Antibodies VRC01 and 10E8 neutralize HIV-1 with high breadth and potency even with ig-framework regions substantially reverted to germline

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1100-1106

  Georgiev, Ivelin S ^a   Rudicell, Rebecca S ^a   Saunders, Kevin O ^a   Shi, Wei ^a   Kirys, Tatsiana ^a   McKee, Krisha ^a   O'Dell, Sijy ^a   Chuang, Gwo Yu ^a   Yang, Zhi Yong ^a   Ofek, Gilad ^a   Connors, Mark ^a   Mascola, John R ^a   Nabel, Gary J ^a   Kwong, Peter D ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS ANTIBODY; IMMUNOGLOBULIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; NEUTRALIZING ANTIBODY 10E8; NEUTRALIZING ANTIBODY VRC01; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DRUG POTENCY; DRUG SCREENING; DRUG STRUCTURE; DRUG TARGETING; GERM LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; IC 50; IMMUNOGENICITY; IMMUNOGLOBULIN VARIABLE REGION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERTANT; SOMATIC HYPERMUTATION; VIRUS NEUTRALIZATION; VIRUS STRAIN;

AMINO ACID SEQUENCE; GENES, IMMUNOGLOBULIN; GERM-LINE MUTATION; HIV ANTIBODIES; HIV-1; HUMANS; IMMUNOGLOBULIN HEAVY CHAINS; IMMUNOGLOBULIN LIGHT CHAINS; INHIBITORY CONCENTRATION 50; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUTRALIZATION TESTS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOMATIC HYPERMUTATION, IMMUNOGLOBULIN;

EID: 84893352067     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302515     Document Type: Article

References (37)

