Cited by 976Rheumatoid Arthritis Research and TherapiesOsteoarthritis Treatment and MechanismsNatural Compounds in Disease Treatment

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Distinct fibroblast subsets drive inflammation and damage in arthritis

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Croft, Adam P., Campos, Joana, Jansen, Kathrin, Turner, Jason D., Marshall, Jennifer, Attar, Moustafa, Savary, Loriane, Wehmeyer, Corinna, Naylor, Amy J., Kemble, Samuel, Begum, Jenefa, Dürholz, Kerstin, 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.·2019·Nature

DOI 10.1038/s41586-019-1263-7PMC PMC6690841

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Abstract

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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Additional file 3 of Incidence and severity of G6PI-induced arthritis are not increased in genetically distinct mouse strains upon aging
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Additional file 4 of Incidence and severity of G6PI-induced arthritis are not increased in genetically distinct mouse strains upon aging
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Additional file 1 of Outcome selection for tissue-agnostic drug trials for immune-mediated inflammatory diseases: a systematic review of core outcome sets and regulatory guidance
Aiyegbusi, O. L., di Ruffano, L. F., Retzer, A., Newsome, P. N., Buckley, C. D., & Calvert, M. J. (2022) · Figshare · doi:10.6084/m9.figshare.18482421
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Additional file 1 of A targeted antibody-based array reveals a serum protein signature as biomarker for adolescent idiopathic scoliosis patients
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Additional file 1 of Incidence and severity of G6PI-induced arthritis are not increased in genetically distinct mouse strains upon aging
Andreas, N., Müller, S., Templin, N., Jordan, P. M., Schuhwerk, H., Müller, M., Gerstmeier, J., Miek, L., Andreas, S., Werz, O., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16435827
Additional file 3 of Reprogramming of synovial macrophage metabolism by synovial fibroblasts under inflammatory conditions
Saeki, N., & Imai, Y. (2020) · Figshare · doi:10.6084/m9.figshare.13311271
Additional file 9 of Functional genomics atlas of synovial fibroblasts defining rheumatoid arthritis heritability
Ge, X. J., Frank‐Bertoncelj, M., Klein, K., McGovern, A., Kuret, T., Houtman, M., Burja, B., Micheroli, R., Shi, C., Marks, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16442141
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Additional file 1 of Oncostatin M-driven macrophage-fibroblast circuits as a drug target in autoimmune arthritis
Huynh, N. C.-N., Ling, R., Komagamine, M., Tianshu, S., Tsukasaki, M., Matsuda, K., Okamoto, K., Asano, T., Muro, R., Pluemsakunthai, W., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26755144
Additional file 1 of Lower peripheral helper T cell levels in the synovium are associated with a better response to anti-TNF therapy in rheumatoid arthritis
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Additional file 1 of 18F-FDG and 68 Ga-FAPI PET/CT for the evaluation of periprosthetic joint infection and aseptic loosening in rabbit models
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Additional file 4 of Functional genomics atlas of synovial fibroblasts defining rheumatoid arthritis heritability
Ge, X. J., Frank‐Bertoncelj, M., Klein, K., McGovern, A., Kuret, T., Houtman, M., Burja, B., Micheroli, R., Shi, C., Marks, M., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16442120
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Additional file 2 of A targeted antibody-based array reveals a serum protein signature as biomarker for adolescent idiopathic scoliosis patients
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Županič, A., Edalat, S. G., Burja, B., Busch, M. P., Kuret, T., Ižanc, N., Zingg, R. S., Pich, L. M. M., Sodin‐Šemrl, S., Distler, O., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.23.713616
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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
Publisher: Springer Science and Business Media LLC
Published: 2019-05-29
Volume: 570
Issue: 7760
Pages: 246-251
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-019-1263-7
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: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
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

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