Human intestinal myofibroblasts deposited collagen VI enhances adhesiveness for T cells – A novel mechanism for maintenance of intestinal inflammation

Si Nan Lin, Alessandro Musso, Jie Wang, Pranab K. Mukherjee, Gail A. West, Ren Mao, Ruishen Lyu, Jiannan Li, Shuai Zhao, Michael Elias, Yael Haberman, Lee A. Denson, Subra Kugathasan, Min Hu Chen, Doug Czarnecki, Dina Dejanovic, Hongnga T. Le, Jyotsna Chandra, Jeremy Lipman, Scott R. SteeleQuang Tam Nguyen, Claudio Fiocchi, Florian Rieder*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

9 Scopus citations

Abstract

Objective: Inflammatory bowel diseases (IBD) cause chronic intestinal damage and extracellular matrix (ECM) remodeling. The ECM may play an active role in inflammation by modulating immune cell functions, including cell adhesion, but this hypothesis has not been tested in IBD. Design: Primary human intestinal myofibroblast (HIMF)-derived ECM from IBD and controls, 3D decellularized colon or ECM molecule-coated scaffolds were tested for their adhesiveness for T cells. Matrisome was analysed via proteomics. Functional integrin blockade was used to investigate the underlying mechanism. Analysis of the pediatric Crohn's disease (CD) RISK inception cohort was used to explore an altered ECM gene expression as a potential predictor for a future complicated disease course. Results: HIMF-derived ECM and 3D decellularized colonic ECM from IBD bound more T cells compared to control. Control HIMFs exposed to the pro-inflammatory cytokines Iinterleukin-1β (IL-1β) and tumor necrosis factor (TNF) increased, and to transforming growth factor-β1 (TGF-β1) decreased ECM adhesiveness to T cells. Matrisome analysis of the HIMF-derived ECM revealed collagen VI as a major culprit for differences in T cell adhesion. Collagen VI knockdown in HIMF reduced adhesion T cell as did the blockage of integrin αvβ1. Elevated gene expression of collagen VI in biopsies of pediatric CD patients was linked to risk for future stricturing disease. Conclusion: HIMF-derived ECM in IBD binds a remarkably enhanced number of T cells, which is dependent on Collagen VI and integrin αvβ1. Collagen VI expression is a risk factor for a future complicated CD course. Blocking immune cells retention may represent a novel approach to treatment in IBD.

Original languageEnglish
Pages (from-to)1-21
Number of pages21
JournalMatrix Biology
Volume113
DOIs
StatePublished - Nov 2022

Funding

FundersFunder number
Baylor College School of Medicine
Children's Hospital of Pittsburgh of UPMC
Cohen Children's Medical Center
John Hopkins University, Baltimore
Riley Children's Hospital
Stenosis Therapy and Anti-Fibrotic Research3081
National Institutes of Health
National Institute of Diabetes and Digestive and Kidney DiseasesR01DK123233, P30DK097948
National Institute of Diabetes and Digestive and Kidney Diseases
Children's Hospital Los Angeles
Comer Children's Hospital, University of Chicago Medicine
Leona M. and Harry B. Helmsley Charitable Trust
Texas Children's Hospital
Cleveland Clinic2 P30 DK097948-06, 2 P30 DK097948
Cleveland Clinic
University of Utah
University of North Carolina Wilmington
Crohn's and Colitis Foundation569125
Crohn's and Colitis Foundation
Cedars-Sinai Medical Center
National Natural Science Foundation of China81970483, 82222010, 82170537, 82200573
National Natural Science Foundation of China

    Keywords

    • Cell adhesion
    • Extracellular matrix
    • Inflammatory bowel disease
    • Intestinal T cells

    Fingerprint

    Dive into the research topics of 'Human intestinal myofibroblasts deposited collagen VI enhances adhesiveness for T cells – A novel mechanism for maintenance of intestinal inflammation'. Together they form a unique fingerprint.

    Cite this