AMP-activated protein kinase mediates the interferon-gamma-induced decrease in intestinal epithelial barrier function

J Biol Chem. 2009 Oct 9;284(41):27952-27963. doi: 10.1074/jbc.M109.046292. Epub 2009 Aug 4.

Abstract

Impaired epithelial barrier function plays a crucial role in the pathogenesis of inflammatory bowel disease. Elevated levels of the pro-inflammatory cytokine, interferon-gamma (IFNgamma), are believed to be prominently involved in the pathogenesis of Crohn disease. Treatment of T(84) intestinal epithelial cells with IFNgamma severely impairs their barrier properties measured as transepithelial electrical resistance (TER) or permeability and reduces the expression of tight junction proteins such as occludin and zonula occludens-1 (ZO-1). However, little is known about the signaling events that are involved. The cellular energy sensor, AMP-activated protein kinase (AMPK), is activated in response to cellular stress, as occurs during inflammation. The aim of this study was to investigate a possible role for AMPK in mediating IFNgamma-induced effects on the intestinal epithelial barrier. We found that IFNgamma activates AMPK by phosphorylation, independent of intracellular energy levels. Inhibition of AMPK prevents, at least in part, the IFNgamma-induced decrease in TER. Furthermore, AMPK knockdown prevented the increased epithelial permeability, the decreased TER, and the decrease in occludin and ZO-1 caused by IFNgamma treatment of T(84) cells. However, AMPK activity alone was not sufficient to cause alterations in epithelial barrier function. These data show a novel role for AMPK, in concert with other signals induced by IFNgamma, in mediating reduced epithelial barrier function in a cell model of chronic intestinal inflammation. These findings may implicate AMPK in the pathogenesis of chronic intestinal inflammatory conditions, such as inflammatory bowel disease.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism*
  • Animals
  • Cell Membrane Permeability / physiology
  • Cells, Cultured
  • Electric Impedance
  • Enzyme Activation
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism*
  • Gene Knockdown Techniques
  • Humans
  • Inflammatory Bowel Diseases* / immunology
  • Inflammatory Bowel Diseases* / physiopathology
  • Interferon-gamma / metabolism*
  • Intestinal Absorption / physiology
  • Intestinal Mucosa / cytology
  • Intestinal Mucosa / immunology*
  • Intestinal Mucosa / pathology
  • Intestinal Mucosa / physiology*
  • Membrane Proteins / metabolism
  • Occludin
  • Patch-Clamp Techniques
  • Phosphoproteins / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Zonula Occludens-1 Protein

Substances

  • Membrane Proteins
  • OCLN protein, human
  • Occludin
  • Phosphoproteins
  • RNA, Small Interfering
  • TJP1 protein, human
  • Zonula Occludens-1 Protein
  • Interferon-gamma
  • AMP-Activated Protein Kinases