Tissue-resident B cells orchestrate macrophage polarisation and function

Ondrej Suchanek, John R. Ferdinand, Zewen K. Tuong, Sathi Wijeyesinghe, Anita Chandra, Ann-Katrin Clauder, Larissa N. Almeida, Simon Clare, Katherine Harcourt, Christopher J. Ward, Rachael Bashford-Rogers, Trevor Lawley, Rudolf A. Manz, Klaus Okkenhaug, David Masopust and Menna R. Clatworthy ()
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Ondrej Suchanek: University of Cambridge Department of Medicine
John R. Ferdinand: University of Cambridge Department of Medicine
Zewen K. Tuong: University of Cambridge Department of Medicine
Sathi Wijeyesinghe: University of Minnesota
Anita Chandra: University of Cambridge
Ann-Katrin Clauder: University of Luebeck
Larissa N. Almeida: University of Luebeck
Simon Clare: Wellcome Sanger Institute, Wellcome Genome Campus
Katherine Harcourt: Wellcome Sanger Institute, Wellcome Genome Campus
Christopher J. Ward: University of Cambridge Department of Medicine
Rachael Bashford-Rogers: University of Oxford
Trevor Lawley: Wellcome Sanger Institute, Wellcome Genome Campus
Rudolf A. Manz: University of Luebeck
Klaus Okkenhaug: University of Cambridge
David Masopust: University of Minnesota
Menna R. Clatworthy: University of Cambridge Department of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-20

Abstract: Abstract B cells play a central role in humoral immunity but also have antibody-independent functions. Studies to date have focused on B cells in blood and secondary lymphoid organs but whether B cells reside in non-lymphoid organs (NLO) in homeostasis is unknown. Here we identify, using intravenous labeling and parabiosis, a bona-fide tissue-resident B cell population in lung, liver, kidney and urinary bladder, a substantial proportion of which are B-1a cells. Tissue-resident B cells are present in neonatal tissues and also in germ-free mice NLOs, albeit in lower numbers than in specific pathogen-free mice and following co-housing with ‘pet-store’ mice. They spatially co-localise with macrophages and regulate their polarization and function, promoting an anti-inflammatory phenotype, in-part via interleukin-10 production, with effects on bacterial clearance during urinary tract infection. Thus, our data reveal a critical role for tissue-resident B cells in determining the homeostatic ‘inflammatory set-point’ of myeloid cells, with important consequences for tissue immunity.

Date: 2023
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DOI: 10.1038/s41467-023-42625-4

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