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Distinct fibroblast subsets drive inflammation and damage in arthritis
Open accessAbstract
The identification of lymphocyte subsets with non-overlapping effector functions has been pivotal to the development of targeted therapies in immune-mediated inflammatory diseases (IMIDs)1,2. However, it remains unclear whether fibroblast subclasses with non-overlapping functions also exist and are responsible for the wide variety of tissue-driven processes observed in IMIDs, such as inflammation and damage 3-5. Here we identify and describe the biology of distinct subsets of fibroblasts responsible for mediating either inflammation or tissue damage in arthritis. We show that deletion of fibroblast activation protein-α (FAPα)+ fibroblasts suppressed both inflammation and bone erosions in mouse models of resolving and persistent arthritis. Single-cell transcriptional analysis identified two distinct fibroblast subsets within the FAPα+ population: FAPα+THY1+ immune effector fibroblasts located in the synovial sub-lining, and FAPα+THY1- destructive fibroblasts restricted to the synovial lining layer. When adoptively transferred into the joint, FAPα+THY1- fibroblasts selectively mediate bone and cartilage damage with little effect on inflammation, whereas transfer of FAPα+ THY1+ fibroblasts resulted in a more severe and persistent inflammatory arthritis, with minimal effect on bone and cartilage. Our findings describing anatomically discrete, functionally distinct fibroblast subsets with non-overlapping functions have important implications for cell-based therapies aimed at modulating inflammation and tissue damage.
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“While single-cell sequencing indicates common traits are preserved49–51, it will become increasingly pressing to define common and specific effects of CAFs.”
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“Overwhelming evidence now points to a degree of specialization among CAFs, which may reflect the increasingly appreciated specialization of normal fibroblasts19,50.”
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“Recent studies have implicated a range of mesenchymal progenitor cells (MPs) in the initiation and propagation of fibrosis28–30.”
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Metadata
- Authors
- Croft, A. P., Campos, J., Jansen, K., Turner, J. D., Marshall, J., Attar, M., Savary, L., Wehmeyer, C., Naylor, A. J., Kemble, S., Begum, J., Dürholz, K., Perlman, H., Barone, F., McGettrick, H. M., Fearon, D. T., Wei, K., Raychaudhuri, S., Korsunsky, I., Brenner, M. B., Coles, M., Sansom, S. N., Filer, A., & Buckley, C. D.
- Affiliations
- Queen Elizabeth Hospital Birmingham (GB)
- University of Oxford (GB)
- University of Münster (DE)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Northwestern University (US)
- Cold Spring Harbor Laboratory (US)
- Brigham and Women's Hospital (US)
- University Hospitals Birmingham NHS Foundation Trust (GB)
- Corresponding author
- Buckley, Christopher D.
- ORCID
- Croft, Adam P.
- Campos, Joana
- Jansen, Kathrin
- Turner, Jason D.
- Marshall, Jennifer
- Attar, Moustafa
- Wehmeyer, Corinna
- Naylor, Amy J.
- Kemble, Samuel
- Begum, Jenefa
- Perlman, Harris
- Barone, Francesca
- McGettrick, Helen M.
- Fearon, Douglas T.
- Wei, Kevin
- Raychaudhuri, Soumya
- Korsunsky, Ilya
- Brenner, Michael B.
- Coles, Mark
- Sansom, Stephen N.
- Filer, Andrew
- Buckley, Christopher D.
- Venue
- Nature
- Published
- 2019-05-29
- Volume
- 570
- Issue
- 7760
- Pages
- 246-251
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC6690841
- OpenAlex
- W2944564829
- Cited by
- 976
- References
- 28
- Citations by year
- 2026: 147 · 2025: 144 · 2024: 137 · 2023: 134 · 2022: 128 · 2021: 153 · 2020: 94 · 2019: 36
- FWCI
- 78.26
- Type
- journal article
- Language
- en
- Update notices
- correction (2025-12-12)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (WT104551MA)
- Kennedy Trust for Rheumatology Research (KENN161701, KENN161703)
- National Institute for Health and Care Research (bircrf-2012-1, NF-SI-0617-10128, CL-2018-09-001)
- Academy of Medical Sciences (SGL021\1029)
- Versus Arthritis (19791, 21743, 20015, 14476, 19899, 18547, 21236)
- National Institutes of Health (5r01ar063759-07)
- Medical Research Council (MR/S025308/1, MR/N026977/1)
- National Heart, Lung, and Blood Institute (R01HL134375)
- National Human Genome Research Institute (U01HG009379)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (UH2AR067677, R01-AR063759)
- Topics
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- Health Sciences › Medicine › Rheumatology › Osteoarthritis Treatment and Mechanisms
- Health Sciences › Medicine › Complementary and alternative medicine › Natural Compounds in Disease Treatment
- Keywords
- arthritis, fibroblast activation protein, CD90, synovial lining, bone erosion, cartilage damage, joint inflammation, tissue damage, adoptive transfer, immune-mediated inflammatory diseases
- MeSH terms
- RNA-Seq, Fibroblast Activation Protein Alpha, Animals, Arthritis, Rheumatoid, Bone and Bones, Female, Fibroblasts, Humans, Inflammation, Joints, Male, Membrane Proteins, Endopeptidases, Serine Endopeptidases, Synovial Membrane, Gelatinases, Thy-1 Antigens, Mice, Single-Cell Analysis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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