Systematic memory B cell archiving and random display shape the human splenic marginal zone throughout life

Author:

Kibler Artur1ORCID,Budeus Bettina1ORCID,Homp Ekaterina1ORCID,Bronischewski Kevin1ORCID,Berg Victoria1ORCID,Sellmann Ludger2ORCID,Murke Florian3ORCID,Heinold Andreas3ORCID,Heinemann Falko M.3ORCID,Lindemann Monika3ORCID,Bekeredjian-Ding Isabelle4ORCID,Horn Peter A.3ORCID,Kirschning Carsten J.5ORCID,Küppers Ralf1ORCID,Seifert Marc1ORCID

Affiliation:

1. Institute of Cell Biology (Cancer Research), University of Duisburg-Essen, Essen, Germany

2. Department of Haematology, University Hospital Essen, Essen, Germany

3. Institute for Transfusion Medicine, University Hospital Essen, University of Duisburg-Essen, Essen, Germany

4. Division of Microbiology, Paul-Ehrlich-Institut, Langen, Germany

5. Institute of Medical Microbiology, University of Duisburg-Essen, Essen, Germany

Abstract

Human memory B cells (MBCs) are generated and diversified in secondary lymphoid tissues throughout the organism. A paired immunoglobulin (Ig)-gene repertoire analysis of peripheral blood (PB) and splenic MBCs from infant, adult, and elderly humans revealed that throughout life, circulating MBCs are comprehensively archived in the spleen. Archive MBC clones are systematically preserved and uncoupled from class-switching. Clonality in the spleen increases steadily, but boosts at midlife, thereby outcompeting small clones. The splenic marginal zone (sMZ) represents a primed MBC compartment, generated from a stochastic exchange within the archive memory pool. This is supported by functional assays, showing that PB and splenic CD21+ MBCs acquire transient CD21high expression upon NOTCH2-stimulation. Our study provides insight that the human MBC system in PB and spleen is composed of three interwoven compartments: the dynamic relationship of circulating, archive, and its subset of primed (sMZ) memory changes with age, thereby contributing to immune aging.

Funder

Deutsche Forschungsgemeinschaft

Deutsche Krebshilfe

Publisher

Rockefeller University Press

Subject

Immunology,Immunology and Allergy

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