1. 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.
2. Walker, L. M., M. Huber, K. J. Doores, E. Falkowska, R. Pejchal, J. P. Julien, S. K. Wang, A. Ramos, P. Y. Chan-Hui, M. Moyle, et al; Protocol G Principal Investigators. 2011. Broad neutralization coverage of HIV by multiple highly potent antibodies. Nature 477: 466-470.
3. Scheid, J. F., H. Mouquet, B. Ueberheide, R. Diskin, F. Klein, T. Y. Oliveira, J. Pietzsch, D. Fenyo, A. Abadir, K. Velinzon, et al. 2011. Sequence and structural convergence of broad and potent HIV antibodies that mimic CD4 binding. Science 333: 1633-1637.
4. 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.
5. Walker, L. M., S. K. Phogat, P. Y. Chan-Hui, D. Wagner, P. Phung, J. L. Goss, T. Wrin, M. D. Simek, S. Fling, J. L. Mitcham, 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: 285-289.
6. Liao, H. X., R. Lynch, T. Zhou, F. Gao, S. M. Alam, S. D. Boyd, A. Z. Fire, K. M. Roskin, C. A. Schramm, Z. Zhang, et al; NISC Comparative Sequencing Program. 2013. Co-evolution of a broadly neutralizing HIV-1 antibody and founder virus. Nature 496: 469-476.
7. Georgiev, I. S., N. A. Doria-Rose, T. Zhou, Y. D. Kwon, R. P. Staupe, S. Moquin, G. Y. Chuang, M. K. Louder, S. D. Schmidt, H. R. Altae-Tran, et al. 2013. Delineating antibody recognition in polyclonal sera from patterns of HIV-1 isolate neutralization. Science 340: 751-756.
8. Corti, D., J. P. Langedijk, A. Hinz, M. S. Seaman, F. Vanzetta, B. M. Fernandez-Rodriguez, C. Silacci, D. Pinna, D. Jarrossay, S. Balla- Jhagjhoorsingh, 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.
9. Zhou, T., J. Zhu, X. Wu, S. Moquin, B. Zhang, P. Acharya, I. S. Georgiev, H. R. Altae-Tran, G. Y. Chuang, M. G. Joyce, et al; NISC Comparative Sequencing Program. 2013. Multidonor analysis reveals structural elements, genetic determinants, and maturation pathway for HIV-1 neutralization by VRC01-class antibodies. Immunity 39: 245-258.
10. Huang, J., G. Ofek, L. Laub, M. K. Louder, N. A. Doria-Rose, N. S. Longo, H. Imamichi, R. T. Bailer, B. Chakrabarti, S. K. Sharma, et al. 2012. Broad and potent neutralization of HIV-1 by a gp41-specific human antibody. Nature 491: 406-412.
11. Moldt, B., E. G. Rakasz, N. Schultz, P. Y. Chan-Hui, K. Swiderek, K. L. Weisgrau, S. M. Piaskowski, Z. Bergman, D. I. Watkins, P. Poignard, and D. R. Burton. 2012. Highly potent HIV-specific antibody neutralization in vitro translates into effective protection against mucosal SHIV challenge in vivo. Proc. Natl. Acad. Sci. USA 109: 18921-18925.
12. Balazs, A. B., J. Chen, C. M. Hong, D. S. Rao, L. Yang, and D. Baltimore. 2011. Antibody-based protection against HIV infection by vectored immunoprophylaxis. Nature 481: 81-84.
13. Klein, F., A. Halper-Stromberg, J. A. Horwitz, H. Gruell, J. F. Scheid, S. Bournazos, H. Mouquet, L. A. Spatz, R. Diskin, A. Abadir, et al. 2012. HIV therapy by a combination of broadly neutralizing antibodies in humanized mice. Nature 492: 118-122.
14. Saunders, K. O., R. S. Rudicell, and G. J. Nabel. 2012. The design and evaluation of HIV-1 vaccines. AIDS 26: 1293-1302.
15. Scheid, J. F., H. Mouquet, N. Feldhahn, M. S. Seaman, K. Velinzon, J. Pietzsch, R. G. Ott, R. M. Anthony, H. Zebroski, A. Hurley, et al. 2009. Broad diversity of neutralizing antibodies isolated from memory B cells in HIV-infected individuals. Nature 458: 636-640.
16. Allen, C. D., T. Okada, and J. G. Cyster. 2007. Germinal-center organization and cellular dynamics. Immunity 27: 190-202.
17. 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.
18. 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.
19. Zhou, T., I. Georgiev, X. Wu, Z. Y. Yang, K. Dai, A. Finzi, Y. D. Kwon, J. F. Scheid, W. Shi, L. Xu, et al. 2010. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329: 811-817.
20. Hoot, S., A. T. McGuire, K. W. Cohen, R. K. Strong, L. Hangartner, F. Klein, R. Diskin, J. F. Scheid, D. N. Sather, D. R. Burton, and L. Stamatatos. 2013. Recombinant HIV envelope proteins fail to engage germline versions of anti-CD4bs bNAbs. PLoS Pathog. 9: e1003106.
21. Di Noia, J. M., and M. S. Neuberger. 2007. Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76: 1-22.
22. Bates, J. T., C. J. Keefer, T. J. Utley, B. E. Correia, W. R. Schief, and J. E. Crowe, Jr. 2013. Reversion of somatic mutations of the respiratory syncytial virusspecific human monoclonal antibody Fab19 reveal a direct relationship between association rate and neutralizing potency. J. Immunol. 190: 3732-3739.
23. Lingwood, D., P. M. McTamney, H. M. Yassine, J. R. Whittle, X. Guo, J. C. Boyington, C.-J. Wei, and G. J. Nabel. 2012. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 489: 566-570.
24. Huber, M., K. M. Le, K. J. Doores, Z. Fulton, R. L. Stanfield, I. A. Wilson, and D. R. Burton. 2010. Very few substitutions in a germ line antibody are required to initiate significant domain exchange. J. Virol. 84: 10700-10707.
25. Lo, B. K. 2004. Antibody humanization by CDR grafting. Methods Mol. Biol. 248: 135-159.
26. Gainza, P., K. E. Roberts, I. Georgiev, R. H. Lilien, D. A. Keedy, C.-Y. Chen, F. Reza, A. C. Anderson, D. C. Richardson, J. S. Richardson, and B. R. Donald. 2013. OSPREY: protein design with ensembles, flexibility, and provable algorithms. Methods Enzymol. 523: 87-107.
27. Chen, C.-Y., I. Georgiev, A. C. Anderson, and B. R. Donald. 2009. Computational structure-based redesign of enzyme activity. Proc. Natl. Acad. Sci. USA 106: 3764-3769.
28. Chen, V. B., W. B. Arendall, III, J. J. Headd, D. A. Keedy, R. M. Immormino, G. J. Kapral, L. W. Murray, J. S. Richardson, and D. C. Richardson. 2010. MolProbity: all-Atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 12-21.
29. Schrodinger, LLC. 2010. The PyMOL molecular graphics system, version 1.4. http://www.pymol.org/pymol.
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. De Pascalis, R., M. Iwahashi, M. Tamura, E. A. Padlan, N. R. Gonzales, A. D. Santos, M. Giuliano, P. Schuck, J. Schlom, and S. V. Kashmiri. 2002. Grafting of "abbreviated" complementarity-determining regions containing specificity-determining residues essential for ligand contact to engineer a less immunogenic humanized monoclonal antibody. J. Immunol. 169: 3076-3084.
34. Kim, J. H., and H. J. Hong. 2012. Humanization by CDR grafting and specificitydetermining residue grafting. Methods Mol. Biol. 907: 237-245.
35. Pancera, M., J. S. McLellan, X. Wu, J. Zhu, A. Changela, S. D. Schmidt, Y. Yang, T. Zhou, S. Phogat, J. R. Mascola, and P. D. Kwong. 2010. Crystal structure of PG16 and chimeric dissection with somatically related PG9: structure-function analysis of two quaternary-specific antibodies that effectively neutralize HIV-1. J. Virol. 84: 8098-8110.
36. Jardine, J., J. P. Julien, S. Menis, T. Ota, O. Kalyuzhniy, A. McGuire, D. Sok, P. S. Huang, S. MacPherson, M. Jones, et al. 2013. Rational HIV immunogen design to target specific germline B cell receptors. Science 340: 711-716.
37. Georgiev, I. S., M. G. Joyce, T. Zhou, and P. D. Kwong. 2013. Elicitation of HIV-1-neutralizing antibodies against the CD4-binding site. Curr. Opin. HIV AIDS 8: 382-391.