Lipid rafts are disrupted in mildly inflamed intestinal microenvironments without overt disruption of the epithelial barrier

Am J Physiol Gastrointest Liver Physiol. 2012 Apr 15;302(8):G781-93. doi: 10.1152/ajpgi.00002.2011. Epub 2012 Jan 12.

Abstract

Intestinal epithelial barrier disruption is a feature of inflammatory bowel disease (IBD), but whether barrier disruption precedes or merely accompanies inflammation remains controversial. Tight junction (TJ) adhesion complexes control epithelial barrier integrity. Since some TJ proteins reside in cholesterol-enriched regions of the cell membrane termed lipid rafts, we sought to elucidate the relationship between rafts and intestinal epithelial barrier function. Lipid rafts were isolated from Caco-2 intestinal epithelial cells primed with the proinflammatory cytokine interferon-γ (IFN-γ) or treated with methyl-β-cyclodextrin as a positive control for raft disruption. Rafts were also isolated from the ilea of mice in which colitis had been induced in conjunction with in vivo intestinal permeability measurements, and lastly from intestinal biopsies of ulcerative colitis (UC) patients with predominantly mild or quiescent disease. Raft distribution was analyzed by measuring activity of the raft-associated enzyme alkaline phosphatase and by performing Western blot analysis for flotillin-1. Epithelial barrier integrity was estimated by measuring transepithelial resistance in cytokine-treated cells or in vivo permeability to fluorescent dextran in colitic mice. Raft and nonraft fractions were analyzed by Western blotting for the TJ proteins occludin and zonula occludens-1 (ZO-1). Our results revealed that lipid rafts were disrupted in IFN-γ-treated cells, in the ilea of mice with subclinical colitis, and in UC patients with quiescent inflammation. This was not associated with a clear pattern of occludin or ZO-1 relocalization from raft to nonraft fractions. Significantly, a time-course study in colitic mice revealed that disruption of lipid rafts preceded the onset of increased intestinal permeability. Our data suggest for the first time that lipid raft disruption occurs early in the inflammatory cascade in murine and human colitis and, we speculate, may contribute to subsequent disruption of epithelial barrier function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Biopsy
  • Blotting, Western
  • Caco-2 Cells
  • Centrifugation, Density Gradient
  • Colitis, Ulcerative / pathology
  • Diet
  • Electrophoresis, Polyacrylamide Gel
  • Enteritis / chemically induced
  • Enteritis / genetics
  • Enteritis / pathology*
  • Female
  • Humans
  • Interleukin-10 / genetics
  • Intestinal Mucosa / pathology*
  • Intestines / pathology*
  • Lipid Metabolism
  • Male
  • Membrane Microdomains / pathology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microscopy, Confocal
  • Middle Aged
  • Permeability
  • Tight Junctions / pathology

Substances

  • Interleukin-10