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Double-negative B cells and DNASE1L3 colocalise with microbiota in gut-associated lymphoid tissue

Author

Listed:
  • Lucia Montorsi

    (King’s College London)

  • Michael J. Pitcher

    (King’s College London)

  • Yuan Zhao

    (King’s College London)

  • Chiara Dionisi

    (King’s College London)

  • Alicia Demonti

    (King’s College London
    Claude Bernard Lyon 1 University)

  • Thomas J. Tull

    (King’s College London)

  • Pawan Dhami

    (Genomics Research Platform and Single Cell Laboratory at Guy’s and St Thomas’ NHS Foundation Trust)

  • Richard J. Ellis

    (Advanced Cytometry Platform (Flow Core), Research and Development Department at Guy’s and St Thomas’ NHS Foundation Trust)

  • Cynthia Bishop

    (Advanced Cytometry Platform (Flow Core), Research and Development Department at Guy’s and St Thomas’ NHS Foundation Trust)

  • Jeremy D. Sanderson

    (King’s College London
    Guy’s and St Thomas’ Foundation Trust)

  • Sahil Jain

    (Guy’s and St Thomas’ NHS Foundation Trust)

  • David D’Cruz

    (King’s College London
    Guy’s and St Thomas’ NHS Foundation Trust)

  • Deena L. Gibbons

    (King’s College London)

  • Thomas H. Winkler

    (Friedrich-Alexander-University Erlangen-Nürnberg (FAU))

  • Mats Bemark

    (Lund University
    Sahlgrenska University Hospital)

  • Francesca D. Ciccarelli

    (The Francis Crick Institute)

  • Jo Spencer

    (King’s College London)

Abstract

Intestinal homeostasis is maintained by the response of gut-associated lymphoid tissue to bacteria transported across the follicle associated epithelium into the subepithelial dome. The initial response to antigens and how bacteria are handled is incompletely understood. By iterative application of spatial transcriptomics and multiplexed single-cell technologies, we identify that the double negative 2 subset of B cells, previously associated with autoimmune diseases, is present in the subepithelial dome in health. We show that in this location double negative 2 B cells interact with dendritic cells co-expressing the lupus autoantigens DNASE1L3 and C1q and microbicides. We observe that in humans, but not in mice, dendritic cells expressing DNASE1L3 are associated with sampled bacteria but not DNA derived from apoptotic cells. We propose that fundamental features of autoimmune diseases are microbiota-associated, interacting components of normal intestinal immunity.

Suggested Citation

  • Lucia Montorsi & Michael J. Pitcher & Yuan Zhao & Chiara Dionisi & Alicia Demonti & Thomas J. Tull & Pawan Dhami & Richard J. Ellis & Cynthia Bishop & Jeremy D. Sanderson & Sahil Jain & David D’Cruz &, 2024. "Double-negative B cells and DNASE1L3 colocalise with microbiota in gut-associated lymphoid tissue," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48267-4
    DOI: 10.1038/s41467-024-48267-4
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    References listed on IDEAS

    as
    1. Yuan Zhao & Mohamed Uduman & Jacqueline H. Y. Siu & Thomas J. Tull & Jeremy D. Sanderson & Yu-Chang Bryan Wu & Julian Q. Zhou & Nedyalko Petrov & Richard Ellis & Katrina Todd & Konstantia-Maria Chavel, 2018. "Spatiotemporal segregation of human marginal zone and memory B cell populations in lymphoid tissue," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    2. Rathan Joy Komban & Anneli Strömberg & Adi Biram & Jakob Cervin & Cristina Lebrero-Fernández & Neil Mabbott & Ulf Yrlid & Ziv Shulman & Mats Bemark & Nils Lycke, 2019. "Activated Peyer′s patch B cells sample antigen directly from M cells in the subepithelial dome," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
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