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Recycling of memory B cells between germinal center and lymph node subcapsular sinus supports affinity maturation to antigenic drift

Author

Listed:
  • Yang Zhang

    (University of Birmingham)

  • Laura Garcia-Ibanez

    (University of Birmingham)

  • Carolin Ulbricht

    (Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
    Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute)

  • Laurence S. C. Lok

    (University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus)

  • Jeremy A. Pike

    (Universities of Birmingham and Nottingham
    University of Birmingham)

  • Jennifer Mueller-Winkler

    (The Francis Crick Institute)

  • Thomas W. Dennison

    (University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus)

  • John R. Ferdinand

    (University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus)

  • Cameron J. M. Burnett

    (University of Birmingham)

  • Juan C. Yam-Puc

    (University of Birmingham)

  • Lingling Zhang

    (University of Birmingham
    The Francis Crick Institute)

  • Raul Maqueda Alfaro

    (University of Birmingham
    The National Polytechnic Institute, Cinvestav-IPN, Av. IPN 2508, San Pedro Zacatenco, Gustavo A. Madero)

  • Yousuke Takahama

    (Thymus Biology Section, Experimental Immunology Branch, National Cancer Institute, National Institutes of Health)

  • Izumi Ohigashi

    (University of Tokushima)

  • Geoffrey Brown

    (The National Polytechnic Institute, Cinvestav-IPN, Av. IPN 2508, San Pedro Zacatenco, Gustavo A. Madero)

  • Tomohiro Kurosaki

    (Osaka University
    Laboratory of Lymphocyte Differentiation, RIKEN Center for Integrative Medical Sciences (IMS))

  • Victor L. J. Tybulewicz

    (The Francis Crick Institute
    Imperial College)

  • Antal Rot

    (Queen Mary University London
    Queen Mary University London
    Ludwig-Maximilians University)

  • Anja E. Hauser

    (Charité - Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin
    Deutsches Rheuma-Forschungszentrum (DRFZ), a Leibniz Institute)

  • Menna R. Clatworthy

    (University of Cambridge Molecular Immunity Unit, MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus)

  • Kai-Michael Toellner

    (University of Birmingham)

Abstract

Infection or vaccination leads to the development of germinal centers (GC) where B cells evolve high affinity antigen receptors, eventually producing antibody-forming plasma cells or memory B cells. Here we follow the migratory pathways of B cells emerging from germinal centers (BEM) and find that many BEM cells migrate into the lymph node subcapsular sinus (SCS) guided by sphingosine-1-phosphate (S1P). From the SCS, BEM cells may exit the lymph node to enter distant tissues, while some BEM cells interact with and take up antigen from SCS macrophages, followed by CCL21-guided return towards the GC. Disruption of local CCL21 gradients inhibits the recycling of BEM cells and results in less efficient adaption to antigenic variation. Our findings thus suggest that the recycling of antigen variant-specific BEM cells and transport of antigen back to GC may support affinity maturation to antigenic drift.

Suggested Citation

  • Yang Zhang & Laura Garcia-Ibanez & Carolin Ulbricht & Laurence S. C. Lok & Jeremy A. Pike & Jennifer Mueller-Winkler & Thomas W. Dennison & John R. Ferdinand & Cameron J. M. Burnett & Juan C. Yam-Puc , 2022. "Recycling of memory B cells between germinal center and lymph node subcapsular sinus supports affinity maturation to antigenic drift," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29978-y
    DOI: 10.1038/s41467-022-29978-y
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    References listed on IDEAS

    as
    1. Karin Reif & Eric H. Ekland & Lars Ohl & Hideki Nakano & Martin Lipp & Reinhold Förster & Jason G. Cyster, 2002. "Balanced responsiveness to chemoattractants from adjacent zones determines B-cell position," Nature, Nature, vol. 416(6876), pages 94-99, March.
    2. Tobias Junt & E. Ashley Moseman & Matteo Iannacone & Steffen Massberg & Philipp A. Lang & Marianne Boes & Katja Fink & Sarah E. Henrickson & Dmitry M. Shayakhmetov & Nelson C. Di Paolo & Nico van Rooi, 2007. "Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells," Nature, Nature, vol. 450(7166), pages 110-114, November.
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