouquet, I. S. Georgiev, M. Pancera, T. Zhou, R. B. Incesu, B. Z. Fu, et al. 2013. Somatic mutations of the immunoglobulin framework are generally required for broad and potent HIV-1 neutralization. Cell 153: 126-138.