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

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, Deena L. Gibbons, Thomas H. Winkler, Mats Bemark, Francesca D. Ciccarelli and Jo Spencer ()
Additional contact information
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
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
Sahil Jain: Guy’s and St Thomas’ NHS Foundation Trust
David D’Cruz: King’s College London
Deena L. Gibbons: King’s College London
Thomas H. Winkler: Friedrich-Alexander-University Erlangen-Nürnberg (FAU)
Mats Bemark: Lund University
Francesca D. Ciccarelli: The Francis Crick Institute
Jo Spencer: King’s College London

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48267-4

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