β-Catenin and p120 mediate PPARδ-dependent proliferation induced by Helicobacter pylori in human and rodent epithelia

Gastroenterology. 2011 Aug;141(2):553-64. doi: 10.1053/j.gastro.2011.05.004. Epub 2011 May 17.

Abstract

Background & aims: Colonization of gastric mucosa by Helicobacter pylori leads to epithelial hyperproliferation, which increases the risk for gastric adenocarcinoma. One H pylori virulence locus associated with cancer risk, cag, encodes a secretion system that transports effectors into host cells and leads to aberrant activation of β-catenin and p120-catenin (p120). Peroxisome proliferator-activated receptor (PPAR)δ is a ligand-activated transcription factor that affects oncogenesis in conjunction with β-catenin. We used a carcinogenic H pylori strain to define the role of microbial virulence constituents and PPARδ in regulating epithelial responses that mediate development of adenocarcinoma.

Methods: Gastric epithelial cells or colonies were co-cultured with the H pylori cag(+) strain 7.13 or cagE(-), cagA(-), soluble lytic transglycosylase(-), or cagA(-)/soluble lytic transglycosylase(-) mutants. Levels of PPARδ and cyclin E1 were determined by real-time, reverse-transcription polymerase chain reaction, immunoblot analysis, or immunofluorescence microscopy; proliferation was measured in 3-dimensional culture. PPARδ and Ki67 expression were determined by immunohistochemical analysis of human biopsies and rodent gastric mucosa.

Results: H pylori induced β-catenin- and p120-dependent expression and activation of PPARδ in gastric epithelial cells, which were mediated by the cag secretion system substrates CagA and peptidoglycan. H pylori stimulated proliferation in vitro, which required PPARδ-mediated activation of cyclin E1; H pylori did not induce expression of cyclin E1 in a genetic model of PPARδ deficiency. PPARδ expression and proliferation in rodent and human gastric tissue was selectively induced by cag(+) strains and PPARδ levels normalized after eradication of H pylori.

Conclusions: The H pylori cag secretion system activates β-catenin, p120, and PPARδ, which promote gastric epithelial cell proliferation via activation of cyclin E1. PPARδ might contribute to gastric adenocarcinoma development in humans.

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

  • Adenocarcinoma / microbiology*
  • Adenocarcinoma / pathology
  • Animals
  • Antigens, Bacterial / genetics
  • Antigens, Bacterial / metabolism
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Catenins / metabolism
  • Cell Proliferation
  • Cell Transformation, Neoplastic
  • Cells, Cultured
  • Cyclin E / metabolism
  • Delta Catenin
  • Epithelial Cells / metabolism*
  • Epithelial Cells / microbiology
  • Gastric Mucosa / metabolism
  • Gastric Mucosa / pathology
  • Gerbillinae
  • Helicobacter Infections / metabolism*
  • Helicobacter pylori / genetics
  • Helicobacter pylori / metabolism*
  • Humans
  • Ki-67 Antigen / metabolism
  • Oncogene Proteins / metabolism
  • PPAR delta / metabolism*
  • Signal Transduction
  • Stomach Neoplasms / microbiology*
  • Stomach Neoplasms / pathology
  • beta Catenin / metabolism

Substances

  • Antigens, Bacterial
  • Bacterial Proteins
  • CCNE1 protein, human
  • Catenins
  • Cyclin E
  • Ki-67 Antigen
  • Oncogene Proteins
  • PPAR delta
  • beta Catenin
  • cagA protein, Helicobacter pylori
  • Delta Catenin