Crohn's disease-associated Escherichia coli LF82 aggravates colitis in injured mouse colon via signaling by flagellin

Inflamm Bowel Dis. 2008 Aug;14(8):1051-60. doi: 10.1002/ibd.20423.

Abstract

Background: Ileal lesions in Crohn's disease patients are colonized by pathogenic adherent-invasive Escherichia coli (AIEC) that harbor various virulence factors involved in adhesion to and invasion of intestinal epithelial cultured cells. We investigated in a mouse model of colonic inflammation the behavior of virulent AIEC reference bacteria LF82 compared to that of nonflagellated LF82 mutants.

Methods: BALBc/J mice with intact or dextran sulfate sodium (DSS)-injured colon were orally challenged daily with 10(8) bacteria. The severity of colitis was assessed by determining disease activity index, colonic histological score, and myeoloperoxidase activity. Flagellin receptor and cytokine expression was measured by reverse-transcriptase polymerase chain reaction (RT-PCR) in colonic tissue.

Results: In contrast to nonpathogenic E. coli, virulent LF82 bacteria exacerbated colitis in DSS-treated mice, substantially reducing survival rate, greatly lowering stool consistency, inducing marked weight loss and increased rectal bleeding, and significantly increasing erosive lesions and mucosal inflammation. Nonflagellated LF82 mutants behaved like nonpathogenic E. coli K-12. Interestingly, oral infection with LF82 virulent bacteria, but not with a nonvirulent LF82 mutant, induced a 7.0-fold increase in the levels of TLR5 and a 3.1-fold increase in those of ipaf mRNA, which encode respectively membrane and cytosolic receptors involved in the recognition of flagellin. Hence, a 5.6-fold increase in IL-1beta and a 5.3-fold increase in mRNA of IL-6 were observed in mice challenged with AIEC LF82 bacteria.

Conclusions: Crohn's disease-associated virulent AIEC LF82 bacteria, via expression of flagella, are able to potentiate an inflammatory mucosal immune response involving increased expression of TLR5 and IPAF flagellin receptors.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / biosynthesis
  • Calcium-Binding Proteins / biosynthesis
  • Colitis / immunology
  • Colitis / microbiology*
  • Crohn Disease / immunology
  • Crohn Disease / microbiology*
  • Disease Models, Animal
  • Escherichia coli / pathogenicity*
  • Flagellin / immunology*
  • Gene Expression
  • Gene Expression Regulation, Bacterial*
  • Intestinal Mucosa / immunology
  • Intestinal Mucosa / microbiology
  • Mice
  • Mice, Inbred BALB C
  • Reverse Transcriptase Polymerase Chain Reaction
  • Severity of Illness Index
  • Signal Transduction
  • Toll-Like Receptor 5 / biosynthesis

Substances

  • Apoptosis Regulatory Proteins
  • Calcium-Binding Proteins
  • Ipaf protein, mouse
  • Toll-Like Receptor 5
  • Flagellin