Mosaic nanoparticle display of diverse influenza virus hemagglutinins elicits broad B cell responses
The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hy...
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| Published in | Nature immunology Vol. 20; no. 3; pp. 362 - 372 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.03.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD–np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD–np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge.
Antigenic variation of influenza A viruses necessitates the annual reformulation of vaccines. Kanekiyo et al. develop a mosaic nanoparticle vaccine against influenza virus that is able to elicit neutralizing antibodies that span nearly 100 years of variation of influenza A virus. |
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| AbstractList | The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD–np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD–np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge.
Antigenic variation of influenza A viruses necessitates the annual reformulation of vaccines. Kanekiyo et al. develop a mosaic nanoparticle vaccine against influenza virus that is able to elicit neutralizing antibodies that span nearly 100 years of variation of influenza A virus. The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD-np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD-np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge. The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD–np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD–np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge.Antigenic variation of influenza A viruses necessitates the annual reformulation of vaccines. Kanekiyo et al. develop a mosaic nanoparticle vaccine against influenza virus that is able to elicit neutralizing antibodies that span nearly 100 years of variation of influenza A virus. The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD-np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD-np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge.The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here we designed a vaccine using the hypervariable receptor-binding domain (RBD) of viral hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 influenza viruses spanning over 90 years. Co-display of RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD-np elicited broader antibody responses than those induced by an admixture of nanoparticles encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD-np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge. The current influenza vaccine has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine efficacy. This necessitates new approaches that provide broader protection against influenza. Here, we design a vaccine utilizing the hypervariable receptor-binding domain (RBD) of virus hemagglutinin displayed on a nanoparticle (np) able to elicit antibody responses that neutralize H1N1 viruses spanning over 90 years. Co-displaying RBDs from multiple strains across time, so that the adjacent RBDs are heterotypic, provides an avidity advantage to cross-reactive B cells. Immunization with the mosaic RBD-np elicited broader antibody responses than those induced by an admixture of nps encompassing the same set of RBDs as separate homotypic arrays. Furthermore, we identified a broadly neutralizing monoclonal antibody in a mouse immunized with mosaic RBD-np. The mosaic antigen array signifies a unique approach that subverts monotypic immunodominance and allows otherwise subdominant cross-reactive B cell responses to emerge. |
| Audience | Academic |
| Author | Yang, Eun Sung Boyoglu-Barnum, Seyhan Kong, Wing-Pui Prabhakaran, Madhu S. Kwong, Peter D. Creanga, Adrian Koup, Richard A. Graham, Barney S. McDermott, Adrian B. Gillespie, Rebecca A. Georgiev, Ivelin S. Kanekiyo, Masaru Joyce, M. Gordon Yassine, Hadi M. Wheatley, Adam K. Ledgerwood, Julie E. Tsybovsky, Yaroslav Mascola, John R. Harris, Audray K. Andersen, Hanne Baxa, Ulrich Andrews, Sarah F. Leung, Kwanyee Ambrozak, David R. Gallagher, John R. Zephir, Kathryn L. Fisher, Brian E. |
| AuthorAffiliation | 2 Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, United States 5 Present address: Henry M. Jackson Foundation for the Advancement of Military Medicine, U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD 20910, United States 10 These authors contributed equally to this work 4 Bioqual, Inc., Rockville, MD 20852, United States 9 Present address: Cryo-EM facility, Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD 21701, United States 1 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, United States 8 Present address: Vanderbilt Vaccine Center and Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, United States 3 Electron Microscope Laboratory, Cancer Research Technology P |
| AuthorAffiliation_xml | – name: 8 Present address: Vanderbilt Vaccine Center and Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN 37232, United States – name: 3 Electron Microscope Laboratory, Cancer Research Technology Program, Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research, Frederick, MD 21702, United States – name: 4 Bioqual, Inc., Rockville, MD 20852, United States – name: 6 Present address: Biomedical Research Center, Qatar University, Doha, Qatar – name: 5 Present address: Henry M. Jackson Foundation for the Advancement of Military Medicine, U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD 20910, United States – name: 10 These authors contributed equally to this work – name: 7 Present address: Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne, Victoria, Australia – name: 1 Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, United States – name: 2 Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892, United States – name: 9 Present address: Cryo-EM facility, Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick, MD 21701, United States |
