H7N9 influenza virus neutralizing antibodies that possess few somatic mutations.

Avian H7N9 influenza viruses are group 2 influenza A viruses that have been identified as the etiologic agent for a current major outbreak that began in China in 2013 and may pose a pandemic threat. Here, we examined the human H7-reactive antibody response in 75 recipients of a monovalent inactivated A/Shanghai/02/2013 H7N9 vaccine. After 2 doses of vaccine, the majority of donors had memory B cells that secreted IgGs specific for H7 HA, with dominant responses against single HA subtypes, although frequencies of H7-reactive B cells ranged widely between donors. We isolated 12 naturally occurring mAbs with low half-maximal effective concentrations for binding, 5 of which possessed neutralizing and HA-inhibiting activities. The 5 neutralizing mAbs exhibited narrow breadth of reactivity with influenza H7 strains. Epitope-mapping studies using neutralization escape mutant analysis, deuterium exchange mass spectrometry, and x-ray crystallography revealed that these neutralizing mAbs bind near the receptor-binding pocket on HA. All 5 neutralizing mAbs possessed low numbers of somatic mutations, suggesting the clones arose from naive B cells. The most potent mAb, H7.167, was tested as a prophylactic treatment in a mouse intranasal virus challenge study, and systemic administration of the mAb markedly reduced viral lung titers.

[1]  Andrea A. Berry,et al.  Effect of Varying Doses of a Monovalent H7N9 Influenza Vaccine With and Without AS03 and MF59 Adjuvants on Immune Response: A Randomized Clinical Trial. , 2015, JAMA.

[2]  Francisco A. Chaves,et al.  Seasonal Influenza Can Poise Hosts for CD4 T-Cell Immunity to H7N9 Avian Influenza. , 2015, The Journal of infectious diseases.

[3]  Jianmin Wang,et al.  Human monoclonal antibodies targeting the haemagglutinin glycoprotein can neutralize H7N9 influenza virus , 2015, Nature Communications.

[4]  J. Wrammert,et al.  Preexisting human antibodies neutralize recently emerged H7N9 influenza strains. , 2015, The Journal of clinical investigation.

[5]  Wei Wang,et al.  Antibodies to Antigenic Site A of Influenza H7 Hemagglutinin Provide Protection against H7N9 Challenge , 2015, PloS one.

[6]  P. Dormitzer,et al.  A Cell Culture–Derived MF59-Adjuvanted Pandemic A/H7N9 Vaccine Is Immunogenic in Adults , 2014, Science Translational Medicine.

[7]  Jens Meiler,et al.  Human antibodies that neutralize respiratory droplet transmissible H5N1 influenza viruses. , 2013, The Journal of clinical investigation.

[8]  Zexian Liu,et al.  Towards a better understanding of the novel avian-origin H7N9 influenza A virus in China , 2013, Scientific Reports.

[9]  Guohua Deng,et al.  H7N9 Influenza Viruses Are Transmissible in Ferrets by Respiratory Droplet , 2013, Science.

[10]  Y. Guan,et al.  Infectivity, Transmission, and Pathology of Human-Isolated H7N9 Influenza Virus in Ferrets and Pigs , 2013, Science.

[11]  P. Collins,et al.  Receptor binding by an H7N9 influenza virus from humans , 2013, Nature.

[12]  Yu Wang,et al.  Origin and diversity of novel avian influenza A H7N9 viruses causing human infection: phylogenetic, structural, and coalescent analyses , 2013, The Lancet.

[13]  Jie Dong,et al.  Human Infection with a Novel Avian-Origin Influenza A (H7N9) Virus. , 2018 .

[14]  G. Neumann,et al.  Genetic analysis of novel avian A(H7N9) influenza viruses isolated from patients in China, February to April 2013. , 2013, Euro surveillance : bulletin Europeen sur les maladies transmissibles = European communicable disease bulletin.

[15]  Virginia Pascual,et al.  Induction of ICOS+CXCR3+CXCR5+ TH Cells Correlates with Antibody Responses to Influenza Vaccination , 2013, Science Translational Medicine.

[16]  James E. Crowe,et al.  A recurring motif for antibody recognition of the receptor-binding site of influenza hemagglutinin , 2013, Nature Structural &Molecular Biology.

[17]  James E. Crowe,et al.  Influenza Human Monoclonal Antibody 1F1 Interacts with Three Major Antigenic Sites and Residues Mediating Human Receptor Specificity in H1N1 Viruses , 2012, PLoS pathogens.

