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Recruitment of plasma cells from IL-21-dependent and IL-21-independent immune reactions to the bone marrow

Author

Listed:
  • Marta Ferreira-Gomes

    (ein Institut der Leibniz Gemeinschaft)

  • Yidan Chen

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Pawel Durek

    (ein Institut der Leibniz Gemeinschaft)

  • Hector Rincon-Arevalo

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin
    Universidad de Antioquia UdeA
    and Berlin Institute of Health)

  • Frederik Heinrich

    (ein Institut der Leibniz Gemeinschaft)

  • Laura Bauer

    (University Hospital Schleswig-Holstein)

  • Franziska Szelinski

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Gabriela Maria Guerra

    (ein Institut der Leibniz Gemeinschaft)

  • Ana-Luisa Stefanski

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Antonia Niedobitek

    (ein Institut der Leibniz Gemeinschaft)

  • Annika Wiedemann

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Marina Bondareva

    (ein Institut der Leibniz Gemeinschaft)

  • Jacob Ritter

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Katrin Lehmann

    (ein Institut der Leibniz Gemeinschaft)

  • Sebastian Hardt

    (Charité-Universitätsmedizin Berlin)

  • Christian Hipfl

    (Charité-Universitätsmedizin Berlin)

  • Sascha Hein

    (Bundesinstitut für Impfstoffe und biomedizinische Arzneimittel)

  • Eberhard Hildt

    (Bundesinstitut für Impfstoffe und biomedizinische Arzneimittel)

  • Mareen Matz

    (Berlin Institute of Health at Charité-Universitätsmedizin Berlin)

  • Henrik E. Mei

    (ein Institut der Leibniz Gemeinschaft)

  • Qingyu Cheng

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Van Duc Dang

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Mario Witkowski

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Andreia C. Lino

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Andrey Kruglov

    (ein Institut der Leibniz Gemeinschaft)

  • Fritz Melchers

    (ein Institut der Leibniz Gemeinschaft)

  • Carsten Perka

    (Charité-Universitätsmedizin Berlin)

  • Eva V. Schrezenmeier

    (ein Institut der Leibniz Gemeinschaft
    and Berlin Institute of Health
    Berlin Institute of Health at Charité-Universitätsmedizin Berlin)

  • Andreas Hutloff

    (University Hospital Schleswig-Holstein)

  • Andreas Radbruch

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Thomas Dörner

    (ein Institut der Leibniz Gemeinschaft
    Charité-Universitätsmedizin Berlin)

  • Mir-Farzin Mashreghi

    (ein Institut der Leibniz Gemeinschaft)

Abstract

Bone marrow plasma cells (BMPC) are the correlate of humoral immunity, consistently releasing antibodies into the bloodstream. It remains unclear if BMPC reflect different activation environments or maturation of their precursors. Here we define human BMPC heterogeneity and track the recruitment of antibody-secreting cells (ASC) from SARS-CoV-2 vaccine immune reactions to the bone marrow (BM). Trajectories based on single-cell transcriptomes and repertoires of peripheral and BM ASC reveal sequential colonisation of BMPC compartments. In activated B cells, IL-21 suppresses CD19 expression, indicating that CD19low-BMPC are derived from follicular, while CD19high-BMPC originate from extrafollicular immune reactions. In primary immune reactions, both CD19low- and CD19high-BMPC compartments are populated. In secondary immune reactions, most BMPC are recruited to CD19high-BMPC compartments, reflecting their origin from extrafollicular reactivations of memory B cells. A pattern also observable in vaccinated-convalescent individuals and upon diphtheria/tetanus/pertussis recall-vaccination. Thus, BMPC diversity reflects the evolution of a given humoral immune response.

Suggested Citation

  • Marta Ferreira-Gomes & Yidan Chen & Pawel Durek & Hector Rincon-Arevalo & Frederik Heinrich & Laura Bauer & Franziska Szelinski & Gabriela Maria Guerra & Ana-Luisa Stefanski & Antonia Niedobitek & Ann, 2024. "Recruitment of plasma cells from IL-21-dependent and IL-21-independent immune reactions to the bone marrow," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48570-0
    DOI: 10.1038/s41467-024-48570-0
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    as
    1. Jackson S. Turner & Jane A. O’Halloran & Elizaveta Kalaidina & Wooseob Kim & Aaron J. Schmitz & Julian Q. Zhou & Tingting Lei & Mahima Thapa & Rita E. Chen & James Brett Case & Fatima Amanat & Adriana, 2021. "SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses," Nature, Nature, vol. 596(7870), pages 109-113, August.
    2. Dennis Schaefer-Babajew & Zijun Wang & Frauke Muecksch & Alice Cho & Maximilian Loewe & Melissa Cipolla & Raphael Raspe & Brianna Johnson & Marie Canis & Justin DaSilva & Victor Ramos & Martina Turroj, 2023. "Antibody feedback regulates immune memory after SARS-CoV-2 mRNA vaccination," Nature, Nature, vol. 613(7945), pages 735-742, January.
    3. Junyue Cao & Malte Spielmann & Xiaojie Qiu & Xingfan Huang & Daniel M. Ibrahim & Andrew J. Hill & Fan Zhang & Stefan Mundlos & Lena Christiansen & Frank J. Steemers & Cole Trapnell & Jay Shendure, 2019. "The single-cell transcriptional landscape of mammalian organogenesis," Nature, Nature, vol. 566(7745), pages 496-502, February.
    4. Ariën Schiepers & Marije F. L. Wout & Allison J. Greaney & Trinity Zang & Hiromi Muramatsu & Paulo J. C. Lin & Ying K. Tam & Luka Mesin & Tyler N. Starr & Paul D. Bieniasz & Norbert Pardi & Jesse D. B, 2023. "Molecular fate-mapping of serum antibody responses to repeat immunization," Nature, Nature, vol. 615(7952), pages 482-489, March.
    5. Dimitra Zotos & Isaak Quast & Connie S. N. Li-Wai-Suen & Craig I. McKenzie & Marcus J. Robinson & Andrey Kan & Gordon K. Smyth & Philip D. Hodgkin & David M. Tarlinton, 2021. "The concerted change in the distribution of cell cycle phases and zone composition in germinal centers is regulated by IL-21," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Doan C. Nguyen & Swetha Garimalla & Haopeng Xiao & Shuya Kyu & Igor Albizua & Jacques Galipeau & Kuang-Yueh Chiang & Edmund K. Waller & Ronghu Wu & Greg Gibson & James Roberson & Frances E. Lund & Tro, 2018. "Factors of the bone marrow microniche that support human plasma cell survival and immunoglobulin secretion," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    7. Wafaa B. Alsoussi & Sameer Kumar Malladi & Julian Q. Zhou & Zhuoming Liu & Baoling Ying & Wooseob Kim & Aaron J. Schmitz & Tingting Lei & Stephen C. Horvath & Alexandria J. Sturtz & Katherine M. McInt, 2023. "SARS-CoV-2 Omicron boosting induces de novo B cell response in humans," Nature, Nature, vol. 617(7961), pages 592-598, May.
    8. Rudolf A. Manz & Andreas Thiel & Andreas Radbruch, 1997. "Lifetime of plasma cells in the bone marrow," Nature, Nature, vol. 388(6638), pages 133-134, July.
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