Increased Production of LIGHT by T Cells in Eosinophilic Esophagitis Promotes Differentiation of Esophageal Fibroblasts Toward an Inflammatory Phenotype.


Journal

Gastroenterology
ISSN: 1528-0012
Titre abrégé: Gastroenterology
Pays: United States
ID NLM: 0374630

Informations de publication

Date de publication:
11 2020
Historique:
received: 27 01 2020
revised: 07 06 2020
accepted: 18 07 2020
pubmed: 28 7 2020
medline: 13 4 2021
entrez: 27 7 2020
Statut: ppublish

Résumé

Eosinophilic esophagitis (EoE) is an antigen-mediated eosinophilic disease of the esophagus that involves fibroblast activation and progression to fibrostenosis. Cytokines produced by T-helper type 2 cells and transforming growth factor beta 1 (TGFβ1) contribute to the development of EoE, but other cytokines involved in pathogenesis are unknown. We investigate the effects of tumor necrosis factor superfamily member 14 (TNFSF14, also called LIGHT) on fibroblasts in EoE. We analyzed publicly available esophageal CD3 LIGHT was up-regulated in the esophageal tissues from patients with EoE, compared with control individuals, and expressed by several T-cell populations, including T-helper type 2 cells. TNF receptor superfamily member 14 (TNFRSF14, also called HVEM) and lymphotoxin beta receptor are receptors for LIGHT that were expressed by fibroblasts from healthy donors or patients with active EoE. Stimulation of esophageal fibroblasts with LIGHT induced inflammatory gene transcription, whereas stimulation with TGFβ1 induced transcription of genes associated with a myofibroblast phenotype. Stimulation of fibroblasts with TGFβ1 increased expression of HVEM; subsequent stimulation with LIGHT resulted in their differentiation into cells that express markers of myofibroblasts and inflammatory chemokines and cytokines. Eosinophils tethered to esophageal fibroblasts after LIGHT stimulation via intercellular adhesion molecule-1. T cells in esophageal tissues from patients with EoE express increased levels of LIGHT compared with control individuals, which induces differentiation of fibroblasts into cells with inflammatory characteristics. TGFβ1 increases fibroblast expression of HVEM, a receptor for LIGHT. LIGHT mediates interactions between esophageal fibroblasts and eosinophils via ICAM1. This pathway might be targeted for the treatment of EoE.

Sections du résumé

BACKGROUND & AIMS
Eosinophilic esophagitis (EoE) is an antigen-mediated eosinophilic disease of the esophagus that involves fibroblast activation and progression to fibrostenosis. Cytokines produced by T-helper type 2 cells and transforming growth factor beta 1 (TGFβ1) contribute to the development of EoE, but other cytokines involved in pathogenesis are unknown. We investigate the effects of tumor necrosis factor superfamily member 14 (TNFSF14, also called LIGHT) on fibroblasts in EoE.
METHODS
We analyzed publicly available esophageal CD3
RESULTS
LIGHT was up-regulated in the esophageal tissues from patients with EoE, compared with control individuals, and expressed by several T-cell populations, including T-helper type 2 cells. TNF receptor superfamily member 14 (TNFRSF14, also called HVEM) and lymphotoxin beta receptor are receptors for LIGHT that were expressed by fibroblasts from healthy donors or patients with active EoE. Stimulation of esophageal fibroblasts with LIGHT induced inflammatory gene transcription, whereas stimulation with TGFβ1 induced transcription of genes associated with a myofibroblast phenotype. Stimulation of fibroblasts with TGFβ1 increased expression of HVEM; subsequent stimulation with LIGHT resulted in their differentiation into cells that express markers of myofibroblasts and inflammatory chemokines and cytokines. Eosinophils tethered to esophageal fibroblasts after LIGHT stimulation via intercellular adhesion molecule-1.
CONCLUSIONS
T cells in esophageal tissues from patients with EoE express increased levels of LIGHT compared with control individuals, which induces differentiation of fibroblasts into cells with inflammatory characteristics. TGFβ1 increases fibroblast expression of HVEM, a receptor for LIGHT. LIGHT mediates interactions between esophageal fibroblasts and eosinophils via ICAM1. This pathway might be targeted for the treatment of EoE.

Identifiants

pubmed: 32712105
pii: S0016-5085(20)34997-0
doi: 10.1053/j.gastro.2020.07.035
pmc: PMC7726704
mid: NIHMS1615942
pii:
doi:

Substances chimiques

ICAM1 protein, human 0
Inflammation Mediators 0
Receptors, Tumor Necrosis Factor, Member 14 0
TNFRSF14 protein, human 0
TNFSF14 protein, human 0
Tumor Necrosis Factor Ligand Superfamily Member 14 0
Intercellular Adhesion Molecule-1 126547-89-5

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1778-1792.e13

Subventions

Organisme : NIAID NIH HHS
ID : K24 AI135034
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI092135
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK114457
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM119850
Pays : United States

Informations de copyright

Copyright © 2020 AGA Institute. Published by Elsevier Inc. All rights reserved.

Auteurs

Mario C Manresa (MC)

Department of Pediatrics, University of California, San Diego, San Diego; Division of Allergy Immunology; La Jolla Institute for Immunology, La Jolla, California.

Austin W T Chiang (AWT)

Department of Pediatrics, University of California, San Diego, San Diego; Novo Nordisk Foundation Center for Biosustainability at the University of California, San Diego, San Diego, California.

Richard C Kurten (RC)

Department of Physiology and Biophysics, University of Arkansas for Medical Sciences, Arkansas Children's Hospital Research Institute, Little Rock, Arkansas.

Ranjan Dohil (R)

Rady Children's Hospital, San Diego.

Howard Brickner (H)

Department of Medicine, University of California, San Diego, San Diego, California.

Lucas Dohil (L)

Department of Pediatrics, University of California, San Diego, San Diego.

Rana Herro (R)

Cincinnati Children's Hospital Medical Center, Immunobiology Division, Cincinnati, Ohio.

Praveen Akuthota (P)

Division of Gastroenterology, Department of Pediatrics, University of California, San Diego; Division of Pulmonary, Critical Care, and Sleep Medicine, University of California San Diego, La Jolla, California.

Nathan E Lewis (NE)

Department of Pediatrics, University of California, San Diego, San Diego; Novo Nordisk Foundation Center for Biosustainability at the University of California, San Diego, San Diego, California; Department of Bioengineering, University of California, San Diego, San Diego, California.

Michael Croft (M)

La Jolla Institute for Immunology, La Jolla, California; Division of Gastroenterology, Department of Pediatrics, University of California, San Diego.

Seema S Aceves (SS)

Department of Pediatrics, University of California, San Diego, San Diego; Division of Allergy Immunology; Rady Children's Hospital, San Diego; Division of Gastroenterology, Department of Pediatrics, University of California, San Diego. Electronic address: saceves@health.ucsd.edu.

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Classifications MeSH