A multifunctional human monoclonal neutralizing antibody that targets a unique conserved epitope on influenza HA

Bangaru, Sandhya; Zhang, Heng; Gilchuk, Iuliia M.; Voss, Thomas G.; Irving, Ryan P.; Gilchuk, Pavlo; Matta, Pranathi; Zhu, Xueyong; Lang, Shanshan; Nieusma, Travis; Richt, Juergen A.; Albrecht, Randy A.; Vanderven, Hillary A.; Bombardi, Robin; Kent, Stephen J.; Ward, Andrew B.; Wilson, Ian A.; Crowe, James E.

doi:10.1038/s41467-018-04704-9

Title: A multifunctional human monoclonal neutralizing antibody that targets a unique conserved epitope on influenza HA

Journal Article · Tue Jul 10 00:00:00 EDT 2018 · Nature Communications

DOI:https://doi.org/10.1038/s41467-018-04704-9· OSTI ID:1498306

Bangaru, Sandhya; Zhang, Heng; Gilchuk, Iuliia M.; Voss, Thomas G.; Irving, Ryan P.; Gilchuk, Pavlo; Matta, Pranathi; Zhu, Xueyong; Lang, Shanshan; Nieusma, Travis; Richt, Juergen A.; Albrecht, Randy A.; Vanderven, Hillary A.; Bombardi, Robin; Kent, Stephen J.; Ward, Andrew B.;

;

Cite

Export

Save

Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1498306

Journal Information:: Nature Communications, Vol. 9, Issue 1; ISSN 2041-1723

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: ENGLISH

References (63)

