Receptor mimicry by antibody F045-092 facilitates universal binding to the H3 subtype of influenza virus

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lee, Peter S ^a   Ohshima, Nobuko ^b   Stanfield, Robyn L ^a   Yu, Wenli ^a   Iba, Yoshitaka ^b   Okuno, Yoshinobu ^c   Kurosawa, Yoshikazu ^b   Wilson, Ian A ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b FUJITA HEALTH UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

F045 092 ANTIBODY; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOGLOBULIN G; INFLUENZA VIRUS HEMAGGLUTININ; NEUTRALIZING ANTIBODY; RECEPTOR; SIALOGLYCAN RECEPTOR; UNCLASSIFIED DRUG; VIRUS ANTIBODY;

ANTIBODY; CRYSTAL STRUCTURE; INFLUENZA; MIMICRY; PROTEIN; VACCINE; VIRUS;

ANTIBODY AFFINITY; ANTIBODY COMBINING SITE; ANTIBODY STRUCTURE; ANTIGEN RECOGNITION; ARTICLE; COMPLEMENTARITY DETERMINING REGION; CROSS REACTION; CRYSTAL STRUCTURE; GLYCOSYLATION; IMMUNE EVASION; INDEL MUTATION; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H13N6); INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H2N2); INFLUENZA A VIRUS (H3N2); INFLUENZA A VIRUS (H3N8); MOLECULAR MIMICRY; NONHUMAN; RECEPTOR AFFINITY; RECEPTOR BINDING; RECEPTOR MIMICRY; VIRUS HEMAGGLUTINATION; VIRUS NEUTRALIZATION; VIRUS STRAIN; BINDING SITE; METABOLISM;

ORTHOMYXOVIRIDAE;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; BINDING SITES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS; INFLUENZA A VIRUS, H3N2 SUBTYPE;

EID: 84911404794     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4614     Document Type: Article

References (64)

