Down-regulation of dual-specificity phosphatase 5 in gastric cancer by promoter CpG island hypermethylation and its potential role in carcinogenesis

Am J Pathol. 2013 Apr;182(4):1275-85. doi: 10.1016/j.ajpath.2013.01.004. Epub 2013 Feb 10.

Abstract

Dual-specificity phosphatase 5 (DUSP5), which regulates the duration and magnitude of ERK1/2 phosphoactivation within the mitogen-activated protein kinase (MAPK) cascade, has recently been proposed to be a tumor suppressor. However, the epigenetic regulation of DUSP5 and its critical roles in gastric cancer (GC) remain unknown. We compared differential RNA expression profiles of GC cell lines with or without treatment with the DNA demethylating agent 5-aza-2'-deoxycytidine. DUSP5 expression was dramatically decreased by DNA methylation. Hypermethylation of the DUSP5 promoter was detected in GC tissue samples, but not in normal healthy gastric mucosa samples. Restoring DUSP5 expression in DUSP5-silenced GC cell lines decreased their growth and colony-forming ability by causing arrest in the transition from G1 to S phase in the cell cycle as a result of dephosphorylation of ERK1/2 in the nucleus. Moreover, in a set of surgically resected GC cases (n = 179), GCs with DUSP5 promoter region hypermethylation (30.2%) exhibited significantly shortened survival, compared with GCs without DUSP5 methylation (P = 0.009). These results suggest that silencing of DUSP5 by promoter hypermethylation causes increased maintenance of phosphorylated ERK1/2, driving cell proliferation and contributing to gastric carcinogenesis. Furthermore, DUSP5 methylation may serve as a prognostic marker for GC, but this requires validation in a larger set of GC samples.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Azacitidine / pharmacology
  • Cell Movement / drug effects
  • Cell Movement / genetics
  • Cell Nucleus / drug effects
  • Cell Nucleus / enzymology
  • Cell Proliferation / drug effects
  • Cell Transformation, Neoplastic / genetics*
  • Cell Transformation, Neoplastic / pathology
  • CpG Islands / genetics*
  • DNA Methylation / genetics*
  • Down-Regulation / drug effects
  • Down-Regulation / genetics*
  • Dual-Specificity Phosphatases / genetics*
  • Dual-Specificity Phosphatases / metabolism
  • Epigenesis, Genetic / drug effects
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Female
  • G1 Phase Cell Cycle Checkpoints / drug effects
  • G1 Phase Cell Cycle Checkpoints / genetics
  • Gastric Mucosa / metabolism
  • Gastric Mucosa / pathology
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genetic Association Studies
  • Humans
  • Male
  • Middle Aged
  • Multivariate Analysis
  • Phosphorylation / drug effects
  • Prognosis
  • Promoter Regions, Genetic / genetics*
  • Reproducibility of Results
  • Stomach Neoplasms / enzymology
  • Stomach Neoplasms / genetics*
  • Stomach Neoplasms / pathology

Substances

  • Extracellular Signal-Regulated MAP Kinases
  • DUSP5 protein, human
  • Dual-Specificity Phosphatases
  • Azacitidine