| Author_xml | – sequence: 1 givenname: Masaru orcidid: 0000-0001-5767-1532 surname: Kanekiyo fullname: Kanekiyo, Masaru email: kanekiyom@nih.gov organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 2 givenname: M. Gordon orcidid: 0000-0002-6808-7232 surname: Joyce fullname: Joyce, M. Gordon organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Henry M. Jackson Foundation for the Advancement of Military Medicine, US Military HIV Research Program, Walter Reed Army Institute of Research – sequence: 3 givenname: Rebecca A. surname: Gillespie fullname: Gillespie, Rebecca A. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 4 givenname: John R. orcidid: 0000-0002-1954-8872 surname: Gallagher fullname: Gallagher, John R. organization: Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 5 givenname: Sarah F. surname: Andrews fullname: Andrews, Sarah F. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 6 givenname: Hadi M. surname: Yassine fullname: Yassine, Hadi M. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Biomedical Research Center, Qatar University – sequence: 7 givenname: Adam K. orcidid: 0000-0002-5593-9387 surname: Wheatley fullname: Wheatley, Adam K. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Microbiology and Immunology, Peter Doherty Institute for Infection and Immunity, University of Melbourne – sequence: 8 givenname: Brian E. surname: Fisher fullname: Fisher, Brian E. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 9 givenname: David R. surname: Ambrozak fullname: Ambrozak, David R. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 10 givenname: Adrian surname: Creanga fullname: Creanga, Adrian organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 11 givenname: Kwanyee surname: Leung fullname: Leung, Kwanyee organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 12 givenname: Eun Sung surname: Yang fullname: Yang, Eun Sung organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 13 givenname: Seyhan surname: Boyoglu-Barnum fullname: Boyoglu-Barnum, Seyhan organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 14 givenname: Ivelin S. surname: Georgiev fullname: Georgiev, Ivelin S. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Vanderbilt Vaccine Center and Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center – sequence: 15 givenname: Yaroslav surname: Tsybovsky fullname: Tsybovsky, Yaroslav organization: Electron Microscope Laboratory, Cancer Research Technology Program, Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research – sequence: 16 givenname: Madhu S. surname: Prabhakaran fullname: Prabhakaran, Madhu S. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 17 givenname: Hanne orcidid: 0000-0003-1103-9608 surname: Andersen fullname: Andersen, Hanne organization: Bioqual, Inc – sequence: 18 givenname: Wing-Pui surname: Kong fullname: Kong, Wing-Pui organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 19 givenname: Ulrich surname: Baxa fullname: Baxa, Ulrich organization: Electron Microscope Laboratory, Cancer Research Technology Program, Leidos Biomedical Research, Inc., Frederick National Laboratory for Cancer Research, Cryo-EM facility, Cancer Research Technology Program, Frederick National Laboratory for Cancer Research – sequence: 20 givenname: Kathryn L. surname: Zephir fullname: Zephir, Kathryn L. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 21 givenname: Julie E. surname: Ledgerwood fullname: Ledgerwood, Julie E. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 22 givenname: Richard A. surname: Koup fullname: Koup, Richard A. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 23 givenname: Peter D. surname: Kwong fullname: Kwong, Peter D. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 24 givenname: Audray K. orcidid: 0000-0002-8875-1874 surname: Harris fullname: Harris, Audray K. organization: Laboratory of Infectious Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 25 givenname: Adrian B. surname: McDermott fullname: McDermott, Adrian B. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 26 givenname: John R. surname: Mascola fullname: Mascola, John R. organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health – sequence: 27 givenname: Barney S. orcidid: 0000-0001-8112-0853 surname: Graham fullname: Graham, Barney S. email: bgraham@nih.gov organization: Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30742080$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 M.K. and B.S.G. conceptualized and devised studies. M.K. designed immunogens. M.K., R.A.G., H.M.Y. and S.B.B. performed animal studies; M.G.J. crystallized and solved Fab structure; J.R.G. and A.K.H. determined cryo-EM structure; S.F.A., A.K.W., B.E.F., D.R.A. and M.S.P. performed FACS and single-cell PCR; M.K., R.A.G., S.F.A. and H.M.Y. produced and characterized proteins; A.C. made viruses by reverse genetics; R.A.G., H.M.Y., K.L., E.S.Y. and W.-P.K. performed virus neutralization assays; I.S.G. performed mathematical simulations; Y.T. and U.B. performed EM experiments; H.A. performed challenge studies; K.L.Z. and J.E.L. conducted clinical trials and provided human samples; M.K., M.G.J., R.A.G., J.R.G., S.F.A., H.M.Y., A.K.W., A.K.H., R.A.K., P.D.K., A.B.M., J.R.M. and B.S.G. analyzed data; M.K. and B.S.G. wrote paper with input from all authors. Author contributions |
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| Snippet | The present vaccine against influenza virus has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes... The current influenza vaccine has the inevitable risk of antigenic discordance between the vaccine and the circulating strains, which diminishes vaccine... |
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| Title | Mosaic nanoparticle display of diverse influenza virus hemagglutinins elicits broad B cell responses |
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