Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis

Gastroenterology. 2004 Jun;126(7):1711-20. doi: 10.1053/j.gastro.2004.03.010.

Abstract

Background & aims: The main limiting factor for sodium absorption in distal colon is the amiloride-sensitive epithelial sodium channel (ENaC). This study aimed to characterize mechanisms involved in the dysregulation of ENaC expression in ulcerative colitis (UC).

Methods: Epithelial preparations from surgically removed inflamed and control sigmoid colons were used. Active electrogenic Na(+) transport (J(Na)) was determined after 8-hour aldosterone stimulation in Ussing-chambers (corrected for the altered epithelial/subepithelial resistance ratio). Subsequently, ENaC alpha-, beta-, and gamma-subunits were analyzed immunohistochemically and in Western and Northern blots (corrected for the inflammatory increase in subepithelial protein content). To study gene regulation, the promoters of beta- and gamma-ENaC were analyzed in reporter gene assays.

Results: In controls, aldosterone stimulated J(Na) and induced ENaC beta- and gamma-subunit expression, whereas this response was virtually abolished in UC. Preservation of surface epithelium in UC was indicated by unchanged ENaC alpha-subunit expression, which points also against a mere immaturity or epithelial cell loss. Inhibition of electrogenic sodium transport as well as beta- and gamma-ENaC mRNA expression could be mimicked in control colon by in vitro preexposure for 8 hours to tumor necrosis factor alpha and interferon gamma. Promoter analysis revealed that down-regulation of beta- and gamma-ENaC gene expression was primarily induced by tumor necrosis factor alpha.

Conclusions: We conclude that, in UC, elevated proinflammatory cytokines selectively impair beta- and gamma-ENaC expression, which contributes to diarrhea by reducing colonic sodium absorption.

MeSH terms

  • Antineoplastic Agents / pharmacology
  • Colitis, Ulcerative / immunology
  • Colitis, Ulcerative / pathology
  • Colitis, Ulcerative / physiopathology*
  • Colon / drug effects
  • Colon / pathology
  • Diarrhea / immunology
  • Diarrhea / pathology
  • Diarrhea / physiopathology
  • Down-Regulation
  • Epithelial Sodium Channels
  • Humans
  • Immunohistochemistry
  • Interferon-gamma / pharmacology
  • Promoter Regions, Genetic
  • RNA, Messenger / analysis
  • Receptors, Mineralocorticoid / metabolism
  • Sodium / metabolism
  • Sodium Channels / genetics*
  • Sodium Channels / metabolism*
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / physiology
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Antineoplastic Agents
  • Epithelial Sodium Channels
  • RNA, Messenger
  • Receptors, Mineralocorticoid
  • SCNN1B protein, human
  • Sodium Channels
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Sodium