[18]  Virgil L. Woods,et al.  The prohormone proenkephalin possesses differential conformational features of subdomains revealed by rapid H‐D exchange mass spectrometry , 2012, Protein science : a publication of the Protein Society.

[19]  J. Crowe,et al.  Persistence of Circulating Memory B Cell Clones with Potential for Dengue Virus Disease Enhancement for Decades following Infection , 2011, Journal of Virology.

[20]  James E Crowe,et al.  Epitope-Specific Human Influenza Antibody Repertoires Diversify by B Cell Intraclonal Sequence Divergence and Interclonal Convergence , 2011, The Journal of Immunology.

[21]  J. Crowe,et al.  A Broadly Neutralizing Human Monoclonal Antibody That Recognizes a Conserved, Novel Epitope on the Globular Head of the Influenza H1N1 Virus Hemagglutinin , 2011, Journal of Virology.

[22]  J. Skehel,et al.  A Neutralizing Antibody Selected from Plasma Cells That Binds to Group 1 and Group 2 Influenza A Hemagglutinins , 2011, Science.

[23]  Virgil L. Woods,et al.  Mechanism of Intracellular cAMP Sensor Epac2 Activation , 2011, The Journal of Biological Chemistry.

[24]  P. Emsley,et al.  Features and development of Coot , 2010, Acta crystallographica. Section D, Biological crystallography.

[25]  Randy J. Read,et al.  Acta Crystallographica Section D Biological , 2003 .

[26]  J. Crowe,et al.  Naturally Occurring Human Monoclonal Antibodies Neutralize both 1918 and 2009 Pandemic Influenza A (H1N1) Viruses , 2009, Journal of Virology.

[27]  Vincent B. Chen,et al.  Correspondence e-mail: , 2000 .

[28]  Virgil L. Woods,et al.  Structural insights into glucan phosphatase dynamics using amide hydrogen-deuterium exchange mass spectrometry. , 2009, Biochemistry.

[29]  Steven J. M. Jones,et al.  Circos: an information aesthetic for comparative genomics. , 2009, Genome research.

[30]  Gira Bhabha,et al.  Antibody Recognition of a Highly Conserved Influenza Virus Epitope , 2009, Science.

[31]  Boguslaw Stec,et al.  Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses , 2009, Nature Structural &Molecular Biology.

[32]  John Steel,et al.  Live Attenuated Influenza Viruses Containing NS1 Truncations as Vaccine Candidates against H5N1 Highly Pathogenic Avian Influenza , 2008, Journal of Virology.

[33]  Andrew C. R. Martin,et al.  Analysis and improvements to Kabat and structurally correct numbering of antibody variable domains. , 2008, Molecular immunology.

[34]  Marie-Paule Lefranc,et al.  IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis , 2008, Nucleic Acids Res..

[35]  T. Tatusova,et al.  The Influenza Virus Resource at the National Center for Biotechnology Information , 2007, Journal of Virology.

[36]  Randy J. Read,et al.  Phaser crystallographic software , 2007, Journal of applied crystallography.

[37]  A. García-Sastre,et al.  Hemagglutinin (HA) Proteins from H1 and H3 Serotypes of Influenza A Viruses Require Different Antigen Designs for the Induction of Optimal Protective Antibody Responses as Studied by Codon-Optimized HA DNA Vaccines , 2006, Journal of Virology.

[38]  Ian A. Wilson,et al.  Structure and Receptor Specificity of the Hemagglutinin from an H5N1 Influenza Virus , 2006, Science.

[39]  Mark Wolff,et al.  Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. , 2006, The New England journal of medicine.

[40]  Virgil L. Woods,et al.  Mapping intersubunit interactions of the regulatory subunit (RIalpha) in the type I holoenzyme of protein kinase A by amide hydrogen/deuterium exchange mass spectrometry (DXMS). , 2004, Journal of molecular biology.

[41]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[42]  Ya Ha,et al.  H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes , 2002, The EMBO journal.

[43]  Y. Durocher,et al.  High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells. , 2002, Nucleic acids research.

[44]  J. Thornton,et al.  Satisfying hydrogen bonding potential in proteins. , 1994, Journal of molecular biology.

[45]  Zhongqi Zhang,et al.  Determination of amide hydrogen exchange by mass spectrometry: A new tool for protein structure elucidation , 1993, Protein science : a publication of the Protein Society.

[46]  J. L. Smith,et al.  Structure of myohemerythrin in the azidomet state at 1.7/1.3 A resolution. , 1987, Journal of molecular biology.