Epitope specificity plays a critical role in regulating antibody-dependent cell-mediated cytotoxicity against influenza A virus

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 42, 2016, Pages 11931-11936

  He, Wenqian ^a   Tan, Gene S ^a   Mullarkey, Caitlin E ^a   Lee, Amanda J ^b   Lam, Mannie Man Wai ^c   Krammer, Florian ^a   Henry, Carole ^d   Wilson, Patrick C ^d   Ashkar, Ali A ^b   Palese, Peter ^a,b   Miller, Matthew S ^c  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b MCMASTER UNIVERSITY   (Canada)

^c MCMASTER UNIVERSITY   (Canada)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

ADCC; Antibody; Fc receptor; Influenza virus; NK cell

Indexed keywords

EPITOPE; FC RECEPTOR; IMMUNOGLOBULIN G; INFLUENZA VIRUS HEMAGGLUTININ; POLYCLONAL ANTIBODY; VIRUS GLYCOPROTEIN; BIOLOGICAL MARKER; IMMUNOGLOBULIN FC FRAGMENT; NEUTRALIZING ANTIBODY; PROTEIN BINDING; VIRUS ANTIBODY; VIRUS ANTIGEN;

ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY PRODUCTION; ANTIBODY SPECIFICITY; ARTICLE; BINDING COMPETITION; CELL SURFACE; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; INFLUENZA A VIRUS; NONHUMAN; PRIORITY JOURNAL; VIRUS PARTICLE; ANTIBODY AFFINITY; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; IMMUNOLOGY; INFLUENZA; METABOLISM; NATURAL KILLER CELL; PROTEIN DOMAIN; VIROLOGY;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, VIRAL; BINDING, COMPETITIVE; BIOMARKERS; CELL LINE; EPITOPES; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNOGLOBULIN FC FRAGMENTS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS; INFLUENZA, HUMAN; KILLER CELLS, NATURAL; MODELS, BIOLOGICAL; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECEPTORS, FC;

EID: 84991660674     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1609316113     Document Type: Article

References (44)

