Distinct germinal center selection at local sites shapes memory B cell response to viral escape
Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at t...
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| Published in | The Journal of experimental medicine Vol. 212; no. 10; pp. 1709 - 1723 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
The Rockefeller University Press
21.09.2015
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| Abstract | Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of VH mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines. |
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| AbstractList | Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of VH mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines. Local germinal center reactions that persist in the lung after influenza infection are required for the generation of cross-reactive memory B cells. Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of VH mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines. Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of VH mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines.Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of VH mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines. Local germinal center reactions that persist in the lung after influenza infection are required for the generation of cross-reactive memory B cells. Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events dictating the cross-reactive memory B cell responses remain to be fully defined. Here, we demonstrated that lung-resident memory compartments at the site of infection, rather than those in secondary lymphoid organs, harbor elevated frequencies of cross-reactive B cells that mediate neutralizing antibody responses to viral escape. The elevated cross-reactivity in the lung memory compartments was correlated with high numbers of V H mutations and was dependent on a developmental pathway involving persistent germinal center (GC) responses. The persistent GC responses were focused in the infected lungs in association with prolonged persistence of the viral antigens. Moreover, the persistent lung GCs supported the exaggerated B cell proliferation and clonal selection for cross-reactive repertoires, which served as the predominant sites for the generation of cross-reactive memory progenitors. Thus, we identified the distinct GC selection at local sites as a key cellular event for cross-reactive memory B cell response to viral escape, a finding with important implications for developing broadly protective influenza vaccines. |
| Author | Inoue, Takeshi Onodera, Taishi Takahashi, Yoshimasa Ato, Manabu Adachi, Yu Yamada, Yuki Tsuiji, Makoto Kobayashi, Kazuo Daio, Rina Kurosaki, Tomohiro |
| AuthorAffiliation | 1 Department of Immunology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan 4 Laboratory for Lymphocyte Differentiation, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa 230-0045, Japan 3 Laboratory of Lymphocyte Differentiation, WPI Immunology Frontier Research Center and Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan 2 Department of Microbiology, Hoshi University School of Pharmacy and Pharmaceutical Sciences, Shinagawa-ku, Tokyo 142-8501, Japan |
| AuthorAffiliation_xml | – name: 3 Laboratory of Lymphocyte Differentiation, WPI Immunology Frontier Research Center and Graduate School of Frontier Biosciences, Osaka University, Suita, Osaka 565-0871, Japan – name: 2 Department of Microbiology, Hoshi University School of Pharmacy and Pharmaceutical Sciences, Shinagawa-ku, Tokyo 142-8501, Japan – name: 1 Department of Immunology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo 162-8640, Japan – name: 4 Laboratory for Lymphocyte Differentiation, RIKEN Center for Integrative Medical Sciences, Yokohama, Kanagawa 230-0045, Japan |
| Author_xml | – sequence: 1 givenname: Yu surname: Adachi fullname: Adachi, Yu – sequence: 2 givenname: Taishi surname: Onodera fullname: Onodera, Taishi – sequence: 3 givenname: Yuki surname: Yamada fullname: Yamada, Yuki – sequence: 4 givenname: Rina surname: Daio fullname: Daio, Rina – sequence: 5 givenname: Makoto surname: Tsuiji fullname: Tsuiji, Makoto – sequence: 6 givenname: Takeshi surname: Inoue fullname: Inoue, Takeshi – sequence: 7 givenname: Kazuo surname: Kobayashi fullname: Kobayashi, Kazuo – sequence: 8 givenname: Tomohiro surname: Kurosaki fullname: Kurosaki, Tomohiro – sequence: 9 givenname: Manabu surname: Ato fullname: Ato, Manabu – sequence: 10 givenname: Yoshimasa surname: Takahashi fullname: Takahashi, Yoshimasa |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26324444$$D View this record in MEDLINE/PubMed |
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| Snippet | Respiratory influenza virus infection induces cross-reactive memory B cells targeting invariant regions of viral escape mutants. However, cellular events... Local germinal center reactions that persist in the lung after influenza infection are required for the generation of cross-reactive memory B cells.... |
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| SubjectTerms | Animals B-Lymphocytes - immunology B-Lymphocytes - virology Cross Reactions Germinal Center - immunology Immunoglobulin G - immunology Immunologic Memory Influenza A virus - pathogenicity Influenza virus Lung - immunology Lung - virology Mice, Inbred BALB C Molecular Sequence Data Mutation Orthomyxoviridae Infections - immunology Single-Domain Antibodies - genetics Single-Domain Antibodies - immunology |
| Title | Distinct germinal center selection at local sites shapes memory B cell response to viral escape |
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