Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pylori-induced apoptosis

Gastroenterology. 2009 Apr;136(4):1297-1307, e1-3. doi: 10.1053/j.gastro.2008.12.059. Epub 2009 Jan 1.

Abstract

Background & aims: Helicobacter pylori infection disrupts the balance between gastric epithelial cell proliferation and apoptosis, which is likely to lower the threshold for the development of gastric adenocarcinoma. H pylori infection is associated with epidermal growth factor (EGF) receptor (EGFR) activation through metalloproteinase-dependent release of EGFR ligands in gastric epithelial cells. Because EGFR signaling regulates cell survival, we investigated whether activation of EGFR following H pylori infection promotes gastric epithelial survival.

Methods: Mouse conditionally immortalized stomach epithelial cells (ImSt) and a human gastric epithelial cell line, AGS cells, as well as wild-type and kinase-defective EGFR (EGFRwa2) mice, were infected with the H pylori cag+ strain 7.13. Apoptosis, caspase activity, EGFR activation (phosphorylation), and EGFR downstream targets were analyzed.

Results: Inhibiting EGFR kinase activity or decreasing EGFR expression significantly increased H pylori-induced apoptosis in ImSt. Blocking H pylori-induced EGFR activation with a heparin-binding (HB)-EGF neutralizing antibody or abrogating a disintegrin and matrix metalloproteinase-17 (ADAM-17) expression increased apoptosis of H pylori-infected AGS and ImSt, respectively. Conversely, pretreatment of ImSt with HB-EGF completely blocked H pylori-induced apoptosis. H pylori infection stimulated gastric epithelial cell apoptosis in EGFRwa2 but not in wild-type mice. Furthermore, H pylori-induced EGFR phosphorylation stimulated phosphotidylinositol-3'-kinase-dependent activation of the antiapoptotic factor Akt, increased expression of the antiapoptotic factor Bcl-2, and decreased expression of the proapoptotic factor Bax.

Conclusions: EGFR activation by H pylori infection has an antiapoptotic effect in gastric epithelial cells that appears to involve Akt signaling and Bcl family members. These findings provide important insights into the mechanisms of H pylori-associated tumorigenesis.

Publication types

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

MeSH terms

  • ADAM Proteins / genetics
  • ADAM Proteins / metabolism
  • ADAM17 Protein
  • Animals
  • Apoptosis*
  • Caspase 3 / metabolism
  • Cell Line
  • Cell Proliferation
  • Disease Models, Animal
  • Epithelial Cells / metabolism
  • Epithelial Cells / microbiology*
  • Epithelial Cells / pathology*
  • ErbB Receptors / metabolism*
  • Gastric Mucosa / metabolism
  • Helicobacter Infections / microbiology
  • Helicobacter Infections / pathology
  • Helicobacter Infections / prevention & control*
  • Helicobacter pylori
  • Humans
  • Mice
  • Mice, Transgenic
  • Proto-Oncogene Proteins c-akt / metabolism
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Signal Transduction / physiology
  • Stomach / microbiology*
  • Stomach / pathology*
  • bcl-2-Associated X Protein / metabolism

Substances

  • Proto-Oncogene Proteins c-bcl-2
  • bcl-2-Associated X Protein
  • ErbB Receptors
  • Proto-Oncogene Proteins c-akt
  • Caspase 3
  • ADAM Proteins
  • ADAM17 Protein
  • ADAM17 protein, human
  • Adam17 protein, mouse