PDGF and TGF-β promote tenascin-C expression in subepithelial myofibroblasts and contribute to intestinal mucosal protection in mice

Br J Pharmacol. 2014 Jan;171(2):375-88. doi: 10.1111/bph.12452.

Abstract

Background and purpose: Tenascin-C (TnC) is a multi-domain extracellular matrix glycoprotein that is expressed at a high level during embryogenesis but is almost absent during normal postnatal life. This multi-domain complex molecule is reported to associate with both pro-inflammatory and anti-inflammatory signalling cascades. In this study, we examined how TnC modulated intestinal inflammation.

Experimental approach: TnC pathophysiology was evaluated in cultures of rat intestinal subepithelial myofibroblasts (ISEMF) and intestinal epithelial cells. Wild-type and TnC(-/-) mice were treated with dextran sodium sulfate (DSS) to induce colitis.

Key results: DSS-induced colitis in mice markedly increased TnC in the damaged mucosal areas and up-regulated mRNA for TnC, pro-inflammatory cytokines and growth factors (PDGF-B and TGF-β1). In addition, 2,4,6-trinitrobenzene sulfonic acid-induced colitis and SAMP1/Yit mice, a model of spontaneous Crohn's disease, also exhibited increased mucosal TnC in colon and ilea respectively. PDGF receptor-α (PDGFRα) positive ISEMF were the primary TnC-producing cells in colon tissues. Accordingly, ISEMF collected from the rat colon constitutively expressed both TnC and PDGFRα. PDGF-BB and TGF-β1 up-regulated both TnC mRNA and protein levels in ISEMF. Knock-down of TnC gene increased susceptibility to DSS-induced colitis, compared with TnC(+/+) littermates. TnC(-/-) mice showed marked abrasion of intestinal mucosal barrier and increased inflammatory scores. Moreover, TnC accelerated both trans-well migration and wound healing in epithelial cells.

Conclusions and implications: The pharmacological profiles of PDGF-BB and TGF-β in colitis tissues and ISEMF suggest that increased TnC production during inflammation contributed to epithelial cell migration, remodelling and protection of intestinal barriers.

Keywords: ISEMF; PDGF; TGF-β; epithelial cell; intestinal inflammation; tenascin-C.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / biosynthesis
  • Actins / genetics
  • Animals
  • Anti-Ulcer Agents*
  • Blotting, Western
  • Cell Movement
  • Colitis / metabolism
  • Colitis / pathology
  • Cytokines / metabolism
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Fluorescent Antibody Technique
  • Intestinal Mucosa / drug effects*
  • Lac Operon
  • Male
  • Mice
  • Microscopy, Immunoelectron
  • Molecular Sequence Data
  • Myofibroblasts / drug effects
  • Myofibroblasts / metabolism*
  • Platelet-Derived Growth Factor / pharmacology*
  • RNA / biosynthesis
  • RNA / genetics
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Platelet-Derived Growth Factor alpha / metabolism
  • Tenascin / biosynthesis*
  • Transforming Growth Factor beta / pharmacology*
  • Wound Healing / drug effects

Substances

  • Actins
  • Anti-Ulcer Agents
  • Cytokines
  • Platelet-Derived Growth Factor
  • Tenascin
  • Transforming Growth Factor beta
  • smooth muscle actin, rat
  • RNA
  • Receptor, Platelet-Derived Growth Factor alpha

Associated data

  • GENBANK/M32599