Defining the antibody cross-reactome directed against the influenza virus surface glycoproteins

Nature Immunology

Volumn 18, Issue 4, 2017, Pages 464-473

  Nachbagauer, Raffael ^a   Choi, Angela ^a   Hirsh, Ariana ^a   Margine, Irina ^a   Iida, Sayaka ^b   Barrera, Aldo ^c   Ferres, Marcela ^c   Albrecht, Randy A ^a   García Sastre, Adolfo ^a   Bouvier, Nicole M ^a   Ito, Kimihito ^b   Medina, Rafael A ^a,c   Palese, Peter ^a   Krammer, Florian ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS REACTING ANTIBODY; INFLUENZA VIRUS HEMAGGLUTININ; VIRUS GLYCOPROTEIN; VIRUS SIALIDASE; IMMUNOGLOBULIN G; NA PROTEIN, INFLUENZA A VIRUS; SIALIDASE; VIRAL PROTEIN; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; EXPERIMENTAL GUINEA PIG; FERRET; HUMAN; HUMORAL IMMUNITY; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); MICROBIAL DIVERSITY; MIDDLE AGED; MOUSE; NONHUMAN; PRIORITY JOURNAL; YOUNG ADULT; ADOLESCENT; AGE; ANIMAL; CLASSIFICATION; CLUSTER ANALYSIS; DISEASE MODEL; FEMALE; GUINEA PIG; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS; MALE; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRUS INFECTION;

ADOLESCENT; ADULT; AGE FACTORS; ANIMALS; ANTIBODIES, VIRAL; CLUSTER ANALYSIS; CROSS REACTIONS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FERRETS; GUINEA PIGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MALE; MICE; MIDDLE AGED; NEURAMINIDASE; ORTHOMYXOVIRIDAE INFECTIONS; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS; YOUNG ADULT;

EID: 85012257296     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3684     Document Type: Article

References (45)