Safety and Immunogenicity of a Subvirion Monovalent Unadjuvanted Inactivated Influenza A(H3N2) Variant Vaccine in Healthy Persons ≥18 Years Old Keitel, Wendy A.; Jackson, Lisa A.; Edupuganti, Srilatha Journal of Infectious Diseases, Vol. 212, Issue 4 https://doi.org/10.1093/infdis/jiv056	journal	February 2015
Antigenically intact hemagglutinin in circulating avian and swine influenza viruses and potential for H3N2 pandemic Tharakaraman, Kannan; Raman, Rahul; Stebbins, Nathan W. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep01822	journal	May 2013
Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation Wiley, D. C.; Wilson, I. A.; Skehel, J. J. Nature, Vol. 289, Issue 5796 https://doi.org/10.1038/289373a0	journal	January 1981
Population-Based Surveillance for Hospitalizations Associated With Respiratory Syncytial Virus, Influenza Virus, and Parainfluenza Viruses Among Young Children Iwane, M. K.; Edwards, K. M.; Szilagyi, P. G. PEDIATRICS, Vol. 113, Issue 6 https://doi.org/10.1542/peds.113.6.1758	journal	June 2004
Cross-reactive and Vaccine-Induced Antibody to an Emerging Swine-Origin Variant of Influenza A Virus Subtype H3N2 (H3N2v) Skowronski, Danuta M.; Janjua, Naveed Z.; De Serres, Gaston The Journal of Infectious Diseases, Vol. 206, Issue 12 https://doi.org/10.1093/infdis/jis500	journal	October 2012
Dimeric FcγR Ectodomains as Probes of the Fc Receptor Function of Anti-Influenza Virus IgG Wines, Bruce D.; Vanderven, Hillary A.; Esparon, Sandra E. The Journal of Immunology, Vol. 197, Issue 4 https://doi.org/10.4049/jimmunol.1502551	journal	July 2016
Satisfying Hydrogen Bonding Potential in Proteins McDonald, Ian K.; Thornton, Janet M. Journal of Molecular Biology, Vol. 238, Issue 5 https://doi.org/10.1006/jmbi.1994.1334	journal	May 1994
Update: Influenza Activity — United States and Worldwide, May 24–September 5, 2015 Blanton, Lenee; Kniss, Krista; Smith, Sophie MMWR. Morbidity and Mortality Weekly Report, Vol. 64, Issue 36 https://doi.org/10.15585/mmwr.mm6436a4	journal	September 2015
Identification of Hemagglutinin Residues Responsible for H3N2 Antigenic Drift during the 2014–2015 Influenza Season Chambers, Benjamin S.; Parkhouse, Kaela; Ross, Ted M. Cell Reports, Vol. 12, Issue 1 https://doi.org/10.1016/j.celrep.2015.06.005	journal	July 2015
A common solution to group 2 influenza virus neutralization Friesen, R. H. E.; Lee, P. S.; Stoop, E. J. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1319058110	journal	December 2013
Generation and Protective Ability of Influenza Virus–Specific Antibody-Dependent Cellular Cytotoxicity in Humans Elicited by Vaccination, Natural Infection, and Experimental Challenge Jegaskanda, Sinthujan; Luke, Catherine; Hickman, Heather D. Journal of Infectious Diseases, Vol. 214, Issue 6 https://doi.org/10.1093/infdis/jiw262	journal	June 2016
Cross-Protective Potential of a Novel Monoclonal Antibody Directed against Antigenic Site B of the Hemagglutinin of Influenza A Viruses Yoshida, Reiko; Igarashi, Manabu; Ozaki, Hiroichi PLoS Pathogens, Vol. 5, Issue 3 https://doi.org/10.1371/journal.ppat.1000350	journal	March 2009
DoG Picker and TiltPicker: Software tools to facilitate particle selection in single particle electron microscopy Voss, N. R.; Yoshioka, C. K.; Radermacher, M. Journal of Structural Biology, Vol. 166, Issue 2 https://doi.org/10.1016/j.jsb.2009.01.004	journal	May 2009
Influenza Vaccination Among the Elderly in the United States—Reply Simonsen, Lone; Reichert, Thomas A.; Viboud, Cecile Archives of Internal Medicine, Vol. 165, Issue 17 https://doi.org/10.1001/archinte.165.17.2039	journal	September 2005
Receptor Binding and Membrane Fusion in Virus Entry: The Influenza Hemagglutinin Skehel, John J.; Wiley, Don C. Annual Review of Biochemistry, Vol. 69, Issue 1 https://doi.org/10.1146/annurev.biochem.69.1.531	journal	June 2000
Glycosylation of the hemagglutinin modulates the sensitivity of H3N2 influenza viruses to innate proteins in airway secretions and virulence in mice Tate, Michelle D.; Job, Emma R.; Brooks, Andrew G. Virology, Vol. 413, Issue 1 https://doi.org/10.1016/j.virol.2011.01.036	journal	April 2011
Mapping of Antigenic Changes in the Haemagglutinin of Hong Kong Influenza (H3N2) Strains using a Large Panel of Monoclonal Antibodies Underwood, P. A. Journal of General Virology, Vol. 62, Issue 1 https://doi.org/10.1099/0022-1317-62-1-153	journal	September 1982
Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets Pearce, M. B.; Jayaraman, A.; Pappas, C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 10 https://doi.org/10.1073/pnas.1119945109	journal	February 2012
Automated molecular microscopy: The new Leginon system Suloway, Christian; Pulokas, James; Fellmann, Denis Journal of Structural Biology, Vol. 151, Issue 1 https://doi.org/10.1016/j.jsb.2005.03.010	journal	July 2005
The contents of the syringe Salzberg, Steven Nature, Vol. 454, Issue 7201 https://doi.org/10.1038/454160a	journal	July 2008
