Immunofibroblasts are pivotal drivers of tertiary lymphoid structure formation and local pathology.


Journal

Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876

Informations de publication

Date de publication:
02 07 2019
Historique:
pubmed: 20 6 2019
medline: 31 3 2020
entrez: 20 6 2019
Statut: ppublish

Résumé

Resident fibroblasts at sites of infection, chronic inflammation, or cancer undergo phenotypic and functional changes to support leukocyte migration and, in some cases, aggregation into tertiary lymphoid structures (TLS). The molecular programming that shapes these changes and the functional requirements of this population in TLS development are unclear. Here, we demonstrate that external triggers at mucosal sites are able to induce the progressive differentiation of a population of podoplanin (pdpn)-positive stromal cells into a network of immunofibroblasts that are able to support the earliest phases of TLS establishment. This program of events, that precedes lymphocyte infiltration in the tissue, is mediated by paracrine and autocrine signals mainly regulated by IL13. This initial fibroblast network is expanded and stabilized, once lymphocytes are recruited, by the local production of the cytokines IL22 and lymphotoxin. Interfering with this regulated program of events or depleting the immunofibroblasts in vivo results in abrogation of local pathology, demonstrating the functional role of immunofibroblasts in supporting TLS maintenance in the tissue and suggesting novel therapeutic targets in TLS-associated diseases.

Identifiants

pubmed: 31213547
pii: 1905301116
doi: 10.1073/pnas.1905301116
pmc: PMC6613169
doi:

Substances chimiques

Interleukin-13 0
Interleukins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

13490-13497

Subventions

Organisme : Arthritis Research UK
ID : G0601156
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom
Organisme : Versus Arthritis
ID : 21236
Pays : United Kingdom
Organisme : National Centre for the Replacement, Refinement and Reduction of Animals in Research
ID : NC/K000527/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019 the Author(s). Published by PNAS.

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

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Auteurs

Saba Nayar (S)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Joana Campos (J)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Charlotte G Smith (CG)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Valentina Iannizzotto (V)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

David H Gardner (DH)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Frédéric Mourcin (F)

UMR INSERM U1236, Université Rennes 1, Etablissement Français du Sang, 35043 Rennes, France.

David Roulois (D)

UMR INSERM U1236, Université Rennes 1, Etablissement Français du Sang, 35043 Rennes, France.

Jason Turner (J)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Marvin Sylvestre (M)

UMR INSERM U1236, Université Rennes 1, Etablissement Français du Sang, 35043 Rennes, France.

Saba Asam (S)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Bridget Glaysher (B)

Centre for Immunology and Infection, Department of Biology, Hull York Medical School, University of York, YO10 5DD York, United Kingdom.

Simon J Bowman (SJ)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Douglas T Fearon (DT)

Cancer Research UK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, CB2 0RE Cambridge, United Kingdom.

Andrew Filer (A)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Karin Tarte (K)

UMR INSERM U1236, Université Rennes 1, Etablissement Français du Sang, 35043 Rennes, France.

Sanjiv A Luther (SA)

Department of Biochemistry, Center of Immunity and Infection, University of Lausanne, 1066 Epalinges, Switzerland.

Benjamin A Fisher (BA)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Christopher D Buckley (CD)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

Mark C Coles (MC)

Centre for Immunology and Infection, Department of Biology, Hull York Medical School, University of York, YO10 5DD York, United Kingdom; f.barone@bham.ac.uk mark.coles@kennedy.ox.ac.uk.

Francesca Barone (F)

Rheumatoid Arthritis Pathogenesis Centre of Excellence, Institute of Inflammation and Ageing, College of Medical & Dental Sciences, University of Birmingham Research Laboratories, Queen Elizabeth Hospital, B15 2WB Birmingham, United Kingdom; f.barone@bham.ac.uk mark.coles@kennedy.ox.ac.uk.
bNIHR Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, University of Birmingham, B15 2TT, Birmingham, UK.

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