Broadly neutralizing hemagglutinin stalk–specific antibodies require FcγR interactions for protection against influenza virus in vivo - Nature Medicine
- ️Ravetch, Jeffrey V
- ️Sun Jan 12 2014
World Health Organization. Influenza (Seasonal) Fact sheet 211 http://www.who.int/mediacentre/factsheets/fs211/en/ (2009).
Ahmed, R., Oldstone, M.B. & Palese, P. Protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic. Nat. Immunol. 8, 1188–1193 (2007).
Martinez, O., Tsibane, T. & Basler, C.F. Neutralizing anti-influenza virus monoclonal antibodies: therapeutics and tools for discovery. Int. Rev. Immunol. 28, 69–92 (2009).
Couch, R.B. & Kasel, J.A. Immunity to influenza in man. Annu. Rev. Microbiol. 37, 529–549 (1983).
Wang, T.T. & Palese, P. Biochemistry. Catching a moving target. Science 333, 834–835 (2011).
Skehel, J.J. & Wiley, D.C. Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu. Rev. Biochem. 69, 531–569 (2000).
Knossow, M. et al. Mechanism of neutralization of influenza virus infectivity by antibodies. Virology 302, 294–298 (2002).
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).
Dreyfus, C. et al. Highly conserved protective epitopes on influenza B viruses. Science 337, 1343–1348 (2012).
Barbey-Martin, C. et al. An antibody that prevents the hemagglutinin low pH fusogenic transition. Virology 294, 70–74 (2002).
Ekiert, D.C. et al. Antibody recognition of a highly conserved influenza virus epitope. Science 324, 246–251 (2009).
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).
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).
Abboud, N. et al. A requirement for FcgγR in antibody-mediated bacterial toxin neutralization. J. Exp. Med. 207, 2395–2405 (2010).
Bournazos, S., Chow, S.K., Abboud, N., Casadevall, A. & Ravetch, J.V. Human IgG Fc domain engineering enhances anti-toxin neutralizing antibody activity. J. Clin. Invest. (in the press).
Schmitz, N. et al. Universal vaccine against influenza virus: linking TLR signaling to anti-viral protection. Eur. J. Immunol. 42, 863–869 (2012).
Huber, V.C., Lynch, J.M., Bucher, D.J., Le, J. & Metzger, D.W. Fc receptor–mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol. 166, 7381–7388 (2001).
Nimmerjahn, F. & Ravetch, J.V. Fcγ receptors as regulators of immune responses. Nat. Rev. Immunol. 8, 34–47 (2008).
Nimmerjahn, F. & Ravetch, J.V. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310, 1510–1512 (2005).
Tan, G.S. et al. A pan-H1 anti-hemagglutinin monoclonal antibody with potent broad-spectrum efficacy in vivo. J. Virol. 86, 6179–6188 (2012).
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).
Reale, M.A. et al. Characterization of monoclonal antibodies specific for sequential influenza A/PR/8/34 virus variants. J. Immunol. 137, 1352–1358 (1986).
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).
Smith, P., DiLillo, D.J., Bournazos, S., Li, F. & Ravetch, J.V. Mouse model recapitulating human Fcγ receptor structural and functional diversity. Proc. Natl. Acad. Sci. USA 109, 6181–6186 (2012).
Manicassamy, B. et al. Protection of mice against lethal challenge with 2009 H1N1 influenza A virus by 1918-like and classical swine H1N1 based vaccines. PLoS Pathog. 6, e1000745 (2010).
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).
Jegaskanda, S., Weinfurter, J.T., Friedrich, T.C. & Kent, S.J. Antibody-dependent cellular cytotoxicity (ADCC) is associated with control of pandemic H1N1 influenza virus infection of macaques. J. Virol. 87, 5512–5522 (2013).
Srivastava, V. et al. Identification of dominant ADCC epitopes on hemagglutinin antigen of pandemic H1N1 influenza virus. J. Virol. 87, 5831–5840 (2013).
Alter, G., Malenfant, J.M. & Altfeld, M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294, 15–22 (2004).
Nimmerjahn, F. & Ravetch, J.V. Analyzing antibody–Fc-receptor interactions. Methods Mol. Biol. 415, 151–162 (2008).
El Bakkouri, K. et al. Universal vaccine based on ectodomain of matrix protein 2 of influenza A: Fc receptors and alveolar macrophages mediate protection. J. Immunol. 186, 1022–1031 (2011).
Jegerlehner, A., Schmitz, N., Storni, T. & Bachmann, M.F. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 172, 5598–5605 (2004).
Tedder, T.F., Baras, A. & Xiu, Y. Fcγ receptor–dependent effector mechanisms regulate CD19 and CD20 antibody immunotherapies for B lymphocyte malignancies and autoimmunity. Springer Semin. Immunopathol. 28, 351–364 (2006).
Nordstrom, J.L. et al. Anti-tumor activity and toxicokinetics analysis of MGAH22, an anti-HER2 monoclonal antibody with enhanced Fcγ receptor binding properties. Breast Cancer Res. 13, R123 (2011).
Clynes, R.A., Towers, T.L., Presta, L.G. & Ravetch, J.V. Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6, 443–446 (2000).
Yang, X. et al. Cetuximab-mediated tumor regression depends on innate and adaptive immune responses. Mol. Ther. 21, 91–100 (2013).
Belser, J.A., Katz, J.M. & Tumpey, T.M. The ferret as a model organism to study influenza A virus infection. Dis. Model. Mech. 4, 575–579 (2011).
Nimmerjahn, F. & Ravetch, J.V. Antibodies, Fc receptors and cancer. Curr. Opin. Immunol. 19, 239–245 (2007).
Nimmerjahn, F. & Ravetch, J.V. FcγRs in health and disease. Curr. Top. Microbiol. Immunol. 350, 105–125 (2011).
Barkas, T. & Watson, C.M. Induction of an Fc conformational change by binding of antigen: the generation of protein A–reactive sites in chicken immunoglobulin. Immunology 36, 557–561 (1979).
Kilàr, F. & Zavodszky, P. Non-covalent interactions between Fab and Fc regions in immunoglobulin G molecules. Hydrogen-deuterium exchange studies. Eur. J. Biochem. 162, 57–61 (1987).
Torres, M., Fernandez-Fuentes, N., Fiser, A. & Casadevall, A. The immunoglobulin heavy chain constant region affects kinetic and thermodynamic parameters of antibody variable region interactions with antigen. J. Biol. Chem. 282, 13917–13927 (2007).
Oda, M., Kozono, H., Morii, H. & Azuma, T. Evidence of allosteric conformational changes in the antibody constant region upon antigen binding. Int. Immunol. 15, 417–426 (2003).
Schlessinger, J., Steinberg, I.Z., Givol, D., Hochman, J. & Pecht, I. Antigen-induced conformational changes in antibodies and their Fab fragments studied by circular polarization of fluorescence. Proc. Natl. Acad. Sci. USA 72, 2775–2779 (1975).
Tong, H. et al. Peptide-conjugation induced conformational changes in human IgG1 observed by optimized negative-staining and individual-particle electron tomography. Sci. Rep. 3, 1089 (2013).
Takai, T., Li, M., Sylvestre, D., Clynes, R. & Ravetch, J.V. FcR γ chain deletion results in pleiotrophic effector cell defects. Cell 76, 519–529 (1994).
Takai, T., Ono, M., Hikida, M., Ohmori, H. & Ravetch, J.V. Augmented humoral and anaphylactic responses in FcγRII-deficient mice. Nature 379, 346–349 (1996).
Ioan-Facsinay, A. et al. FcγRI (CD64) contributes substantially to severity of arthritis, hypersensitivity responses, and protection from bacterial infection. Immunity 16, 391–402 (2002).
Hazenbos, W.L. et al. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc γ RIII (CD16) deficient mice. Immunity 5, 181–188 (1996).
Nimmerjahn, F. et al. FcγRIV deletion reveals its central role for IgG2a and IgG2b activity in vivo. Proc. Natl. Acad. Sci. USA 107, 19396–19401 (2010).
Li, F. & Ravetch, J.V. Inhibitory Fcγ receptor engagement drives adjuvant and anti-tumor activities of agonistic CD40 antibodies. Science 333, 1030–1034 (2011).
Nimmerjahn, F., Bruhns, P., Horiuchi, K. & Ravetch, J.V. FcγRIV: a novel FcR with distinct IgG subclass specificity. Immunity 23, 41–51 (2005).
Wang, T.T. et al. Broadly protective monoclonal antibodies against H3 influenza viruses following sequential immunization with different hemagglutinins. PLoS Pathog. 6, e1000796 (2010).