Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response

J Clin Invest. 2001 Jan;107(1):99-109. doi: 10.1172/JCI10501.

Abstract

This study investigated whether soluble paracrine factors mediated Salmonella-induced IL-8 expression in polarized model intestinal epithelia. We found that the basolateral media of model epithelia that had been apically infected with Salmonella typhimurium for a short period (10 minutes) could activate IL-8 secretion in virgin model epithelia, demonstrating that a proinflammatory factor (PIF) was indeed present. Initial characterization found that PIF was a heat-stable protein with a molecular mass of about 50 kDa that acts on the basolateral, but not apical, surface of model intestinal epithelia to elicit IL-8 secretion. PIF was not present in the media of model epithelia stimulated with other inducers of IL-8 secretion (TNF-alpha or carbachol) but was present in S. typhimurium supernatants, indicating PIF is of bacterial origin. PIF was purified from bacterial culture supernatants by anion/cation exchange chromatography and SDS-PAGE and found by using microsequencing to be the protein flagellin. In support of this finding, flagellin-deficient S. typhimurium mutants did not secrete detectable levels of PIF (i.e., a bioactivity that induced IL-8 secretion when placed basolaterally on model epithelia). Furthermore, viable flagellin-deficient mutant organisms (fliC/fljB and flhD) failed to elicit IL-8 secretion when added apically to model intestinal epithelia. These findings indicate that translocation of flagellin across epithelia, subsequent to apical epithelial-S. typhimurium interaction, is likely a major means of activating a mucosal inflammatory response.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Cell Line
  • Epithelium / immunology
  • Epithelium / microbiology
  • Flagellin / genetics
  • Flagellin / metabolism*
  • Humans
  • Inflammation / etiology*
  • Inflammation / immunology
  • Inflammation / microbiology
  • Inflammation Mediators / metabolism
  • Interleukin-8 / metabolism
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / microbiology*
  • Models, Biological
  • Mutation
  • Salmonella typhimurium / genetics
  • Salmonella typhimurium / pathogenicity*
  • Salmonella typhimurium / physiology

Substances

  • Inflammation Mediators
  • Interleukin-8
  • Flagellin