Evidence for N-Glycan Shielding of Antigenic Sites during Evolution of Human Influenza A Virus Hemagglutinin Kobayashi, Y.; Suzuki, Y. Journal of Virology, Vol. 86, Issue 7 https://doi.org/10.1128/JVI.06147-11	journal	January 2012
Structural evidence for recognition of a single epitope by two distinct antibodies Fleury, Damien; Daniels, Rod S.; Skehel, John J. Proteins: Structure, Function, and Genetics, Vol. 40, Issue 4 https://doi.org/10.1002/1097-0134(20000901)40:4<572::AID-PROT30>3.0.CO;2-N	journal	January 2000
The Influenza Virus Resource at the National Center for Biotechnology Information Bao, Y.; Bolotov, P.; Dernovoy, D. Journal of Virology, Vol. 82, Issue 2 https://doi.org/10.1128/JVI.02005-07	journal	October 2007
Mechanisms of Hemagglutinin Targeted Influenza Virus Neutralization Brandenburg, Boerries; Koudstaal, Wouter; Goudsmit, Jaap PLoS ONE, Vol. 8, Issue 12 https://doi.org/10.1371/journal.pone.0080034	journal	December 2013
Cross-Reactive Influenza-Specific Antibody-Dependent Cellular Cytotoxicity Antibodies in the Absence of Neutralizing Antibodies Jegaskanda, Sinthujan; Job, Emma R.; Kramski, Marit The Journal of Immunology, Vol. 190, Issue 4 https://doi.org/10.4049/jimmunol.1201574	journal	January 2013
Analytical molecular surface calculation Connolly, M. L. Journal of Applied Crystallography, Vol. 16, Issue 5 https://doi.org/10.1107/S0021889883010985	journal	October 1983
Epitope specificity plays a critical role in regulating antibody-dependent cell-mediated cytotoxicity against influenza A virus He, Wenqian; Tan, Gene S.; Mullarkey, Caitlin E. Proceedings of the National Academy of Sciences, Vol. 113, Issue 42 https://doi.org/10.1073/pnas.1609316113	journal	October 2016
Broadly Neutralizing Hemagglutinin Stalk-Specific Antibodies Induce Potent Phagocytosis of Immune Complexes by Neutrophils in an Fc-Dependent Manner Mullarkey, Caitlin E.; Bailey, Mark J.; Golubeva, Diana A. mBio, Vol. 7, Issue 5 https://doi.org/10.1128/mBio.01624-16	journal	October 2016
Antibody Recognition of a Highly Conserved Influenza Virus Epitope Ekiert, D. C.; Bhabha, G.; Elsliger, M. -A. Science, Vol. 324, Issue 5924 https://doi.org/10.1126/science.1171491	journal	April 2009
Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses Sui, Jianhua; Hwang, William C.; Perez, Sandra Nature Structural & Molecular Biology, Vol. 16, Issue 3 https://doi.org/10.1038/nsmb.1566	journal	February 2009
A Highly Conserved Neutralizing Epitope on Group 2 Influenza A Viruses Ekiert, D. C.; Friesen, R. H. E.; Bhabha, G. Science, Vol. 333, Issue 6044 https://doi.org/10.1126/science.1204839	journal	July 2011
Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid Weis, W.; Brown, J. H.; Cusack, S. Nature, Vol. 333, Issue 6172 https://doi.org/10.1038/333426a0	journal	June 1988
Human Infections with Novel Reassortant Influenza A(H3N2)v Viruses, United States, 2011 Lindstrom, Stephen; Garten, Rebecca; Balish, Amanda Emerging Infectious Diseases, Vol. 18, Issue 5 https://doi.org/10.3201/eid1805.111922	journal	May 2012
Broadly neutralizing hemagglutinin stalk–specific antibodies require FcγR interactions for protection against influenza virus in vivo DiLillo, David J.; Tan, Gene S.; Palese, Peter Nature Medicine, Vol. 20, Issue 2 https://doi.org/10.1038/nm.3443	journal	January 2014
Heterosubtypic antibody recognition of the influenza virus hemagglutinin receptor binding site enhanced by avidity Lee, P. S.; Yoshida, R.; Ekiert, D. C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 42 https://doi.org/10.1073/pnas.1212371109	journal	October 2012
Recognition of influenza H3N2 variant virus by human neutralizing antibodies Bangaru, Sandhya; Nieusma, Travis; Kose, Nurgun JCI Insight, Vol. 1, Issue 10 https://doi.org/10.1172/jci.insight.86673	journal	July 2016
Fc Receptor-Mediated Phagocytosis Makes a Significant Contribution to Clearance of Influenza Virus Infections Huber, Victor C.; Lynch, Joyce M.; Bucher, Doris J. The Journal of Immunology, Vol. 166, Issue 12 https://doi.org/10.4049/jimmunol.166.12.7381	journal	June 2001
Crystals of a gragment of influenza haemagglutinin in the low pH induced conformation Bullough, P. A.; Hughson, F. M.; Treharne, A. C. Journal of Molecular Biology, Vol. 236, Issue 4 https://doi.org/10.1016/0022-2836(94)90027-2	journal	March 1994
Hemagglutinin Stalk- and Neuraminidase-Specific Monoclonal Antibodies Protect against Lethal H10N8 Influenza Virus Infection in Mice Wohlbold, Teddy John; Chromikova, Veronika; Tan, Gene S. Journal of Virology, Vol. 90, Issue 2 https://doi.org/10.1128/JVI.02275-15	journal	October 2015
EMAN2: An extensible image processing suite for electron microscopy Tang, Guang; Peng, Liwei; Baldwin, Philip R. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.009	journal	January 2007
MolProbity : all-atom structure validation for macromolecular crystallography Chen, Vincent B.; Arendall, W. Bryan; Headd, Jeffrey J. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 1 https://doi.org/10.1107/S0907444909042073	journal	December 2009