1. Krammer F, Palese P (2015) Advances in the development of influenza virus vaccines. Nat Rev Drug Discov 14(3):167-182.
2. Miller MS, et al. (2013) 1976 and 2009 H1N1 influenza virus vaccines boost antihemagglutinin stalk antibodies in humans. J Infect Dis 207(1):98-105.
3. Miller MS, et al. (2013) Neutralizing antibodies against previously encountered influenza virus strains increase over time: A longitudinal analysis. Sci Transl Med 5(198):198ra107.
4. Ellebedy AH, et al. (2014) Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc Natl Acad Sci USA 111(36):13133-13138.
5. Li G-M, et al. (2012) Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci USA 109(23):9047-9052.
6. Wrammert J, et al. (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208(1):181-193.
7. Halliley JL, et al. (2015) High-affinity H7 head and stalk domain-specific antibody responses to an inactivated influenza H7N7 vaccine after priming with live attenuated influenza vaccine. J Infect Dis 212(8):1270-1278.
8. Pica N, et al. (2012) 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(7):2573-2578.
9. Krammer F, et al. (2014) H3 stalk-based chimeric hemagglutinin influenza virus constructs protect mice from H7N9 challenge. J Virol 88(4):2340-2343.
10. Krammer F, Pica N, Hai R, Tan GS, Palese P (2012) Hemagglutinin stalk-reactive antibodies are boosted following sequential infection with seasonal and pandemic H1N1 influenza virus in mice. J Virol 86(19):10302-10307.
11. Krammer F, et al. (2014) Assessment of influenza virus hemagglutinin stalk-based immunity in ferrets. J Virol 88(6):3432-3442.
12. Steel J, et al. (2010) Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 1(1):e00018-10.
13. Wohlbold TJ, et al. (2015) Vaccination with soluble headless hemagglutinin protects mice from challenge with divergent influenza viruses. Vaccine 33(29):3314-3321.
14. Yassine HM, et al. (2015) Hemagglutinin-stem nanoparticles generate heterosubtypic influenza protection. Nat Med 21(9):1065-1070.
15. Impagliazzo A, et al. (2015) A stable trimeric influenza hemagglutinin stem as a broadly protective immunogen. Science 349(6254):1301-6.
16. Krammer F, Palese P (2014) Universal influenza virus vaccines: Need for clinical trials. Nat Immunol 15(1):3-5.
17. Brandenburg B, et al. (2013) Mechanisms of hemagglutinin targeted influenza virus neutralization. PLoS One 8(12):e80034.
18. He W, et al. (2015) Broadly neutralizing anti-influenza virus antibodies: Enhancement of neutralizing potency in polyclonal mixtures and IgA backbones. J Virol 89(7):3610-3618.
19. He W, Mullarkey CE, Miller MS (2015) Measuring the neutralization potency of influenza A virus hemagglutinin stalk/stem-binding antibodies in polyclonal preparations by microneutralization assay. Methods 90:95-100.
20. DiLillo DJ, Tan GS, Palese P, Ravetch JV (2014) Broadly neutralizing hemagglutinin stalk-specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat Med 20(2):143-151.
21. Kramski M, Stratov I, Kent SJ (2015) The role of HIV-specific antibody-dependent cellular cytotoxicity in HIV prevention and the influence of the HIV-1 Vpu protein. AIDS 29(2):137-144.
22. Jegaskanda S, Reading PC, Kent SJ (2014) Influenza-specific antibody-dependent cellular cytotoxicity: Toward a universal influenza vaccine. J Immunol 193(2):469-475.
23. DiLillo DJ, Ravetch JV (2015) Differential Fc-receptor engagement drives an antitumor vaccinal effect. Cell 161(5):1035-1045.
24. Tan GS, et al. (2014) Characterization of a broadly neutralizing monoclonal antibody that targets the fusion domain of group 2 influenza A virus hemagglutinin. J Virol 88(23):13580-13592.
25. Moran TM, et al. (1987) Characterization of variable-region genes and shared cross-reactive idiotypes of antibodies specific for antigens of various influenza viruses. Viral Immunol 1(1):1-12.
26. Ekiert DC, et al. (2012) Cross-neutralization of influenza A viruses mediated by a single antibody loop. Nature 489(7417):526-532.
27. Ekiert DC, et al. (2011) A highly conserved neutralizing epitope on group 2 influenza A viruses. Science 333(6044):843-850.
28. Wohlbold TJ, et al. (2015) Hemagglutinin stalk- and neuraminidase-specific monoclonal antibodies protect against lethal H10N8 influenza virus infection in mice. J Virol 90(2):851-861.
29. Wohlbold TJ, et al. (2015) Vaccination with adjuvanted recombinant neuraminidase induces broad heterologous, but not heterosubtypic, cross-protection against influenza virus infection in mice. MBio 6(2):e02556.
30. Monto AS, et al. (2015) Antibody to influenza virus neuraminidase: An independent correlate of protection. J Infect Dis 212(8):1191-1199.
31. Jegaskanda S, et al. (2014) Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity in intravenous immunoglobulin as a potential therapeutic against emerging influenza viruses. J Infect Dis 210(11):1811-1822.
32. Jegaskanda S, et al. (2013) Age-associated cross-reactive antibody-dependent cellular cytotoxicity toward 2009 pandemic influenza A virus subtype H1N1. J Infect Dis 208(7):1051-1061.
33. Jegaskanda S, Weinfurter JT, Friedrich TC, Kent SJ (2013) Antibody-dependent cellular cytotoxicity is associated with control of pandemic H1N1 influenza virus infection of macaques. J Virol 87(10):5512-5522.
34. Jegaskanda S, et al. (2013) Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J Immunol 190(4):1837-1848.
35. Co MDT, et al. (2014) Relationship of preexisting influenza hemagglutination inhibition, complement-dependent lytic, and antibody-dependent cellular cytotoxicity antibodies to the development of clinical illness in a prospective study of A(H1N1) pdm09 influenza in children. Viral Immunol 27(8):375-382.
36. Terajima M, Co MDT, Cruz J, Ennis FA (2015) High antibody-dependent cellular cytotoxicity antibody titers to H5N1 and H7N9 avian influenza A viruses in healthy US adults and older children. J Infect Dis 212(7):1052-1060.
37. DiLillo DJ, Palese P, Wilson PC, Ravetch JV (2016) Broadly neutralizing anti-influenza antibodies require Fc receptor engagement for in vivo protection. J Clin Invest 126(2):605-610.
38. Henry Dunand CJ, et al. (2016) Both neutralizing and non-neutralizing human H7N9 influenza vaccine-induced monoclonal antibodies confer protection. Cell Host Microbe 19(6):800-813.
39. Wang TT, et al. (2015) Anti-HA glycoforms drive B cell affinity selection and determine influenza vaccine efficacy. Cell 162(1):160-169.
40. Pincetic A, et al. (2014) Type I and type II Fc receptors regulate innate and adaptive immunity. Nat Immunol 15(8):707-716.
41. Palese P, Shaw M (2007) Orthomyxoviridae: The viruses and their replication. Fields Virology, eds Knipe DM, et al. (Lippincott Williams & Wilkins, Philadelphia), 5th Ed, pp 1647-1690.
42. Nimmerjahn F, Ravetch JV (2008) Fcgamma receptors as regulators of immune responses. Nat Rev Immunol 8(1):34-47.
43. Andrews SF, et al. (2015) Immune history profoundly affects broadly protective B cell responses to influenza. Sci Transl Med 7(316):316ra192-316ra192.
44. Denman CJ, et al. (2012) Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One 7(1):e30264.