Crohn disease-associated Escherichia coli promote gastrointestinal inflammatory disorders by activation of HIF-dependent responses

Gut Microbes. 2011 Nov-Dec;2(6):335-46. doi: 10.4161/gmic.18771. Epub 2011 Nov 1.

Abstract

Crohn disease (CD) ileal lesions are colonized by adherent-invasive E. coli (AIEC) that locally induce inflammation. Hypoxia inducible factor (HIF)-1alpha protein is expressed in acute and chronically inflamed site; however the molecular basis of this expression is not fully understood. The aim of the study was to access whether AIEC induce HIF-1α expression and to study the consequence of HIF-1α expression on the onset of Crohn disease pathogenesis. We show that HIF-1α is maximally expressed in inflamed ileal epithelium of CD-patients. CEACAM6, a protein that acts as a receptor of AIEC, is expressed in this particular condition. Using CEABAC 10 transgenic mice that express CEACAM6, we show that AIEC bacteria, but not non-pathogenic E. coli K12, induce the production of HIF-1alpha protein and the activation of VEGF/VEGFR signaling. Downstream analyses on human intestinal epithelial cells silenced for hif- 1α, highlight the crucial role of this protein in production of pro-angiogenic factors. This study highlights the crucial role of AIEC bacteria as promoter of inflammatory disorders of the gastrointestinal tract and provides clear evidence that HIF-1α protein plays a major role in mediating this effect.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Bacterial Adhesion
  • Case-Control Studies
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism
  • Crohn Disease / metabolism
  • Crohn Disease / microbiology*
  • Crohn Disease / pathology
  • Escherichia coli / growth & development
  • Escherichia coli / pathogenicity*
  • Escherichia coli Infections / metabolism
  • Escherichia coli Infections / microbiology
  • Female
  • Flagella / metabolism
  • GPI-Linked Proteins / genetics
  • GPI-Linked Proteins / metabolism
  • Gene Silencing
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Ileum / metabolism
  • Ileum / microbiology
  • Ileum / pathology
  • Immunohistochemistry
  • Intestinal Mucosa / metabolism
  • Intestinal Mucosa / microbiology
  • Intestinal Mucosa / pathology*
  • Male
  • Mice
  • Mice, Transgenic
  • Middle Aged
  • Signal Transduction
  • Toll-Like Receptor 5 / metabolism
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism
  • Young Adult

Substances

  • Antigens, CD
  • CEACAM6 protein, human
  • Cell Adhesion Molecules
  • GPI-Linked Proteins
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • TLR5 protein, human
  • Toll-Like Receptor 5
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse