Cross-neutralization of influenza A viruses mediated by a single antibody loop

Nature

Volumn 489, Issue 7417, 2012, Pages 526-532

  Ekiert, Damian C ^a,e   Kashyap, Arun K ^b   Steel, John ^c,f   Rubrum, Adam ^d   Bhabha, Gira ^a   Khayat, Reza ^a   Lee, Jeong Hyun ^b   Dillon, Michael A ^b,g   O'Neil, Ryann E ^b,h   Faynboym, Aleksandr M ^b   Horowitz, Michael ^b   Horowitz, Lawrence ^b   Ward, Andrew B ^a   Palese, Peter ^c   Webby, Richard ^d   Lerner, Richard A ^a   Bhatt, Ramesh R ^b   Wilson, Ian A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Sea Lane Biotechnologies ^*  (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f GENENTECH INC   (United States)

^g NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^h EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; EPITOPE; HEMAGGLUTININ; INFLUENZA VACCINE; NIGRANTYL; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ANTIBODY; ANTIGEN; BIOCHEMISTRY; CHEMICAL BINDING; ELECTRON MICROSCOPY; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLUENZA; NEUTRALIZATION; PHYSIOLOGY; PROTEIN; VIRUS;

ANTIBODY ISOLATION; ANTIVIRAL ACTIVITY; ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; DRUG EFFICACY; ELECTRON MICROSCOPY; IN VIVO STUDY; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOOTPRINTING; RECEPTOR BINDING; VIRUS NEUTRALIZATION; VIRUS STRAIN; X RAY;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY SPECIFICITY; ANTIGENS, VIRAL; BINDING SITES; COMPLEMENTARITY DETERMINING REGIONS; CONSERVED SEQUENCE; CROSS REACTIONS; CRYSTALLOGRAPHY, X-RAY; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA VACCINES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN CONFORMATION;

INFLUENZA A VIRUS;

EID: 84866953140     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11414     Document Type: Article

References (50)

1. Smith, T. J., Chase, E. S., Schmidt, T. J., Olson, N. H. & Baker, T. S. Neutralizing antibody tohuman rhinovirus14penetrates the receptor-binding canyon. Nature 383, 350-354 (1996).
2. Labrijn, A. F. et al. Access of antibody molecules to the conserved coreceptor binding site on glycoprotein gp120 is sterically restricted on primary human immunodeficiency virus type 1. J. Virol. 77, 10557-10565 (2003).
3. Rühlmann, A., Kukla, D., Schwager, P., Bartels, K. & Huber, R. Structure of the complex formed by bovine trypsin and bovine pancreatic trypsin inhibitor. Crystal structure determination and stereochemistryof the contact region. J. Mol. Biol. 77, 417-436 (1973).
4. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
5. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103 (2011).
6. Pejchal, R. et al. Structure and functionofbroadly reactive antibody PG16 reveal an H3 subdomain that mediates potent neutralization of HIV-1. Proc. Natl Acad. Sci. USA 107, 11483-11488 (2010).
7. Kashyap, A. K. et al. Combinatorial antibody libraries from survivors of the Turkish H5N1 avian influenza outbreak reveal virus neutralization strategies. Proc. Natl Acad. Sci. USA 105, 5986-5991 (2008).
8. Kashyap, A. K. et al. Protection from the 2009 H1N1 pandemic influenza by an antibody from combinatorial survivor-based libraries. PLoS Pathogens 6, e1000990 (2010).
9. Ekiert, D. C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251 (2009).
10. 1memoryB cells. PLoS ONE 3, e3942 (2008).
11. Sui, J. et al. Structural and functional bases for broad-spectrum neutralization of avianand humaninfluenzaAviruses. Nature Struct. Mol. Biol. 16, 265-273(2009).
12. Ekiert, D. C. et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850 (2011).
13. Corti, D. et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 333, 850-856 (2011).
14. Corti, D. et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest. 120, 1663-1673 (2010).
15. Wrammert, J. et al. Broadly cross-reactive antibodies dominate the human B cell responseagainst 2009pandemicH1N1influenza virus infection. J. Exp. Med. 208, 181-193 (2011).
16. Wei, C. J. et al. Induction of broadly neutralizing H1N1 influenza antibodies by vaccination. Science 329, 1060-1064 (2010).
17. Barbey-Martin, C. et al. An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 294, 70-74 (2002).
18. Fleury, D., Wharton, S. A., Skehel, J. J., Knossow, M. & Bizebard, T. Antigen distortion allows influenza virus to escape neutralization. Nature Struct. Biol. 5, 119-123 (1998).
19. Xu, R. et al. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328, 357-360 (2010).
20. Whittle, J. R. R. et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocketof influenza virus hemagglutinin. Proc. Natl Acad. Sci. USA 108, 14216-14221 (2011).
21. Fleury, D. et al. A complex of influenza hemagglutinin with a neutralizing antibody that binds outside the virus receptor binding site. Nature Struct. Biol. 6, 530-534 (1999).
22. Fleury, D., Daniels, R. S., Skehel, J. J., Knossow, M. & Bizebard, T. Structural evidence for recognitionof a single epitope bytwo distinct antibodies. Proteins 40, 572-578 (2000).
23. Yoshida, R. et al. Cross-protective potential of a novel monoclonal antibody directed against antigenic site B of the hemagglutinin of influenza A viruses. PLoS Pathog. 5, e1000350 (2009).
24. Ohshima, N. et al. Naturally occurring antibodies in humans can neutralize a variety of influenza virus strains, including H3, H1, H2, and H5. J. Virol. 85, 11048-11057 (2011).
25. Okuno, Y., Isegawa, Y., Sasao, F. & Ueda, S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J. Virol. 67, 2552-2558 (1993).
26. Lee, H. et al. Reactivity-based one-pot synthesis of oligomannoses: defining antigens recognized by 2G12, a broadly neutralizing anti-HIV-1 antibody. Angew. Chem. Int. Ed. 43, 1000-1003 (2004).
27. Calarese, D. A. et al. Antibody domain exchange is an immunological solution to carbohydrate cluster recognition. Science 300, 2065-2071 (2003).
28. Mouquet, H. et al. Polyreactivity increases the apparent affinity of anti-HIV antibodies by heteroligation. Nature 467, 591-595 (2010).
29. Pancera, M. et al. 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 (2010).
30. Wilson, P. C. et al. Somatic hypermutation introduces insertions and deletions into immunoglobulin V genes. J. Exp. Med. 187, 59-70 (1998).
31. de Wildt, R. M., van Venrooij, W. J., Winter, G., Hoet, R. M. & Tomlinson, I. M. Somatic insertions and deletions shape the human antibody repertoire. J. Mol. Biol. 294, 701-710 (1999).
32. Krause, J. C. et al. An insertion mutation that distorts antibody binding site architecture enhances functionofahuman antibody. mBio2, e00345-10 (2011).
33. Zhou, T. et al. Structural basis for broad and potent neutralization of HIV-1 by antibody VRC01. Science 329, 811-817 (2010).
34. Bao, Y. et al. The influenza virus resource at the National Center for Biotechnology Information. J. Virol. 82, 596-601 (2008).
35. Hensley, S. E. et al. Hemagglutinin receptor binding avidity drives influenza A virus antigenic drift. Science 326, 734-736 (2009).
36. Fleishman, S. J. et al. Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332, 816-821 (2011).
37. Abhinandan, K. R. & Martin, A. C. Analysis and improvements to Kabat and structurally correct numbering of antibody variable domains. Mol. Immunol. 45, 3832-3839 (2008).
38. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
39. Fodor, E. et al. Rescue of influenza A virus from recombinant DNA. J. Virol. 73, 9679-9682 (1999).
40. Miyazaki, J. et al. Expression vector system based on the chicken b-actin promoter directs efficient production of interleukin-5. Gene 79, 269-277 (1989).
41. Brown, P. H., Cronan, J. E., Grotli, M. & Beckett, D. The biotin repressor: modulation of allostery by corepressor analogs. J. Mol. Biol. 337, 857-869 (2004).
42. Lander, G. C. et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing. J. Struct. Biol. 166, 95-102 (2009).
43. Voss, N. R., Yoshioka, C. K., Radermacher, M., Potter, C. S. & Carragher, B. DoG Picker and Tilt Picker: software tools to facilitate particle selection in single particle electron microscopy. J. Struct. Biol. 166, 205-213 (2009).
44. Mindell, J. A. & Grigorieff, N. Accurate determinationof local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
45. Hohn, M. et al. SPARX, a new environment for cryo-EM image processing. J. Struct. Biol. 157, 47-55 (2007).
46. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007).
47. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
48. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
49. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
50. Chen, V. B. et al. Mol Probity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D 66, 12-21 (2010).