1. CDC. Update: influenza activity-United States, September 30, 2012-February 9, 2013. MMWR Morb. Mortal. Wkly. Rep. 62, 124-130 (2013).
2. Le, Q. M. et al. Avian flu: isolation of drug-resistant H5N1 virus. Nature 437, 1108 (2005).
3. Stephenson, I. et al. Neuraminidase inhibitor resistance after oseltamivir treatment of acute influenza A and B in children. Clin. Infect. Dis. 48, 389-396 (2009).
4. Gao, R. et al. Human infection with a novel avian-origin influenza A (H7N9) virus. New Engl. J. Med. 368, 1888-1897 (2013).
5. Cohen, J. Influenza. New flu virus in China worries and confuses. Science 340, 129-130 (2013).
6. Wilson, I. A., Skehel, J. J. & Wiley, D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3Å resolution. Nature 289, 366-373 (1981).
7. Weis, W. et al. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333, 426-431 (1988).
8. Zhu, X. et al. Hemagglutinin homologue from H17N10 bat influenza virus exhibits divergent receptor-binding and pH-dependent fusion activities. Proc. Natl Acad. Sci. USA 110, 1458-1463 (2013).
9. Sun, X. et al. Bat-derived influenza hemagglutinin H17 does not bind canonical avian or human receptors and most likely uses a unique entry mechanism. Cell Rep. 3, 769-778 (2013).
10. Tong, S. et al. New world bats harbor diverse influenza A viruses. PLoS Pathog. 9, e1003657 (2013).
11. Bullough, P. A., Hughson, F. M., Skehel, J. J. & Wiley, D. C. Structure of influenza haemagglutinin at the pH of membrane fusion. Nature 371, 37-43 (1994).
12. Whittle, J. R. et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl Acad. Sci. USA 108, 14216-14221 (2011).
13. Schmidt, A. G. et al. Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody. Proc. Natl Acad. Sci. USA 110, 264-269 (2013).
14. Xu, R. et al. A recurring motif for antibody recognition of the receptor-binding site of influenza hemagglutinin. Nat. Struct. Mol. Biol. 20, 363-370 (2013).
15. Hong, M. et al. Antibody recognition of the pandemic H1N1 influenza hemagglutinin receptor binding site. J. Virol. 87, 12471-12480 (2013).
16. Ekiert, D. C. et al. Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489, 526-532 (2012).
17. Lee, P. S. et al. Heterosubtypic antibody recognition of the influenza virus hemagglutinin receptor binding site enhanced by avidity. Proc. Natl Acad. Sci. USA 109, 17040-17045 (2012).
18. Julien, J. P., Lee, P. S. & Wilson, I. A. Structural insights into key sites of vulnerability on HIV-1 Env and influenza HA. Immunol. Rev. 250, 180-198 (2012).
19. 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).
20. Harris, A. et al. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc. Natl Acad. Sci. USA 103, 19123-19127 (2006).
21. Ekiert, D. C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251 (2009).
22. 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).
23. Tsibane, T. et al. Influenza human monoclonal antibody 1F1 interacts with three major antigenic sites and residues mediating human receptor specificity in H1N1 viruses. PLoS Pathog. 8, e1003067 (2012).
24. Stanfield, R. L., Zemla, A., Wilson, I. A. & Rupp, B. Antibody elbow angles are influenced by their light chain class. J. Mol. Biol. 357, 1566-1574 (2006).
25. Wiley, D. C., Wilson, I. A. & Skehel, J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 289, 373-378 (1981).
26. Sui, J. et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol. 16, 265-273 (2009).
27. Almagro, J. C. et al. Characterization of a high-affinity human antibody with a disulfide bridge in the third complementarity-determining region of the heavy chain. J. Mol. Recognit. 25, 125-135 (2012).
28. Kong, L. et al. Hepatitis C virus E2 envelope glycoprotein core structure. Science 342, 1090-1094 (2013).
29. Ekiert, D. C. et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850 (2011).
30. Dreyfus, C. et al. Highly conserved protective epitopes on influenza B viruses. Science 337, 1343-1348 (2012).
31. Dreyfus, C., Ekiert, D. C. & Wilson, I. A. Structure of a classical broadly neutralizing stem antibody in complex with a pandemic H2 hemagglutinin. J. Virol. 87, 7149-7154 (2013).
32. Friesen, R. H. et al. A common solution to group 2 influenza virus neutralization. Proc. Natl Acad. Sci. USA 111, 450-455 (2014).
33. Skehel, J. J. et al. A carbohydrate side chain on hemagglutinins of Hong Kong influenza viruses inhibits recognition by a monoclonal antibody. Proc. Natl Acad. Sci. USA 81, 1779-1783 (1984).
34. Abe, Y. et al. Effect of the addition of oligosaccharides on the biological activities and antigenicity of influenza A/H3N2 virus hemagglutinin. J. Virol. 78, 9605-9611 (2004).
35. Wang, C. C. et al. Glycans on influenza hemagglutinin affect receptor binding and immune response. Proc. Natl Acad. Sci. USA 106, 18137-18142 (2009).
36. Xu, R. et al. Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science 328, 357-360 (2010).
37. Wei, C. J. et al. Cross-neutralization of 1918 and 2009 influenza viruses: role of glycans in viral evolution and vaccine design. Sci. Transl. Med. 2, 24ra21 (2010).
38. Karlsson Hedestam, G. B. et al. The challenges of eliciting neutralizing antibodies to HIV-1 and to influenza virus. Nat. Rev. Microbiol. 6, 143-155 (2008).
39. Pejchal, R. et al. A potent and broad neutralizing antibody recognizes and penetrates the HIV glycan shield. Science 334, 1097-1103 (2011).
40. McLellan, J. S. et al. Structure of HIV-1 gp120 V1/V2 domain with broadly neutralizing antibody PG9. Nature 480, 336-343 (2011).
41. Julien, J. P. et al. Asymmetric recognition of the HIV-1 trimer by broadly neutralizing antibody PG9. Proc. Natl Acad. Sci. USA 110, 4351-4356 (2013).
42. Pancera, M. et al. Structural basis for diverse N-glycan recognition by HIV-1-neutralizing V1-V2-directed antibody PG16. Nat. Struct. Mol. Biol. 20, 804-813 (2013).
43. Lin, Y. P. et al. Evolution of the receptor binding properties of the influenza A (H3N2) hemagglutinin. Proc. Natl Acad. Sci. USA 109, 21474-21479 (2012).
44. Bizebard, T. et al. Structure of influenza virus haemagglutinin complexed with a neutralizing antibody. Nature 376, 92-94 (1995).
45. Barbey-Martin, C. et al. An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 294, 70-74 (2002).
46. Jardine, J. et al. Rational HIV immunogen design to target specific germline B cell receptors. Science 340, 711-716 (2013).
47. Kanekiyo, M. et al. Self-assembling influenza nanoparticle vaccines elicit broadly neutralizing H1N1 antibodies. Nature 499, 102-106 (2013).
48. Zhang, J. et al. Pentamerization of single-domain antibodies from phage libraries: a novel strategy for the rapid generation of high-avidity antibody reagents. J. Mol. Biol. 335, 49-56 (2004).
49. Wesolowski, J. et al. Single domain antibodies: promising experimental and therapeutic tools in infection and immunity. Med. Microbiol. Immunol. 198, 157-174 (2009).
50. Fleishman, S. J. et al. Computational design of proteins targeting the conserved stem region of influenza hemagglutinin. Science 332, 816-821 (2011).
51. Whitehead, T. A. et al. Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing. Nat. Biotechnol. 30, 543-548 (2012).
52. Niwa, H., Yamamura, K. & Miyazaki, J. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199 (1991).
53. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
54. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
55. Saul, F. A. & Poljak, R. J. Crystal structure of human immunoglobulin fragment Fab New refined at 2.0 Åresolution. Proteins 14, 363-371 (1992).
56. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
57. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
58. Chen, V. B. et al. Mol Probity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
59. McDonald, I. K. & Thornton, J. M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793 (1994).
60. Sheriff, S., Hendrickson, W. A. & Smith, J. L. Structure of myohemerythrin in the azidomet state at 1.7/1.3Å resolution. J. Mol. Biol. 197, 273-296 (1987).
61. Connolly, M. L. Analytical molecular surface calculation. J. Appl. Crystallogr. 16, 548-558 (1983).
62. 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).
63. Bao, Y. et al. The influenza virus resource at the National Center for Biotechnology Information. J. Virol. 82, 596-601 (2008).
64. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).