Gastric epithelial reactive oxygen species prevent normoxic degradation of hypoxia-inducible factor-1alpha in gastric cancer cells

Clin Cancer Res. 2003 Jan;9(1):433-40.

Abstract

The expression of hypoxia inducible factor (HIF)-1alpha protein is tightly regulated by cellular oxygen status. Namely, HIF-1alpha protein is degraded rapidly in normoxic cells, whereas hypoxia stabilizes HIF-1alpha to transactivate hypoxia-responsive genes. Here we show that HIF-1alpha protein is expressed aberrantly in gastric cancer cells under normoxia in a reactive oxygen species (ROS)-dependent manner. The normoxic expression of HIF-1alpha in concordance with its DNA binding activity enhances the transcription of target genes such as vascular endothelial growth factor. The aberrant normoxic expression of HIF-1alpha is not associated with genetic abnormalities such as the loss of von Hippel-Lindau tumor suppressor, but is well correlated with endogenous ROS (hydrogen peroxide) generation. HIF-1alpha expression is blocked by nonmitochondrial ROS inhibitors, but not by inhibitors of mitochondrial electron transfer, which indicates that nonmitochondrial ROS stabilize HIF-1alpha protein in these cells. Gastric epithelial ROS have been linked to Helicobacter pylori-induced gastric carcinogenesis. This study demonstrates for the first time that ROS from H. pylori-infected gastric epithelial cells induce HIF-1alpha expression and subsequently activate HIF-1alpha-mediated transcription. Taken together, these results provide a novel mechanism of HIF-1alpha stabilization in gastric cancer, and demonstrate that gastric epithelial ROS, endogenously generated or H. pylori-stimulated, lead to the constant expression of HIF-1alpha protein under normoxia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dose-Response Relationship, Drug
  • Endothelial Growth Factors / metabolism
  • Genes, Reporter
  • Humans
  • Hypoxia
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Immunoblotting
  • Immunohistochemistry
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Luciferases / metabolism
  • Lymphokines / metabolism
  • Oxygen / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Plasmids / metabolism
  • Promoter Regions, Genetic
  • RNA / metabolism
  • Reactive Oxygen Species*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stomach Neoplasms / metabolism*
  • Time Factors
  • Transcription Factors / metabolism*
  • Transcriptional Activation
  • Transfection
  • Tumor Cells, Cultured
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors

Substances

  • Endothelial Growth Factors
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Intercellular Signaling Peptides and Proteins
  • Lymphokines
  • Reactive Oxygen Species
  • Transcription Factors
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • RNA
  • Luciferases
  • Phosphatidylinositol 3-Kinases
  • Oxygen