Ink4a/Arf-Dependent Loss of Parietal Cells Induced by Oxidative Stress Promotes CD44-Dependent Gastric Tumorigenesis

Cancer Prev Res (Phila). 2015 Jun;8(6):492-501. doi: 10.1158/1940-6207.CAPR-15-0025-T. Epub 2015 Mar 26.

Abstract

Loss of parietal cells initiates the development of spasmolytic polypeptide-expressing metaplasia (SPEM), a precancerous lesion in stomach. CD44 variant (CD44v) that enhances the ability to defend against reactive oxygen species (ROS) in epithelial cells is expressed de novo in SPEM of K19-Wnt1/C2mE mice, a transgenic model of gastric tumorigenesis, and is required for the efficient development of SPEM and gastric tumor in these animals. The role of ROS and its downstream signaling in CD44-dependent gastric tumorigenesis has remained unknown, however. With the use of the K19-Wnt1/C2mE mouse, we now show that parietal cells in the inflamed stomach are highly sensitive to oxidative stress and manifest activation of p38(MAPK) signaling by ROS. Oral treatment with the antioxidant ascorbic acid or genetic ablation of the Ink4a/Arf locus, a major downstream target of ROS-p38(MAPK) signaling, inhibited parietal cell loss and the subsequent gastric tumorigenesis. Our results indicate that signaling activated by oxidative stress in parietal cells plays a key role in CD44-dependent gastric tumorigenesis. .

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-Ribosylation Factor 1 / physiology*
  • Animals
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism
  • Cell Transformation, Neoplastic / pathology*
  • Cells, Cultured
  • Cyclin-Dependent Kinase Inhibitor p16 / physiology*
  • Hyaluronan Receptors / metabolism*
  • Immunoenzyme Techniques
  • Metaplasia / metabolism
  • Metaplasia / pathology
  • Mice
  • Mice, Knockout
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology
  • Oxidative Stress*
  • Parietal Cells, Gastric / metabolism
  • Parietal Cells, Gastric / pathology*
  • Signal Transduction
  • Stomach Neoplasms / genetics
  • Stomach Neoplasms / metabolism
  • Stomach Neoplasms / pathology*
  • Wnt1 Protein / physiology
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Cd44 protein, mouse
  • Cyclin-Dependent Kinase Inhibitor p16
  • Hyaluronan Receptors
  • Wnt1 Protein
  • Wnt1 protein, mouse
  • p38 Mitogen-Activated Protein Kinases
  • ADP-Ribosylation Factor 1