1. Jayasundara, K., Soobiah, C., Thommes, E., Tricco, A.C. & Chit, A. Natural attack rate of influenza in unvaccinated children and adults: a meta-regression analysis. BMC Infect. Dis. 14, 670 (2014).
2. Krammer, F. & Palese, P. Advances in the development of influenza virus vaccines. Nat. Rev. Drug Discov. 14, 167-182 (2015).
3. Horimoto, T. & Kawaoka, Y. Influenza: lessons from past pandemics, warnings from current incidents. Nat. Rev. Microbiol. 3, 591-600 (2005).
4. Wrammert, J. et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J. Exp. Med. 208, 181-193 (2011).
5. Pica, N. et al. Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses. Proc. Natl. Acad. Sci. USA 109, 2573-2578 (2012).
6. Margine, I. et al. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice. J. Virol. 87, 4728-4737 (2013).
7. Yu, X. et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455, 532-536 (2008).
8. Ohmit, S.E., Petrie, J.G., Cross, R.T., Johnson, E. & Monto, A.S. Influenza hemagglutination-inhibition antibody titer as a correlate of vaccine-induced protection. J. Infect. Dis. 204, 1879-1885 (2011).
9. Heaton, N.S., Sachs, D., Chen, C.J., Hai, R. & Palese, P. Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins. Proc. Natl. Acad. Sci. USA 110, 20248-20253 (2013).
10. Yewdell, J.W., Webster, R.G. & Gerhard, W.U. Antigenic variation in three distinct determinants of an influenza type A haemagglutinin molecule. Nature 279, 246-248 (1979).
11. Wohlbold, T.J. & Krammer, F. In the shadow of hemagglutinin: a growing interest in influenza viral neuraminidase and its role as a vaccine antigen. Viruses 6, 2465-2494 (2014).
12. Yang, X. et al. A beneficiary role for neuraminidase in influenza virus penetration through the respiratory mucus. PLoS One 9, e110026 (2014).
13. Wohlbold, T.J. et al. Vaccination with adjuvanted recombinant neuraminidase induces broad heterologous, but not heterosubtypic, cross-protection against influenza virus infection in mice. MBio 6, e02556 (2015).
14. Easterbrook, J.D. et al. Protection against a lethal H5N1 influenza challenge by intranasal immunization with virus-like particles containing 2009 pandemic H1N1 neuraminidase in mice. Virology 432, 39-44 (2012).
15. Ekiert, D.C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246-251 (2009).
16. Ekiert, D.C. et al. A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333, 843-850 (2011).
17. 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).
18. Dreyfus, C. et al. Highly conserved protective epitopes on influenza B viruses. Science 337, 1343-1348 (2012).
19. Jegaskanda, S., Weinfurter, J.T., Friedrich, T.C. & Kent, S.J. Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques. J. Virol. 87, 5512-5522 (2013).
20. Jegaskanda, S. et al. Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J. Immunol. 190, 1837-1848 (2013).
21. Laidlaw, B.J. et al. Cooperativity between CD8+ T cells, non-neutralizing antibodies, and alveolar macrophages is important for heterosubtypic influenza virus immunity. PLoS Pathog. 9, e1003207 (2013).
22. DiLillo, D.J., Palese, P., Wilson, P.C. & Ravetch, J.V. Broadly neutralizing anti-influenza antibodies require Fc receptor engagement for in vivo protection. J. Clin. Invest. 126, 605-610 (2016).
23. Terajima, M. et al. Complement-dependent lysis of influenza a virus-infected cells by broadly cross-reactive human monoclonal antibodies. J. Virol. 85, 13463-13467 (2011).
24. DiLillo, D.J., Tan, G.S., Palese, P. & Ravetch, J.V. Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat. Med. 20, 143-151 (2014).
25. Nachbagauer, R. et al. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans. J. Virol. 88, 13260-13268 (2014).
26. Henry Dunand, C.J. et al. Both neutralizing and non-neutralizing human H7N9 influenza vaccine-induced monoclonal antibodies confer protection. Cell Host Microbe 19, 800-813 (2016).
27. Krause, J.C. et al. Human monoclonal antibodies to pandemic 1957 H2N2 and pandemic 1968 H3N2 influenza viruses. J. Virol. 86, 6334-6340 (2012).
28. Smith, G.J. et al. Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122-1125 (2009).
29. Krammer, F. & Palese, P. Universal influenza virus vaccines: need for clinical trials. Nat. Immunol. 15, 3-5 (2014).
30. Miller, M.S. et al. Neutralizing antibodies against previously encountered influenza virus strains increase over time: a longitudinal analysis. Sci. Transl. Med. 5, 198ra107 (2013).
31. Krammer, F. & Palese, P. Influenza virus hemagglutinin stalk-based antibodies and vaccines. Curr. Opin. Virol. 3, 521-530 (2013).
32. Li, Y. et al. Immune history shapes specificity of pandemic H1N1 influenza antibody responses. J. Exp. Med. 210, 1493-1500 (2013).
33. Garten, R.J. et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325, 197-201 (2009).
34. Li, G.M. et al. Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc. Natl. Acad. Sci. USA 109, 9047-9052 (2012).
35. Gao, R. et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N. Engl. J. Med. 368, 1888-1897 (2013).
36. Chen, H. et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet 383, 714-721 (2014).
37. Martinez-Sobrido, L. & Garcia-Sastre, A. Generation of recombinant influenza virus from plasmid DNA. J. Vis. Exp. 42, 2057 (2010).
38. Krammer, F. et al. Trichoplusia ni cells (High Five) are highly efficient for the production of influenza A virus-like particles: a comparison of two insect cell lines as production platforms for influenza vaccines. Mol. Biotechnol. 45, 226-234 (2010).
39. Krammer, F. et al. A carboxy-terminal trimerization domain stabilizes conformational epitopes on the stalk domain of soluble recombinant hemagglutinin substrates. PLoS One 7, e43603 (2012).
40. Margine, I., Palese, P. & Krammer, F. Expression of functional recombinant hemagglutinin and neuraminidase proteins from the novel H7N9 influenza virus using the baculovirus expression system. J. Vis. Exp. 81, e51112 (2013).
41. Xu, X., Zhu, X., Dwek, R.A., Stevens, J. & Wilson, I.A. Structural characterization of the 1918 influenza virus H1N1 neuraminidase. J. Virol. 82, 10493-10501 (2008).
42. Stevens, J. et al. Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science 303, 1866-1870 (2004).
43. Fonville, J.M. et al. Antibody landscapes after influenza virus infection or vaccination. Science 346, 996-1000. (2014).
44. Ito, K. et al. Gnarled-trunk evolutionary model of influenza A virus hemagglutinin. PLoS One 6, e25953 (2011).
45. Borg, I. & Groenen, P. Modern Multidimensional Scaling: Theory and Applications (Springer, 2005).