Human Infections With Influenza A(H3N2) Variant Virus in the United States, 2011-2012 Epperson, S.; Jhung, M.; Richards, S. Clinical Infectious Diseases, Vol. 57, Issue suppl 1 https://doi.org/10.1093/cid/cit272	journal	June 2013
Structure of myohemerythrin in the azidomet state at resolution Sheriff, Steven; Hendrickson, Wayne A.; Smith, Janet L. Journal of Molecular Biology, Vol. 197, Issue 2 https://doi.org/10.1016/0022-2836(87)90124-0	journal	September 1987
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
The Global Circulation of Seasonal Influenza A (H3N2) Viruses Russell, C. A.; Jones, T. C.; Barr, I. G. Science, Vol. 320, Issue 5874 https://doi.org/10.1126/science.1154137	journal	April 2008
A Unique and Conserved Neutralization Epitope in H5N1 Influenza Viruses Identified by an Antibody against the A/Goose/Guangdong/1/96 Hemagglutinin Zhu, Xueyong; Guo, Yong-Hui; Jiang, Tao Journal of Virology, Vol. 87, Issue 23 https://doi.org/10.1128/JVI.01577-13	journal	September 2013
Mapping the Antigenic and Genetic Evolution of Influenza Virus Smith, D. J. Science, Vol. 305, Issue 5682 https://doi.org/10.1126/science.1097211	journal	July 2004
Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution Wilson, I. A.; Skehel, J. J.; Wiley, D. C. Nature, Vol. 289, Issue 5796 https://doi.org/10.1038/289366a0	journal	January 1981
Analysis and improvements to Kabat and structurally correct numbering of antibody variable domains Abhinandan, K. R.; Martin, Andrew C. R. Molecular Immunology, Vol. 45, Issue 14 https://doi.org/10.1016/j.molimm.2008.05.022	journal	August 2008
Outbreak of Variant Influenza A(H3N2) Virus in the United States Jhung, M. A.; Epperson, S.; Biggerstaff, M. Clinical Infectious Diseases, Vol. 57, Issue 12 https://doi.org/10.1093/cid/cit649	journal	September 2013
The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype) Caton, Andrew J.; Brownlee, George G.; Yewdell, Jonathan W. Cell, Vol. 31, Issue 2 https://doi.org/10.1016/0092-8674(82)90135-0	journal	December 1982
Influenza- and respiratory syncytial virus-associated mortality and hospitalisations Jansen, A. G. S. C.; Sanders, E. A. M.; Hoes, A. W. European Respiratory Journal, Vol. 30, Issue 6 https://doi.org/10.1183/09031936.00034407	journal	August 2007
A Neutralizing Antibody Selected from Plasma Cells That Binds to Group 1 and Group 2 Influenza A Hemagglutinins Corti, D.; Voss, J.; Gamblin, S. J. Science, Vol. 333, Issue 6044 https://doi.org/10.1126/science.1205669	journal	July 2011
Antibody-Dependent Cellular Cytotoxicity Is Associated with Control of Pandemic H1N1 Influenza Virus Infection of Macaques Jegaskanda, S.; Weinfurter, J. T.; Friedrich, T. C. Journal of Virology, Vol. 87, Issue 10 https://doi.org/10.1128/JVI.03030-12	journal	March 2013
Structure and Receptor Specificity of the Hemagglutinin from an H5N1 Influenza Virus Stevens, J.; Blixt, O.; Tumpey, T. M. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1124513	journal	March 2006
Highly Conserved Protective Epitopes on Influenza B Viruses Dreyfus, C.; Laursen, N. S.; Kwaks, T. Science, Vol. 337, Issue 6100 https://doi.org/10.1126/science.1222908	journal	August 2012
MUSCLE: multiple sequence alignment with high accuracy and high throughput Edgar, R. C. Nucleic Acids Research, Vol. 32, Issue 5, p. 1792-1797 https://doi.org/10.1093/nar/gkh340	journal	March 2004
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
EMAN: Semiautomated Software for High-Resolution Single-Particle Reconstructions Ludtke, Steven J.; Baldwin, Philip R.; Chiu, Wah Journal of Structural Biology, Vol. 128, Issue 1 https://doi.org/10.1006/jsbi.1999.4174	journal	December 1999
HA Antibody-Mediated FcγRIIIa Activity Is Both Dependent on FcR Engagement and Interactions between HA and Sialic Acids Cox, Freek; Kwaks, Ted; Brandenburg, Boerries Frontiers in Immunology, Vol. 7 https://doi.org/10.3389/fimmu.2016.00399	journal	September 2016
Receptor mimicry by antibody F045–092 facilitates universal binding to the H3 subtype of influenza virus Lee, Peter S.; Ohshima, Nobuko; Stanfield, Robyn L. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms4614	journal	April 2014
A broadly protective therapeutic antibody against influenza B virus with two mechanisms of action Chai, Ning; Swem, Lee R.; Park, Summer Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14234	journal	January 2017

Similar Records

A Unique and Conserved Neutralization Epitope in H5N1 Influenza Viruses Identified by an Antibody against the A/Goose/Guangdong/1/96 Hemagglutinin

Journal Article · Fri Aug 28 00:00:00 EDT 2015 · J. Virol. · OSTI ID:1498306

Zhu, Xueyong; Guo, Yong-Hui; Jiang, Tao; +10 more

A Potent Germline-like Human Monoclonal Antibody Targets a pH-Sensitive Epitope on H7N9 Influenza Hemagglutinin

Journal Article · Sun Oct 01 00:00:00 EDT 2017 · Cell Host & Microbe · OSTI ID:1498306

Yu, Fei; Song, He; Wu, Yanling; +22 more