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Synovial matrix turnover controls immune cell spatial patterning in inflammation resolution

Abstract:
Immune-mediated inflammatory diseases remain plagued by poor treatment responses and lack curative therapies. Convergent findings suggest a role for stromal compartment and extracellular matrix composition dysregulation. Using rheumatoid arthritis as a model, we define an analytical pipeline combining transcriptomic, proteomic and degradomic analysis to characterise disease activity-specific matrix perturbations. This revealed synergistic contributions from fibroblasts and myeloid cells to matrix composition, with fibroblast subsets defining distinct subsynovial niches through distinct matrix expression profiles. Transcriptional dysregulation of collagen VI was found to be a feature of RA activity, with collagen VI protein accumulation linked to remission-associated states. Spatial analysis and in vitro migration showed collagen VI inhibits immune ingress, confining infiltrating cells to perivascular pockets termed "COL6 dark" zones. Matrix degradation-associated monocytes were found at the leading edge of these zones, expanding immune-permissive niches, and releasing RA-associated collagen VI fragments. Our work reveals how dynamic matrix remodelling can in turn limit, and enable, cell immigration in RA, identifying a new mechanism controlling tissuelevel disease activity.
Publication status:
Published
Peer review status:
Peer reviewed

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Files:
Publisher copy:
10.1038/s44320-025-00149-7

Authors


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Institution:
University of Oxford
Division:
MSD
Department:
NDORMS
Sub department:
Kennedy Institute for Rheumatology
Role:
Author
ORCID:
0000-0002-4052-9772
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDORMS
Sub department:
Kennedy Institute for Rheumatology
Role:
Author
ORCID:
0000-0002-6517-2546
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDORMS
Sub department:
Kennedy Institute for Rheumatology
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDORMS
Sub department:
Kennedy Institute for Rheumatology
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
NDORMS
Sub department:
Kennedy Institute for Rheumatology
Role:
Author
ORCID:
0009-0001-3123-7305


More from this funder
Funder identifier:
https://ror.org/02jkpm469
Grant:
23158


Publisher:
EMBO Press
Journal:
Molecular Systems Biology More from this journal
Publication date:
2025-09-22
Acceptance date:
2025-09-02
DOI:
EISSN:
1744-4292


Language:
English
Keywords:
Pubs id:
2287710
Local pid:
pubs:2287710
Deposit date:
2025-09-12

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