ClC-3 chloride channel/antiporter defect contributes to inflammatory bowel disease in humans and mice

Gut. 2014 Oct;63(10):1587-95. doi: 10.1136/gutjnl-2013-305168. Epub 2014 Jan 17.

Abstract

Background: ClC-3 channel/antiporter plays a critical role in a variety of cellular activities. ClC-3 has been detected in the ileum and colon.

Objective: To determine the functions of ClC-3 in the gastrointestinal tract.

Design: After administration of dextran sulfate sodium (DSS) or 2,4,6-trinitrobenzenesulfonic acid (TNBS), intestines from ClC-3-/- and wild-type mice were examined by histological, cellular, molecular and biochemical approaches. ClC-3 expression was determined by western blot and immunostaining.

Results: ClC-3 expression was reduced in intestinal tissues from patients with UC or Crohn's disease and from mice treated with DSS. Genetic deletion of ClC-3 increased the susceptibility of mice to DSS- or TNBS-induced experimental colitis and prevented intestinal recovery. ClC-3 deficiency promoted DSS-induced apoptosis of intestinal epithelial cells through the mitochondria pathway. ClC-3 interacts with voltage-dependent anion channel 1, a key player in regulation of mitochondria cytochrome c release, but DSS treatment decreased this interaction. In addition, lack of ClC-3 reduced the numbers of Paneth cells and impaired the expression of antimicrobial peptides. These alterations led to dysfunction of the epithelial barrier and invasion of commensal bacteria into the mucosa.

Conclusions: A defect in ClC-3 may contribute to the pathogenesis of IBD by promoting intestinal epithelial cell apoptosis and Paneth cell loss, suggesting that modulation of ClC-3 expression might be a new strategy for the treatment of IBD.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antiporters / drug effects
  • Antiporters / metabolism*
  • Apoptosis
  • Blotting, Western
  • Chloride Channels / physiology*
  • Colitis, Ulcerative / chemically induced
  • Colitis, Ulcerative / metabolism*
  • Colitis, Ulcerative / pathology
  • Crohn Disease / metabolism*
  • Crohn Disease / pathology
  • Dextran Sulfate / toxicity
  • Disease Models, Animal
  • Electrophoresis, Polyacrylamide Gel
  • Gastrointestinal Tract / drug effects
  • Gastrointestinal Tract / metabolism*
  • Gastrointestinal Tract / pathology
  • Humans
  • In Situ Nick-End Labeling
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Paneth Cells / pathology*
  • Trinitrobenzenesulfonic Acid / toxicity

Substances

  • Antiporters
  • Chloride Channels
  • ClC-3 channel
  • Trinitrobenzenesulfonic Acid
  • Dextran Sulfate