Oncogenic EGFR Represses the TET1 DNA Demethylase to Induce Silencing of Tumor Suppressors in Cancer Cells

Cell Rep. 2016 Jul 12;16(2):457-471. doi: 10.1016/j.celrep.2016.05.087. Epub 2016 Jun 23.

Abstract

Oncogene-induced DNA methylation-mediated transcriptional silencing of tumor suppressors frequently occurs in cancer, but the mechanism and functional role of this silencing in oncogenesis are not fully understood. Here, we show that oncogenic epidermal growth factor receptor (EGFR) induces silencing of multiple unrelated tumor suppressors in lung adenocarcinomas and glioblastomas by inhibiting the DNA demethylase TET oncogene family member 1 (TET1) via the C/EBPα transcription factor. After oncogenic EGFR inhibition, TET1 binds to tumor suppressor promoters and induces their re-expression through active DNA demethylation. Ectopic expression of TET1 potently inhibits lung and glioblastoma tumor growth, and TET1 knockdown confers resistance to EGFR inhibitors in lung cancer cells. Lung cancer samples exhibited reduced TET1 expression or TET1 cytoplasmic localization in the majority of cases. Collectively, these results identify a conserved pathway of oncogenic EGFR-induced DNA methylation-mediated transcriptional silencing of tumor suppressors that may have therapeutic benefits for oncogenic EGFR-mediated lung cancers and glioblastomas.

MeSH terms

  • Adenocarcinoma / drug therapy
  • Adenocarcinoma / enzymology
  • Adenocarcinoma of Lung
  • Antineoplastic Agents / pharmacology
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / enzymology
  • CCAAT-Enhancer-Binding Proteins / metabolism
  • Cell Line, Tumor
  • CpG Islands
  • DNA Methylation
  • Drug Screening Assays, Antitumor
  • ErbB Receptors / antagonists & inhibitors
  • ErbB Receptors / genetics*
  • ErbB Receptors / metabolism
  • Gene Expression Regulation, Neoplastic
  • Gene Silencing
  • Glioblastoma / drug therapy
  • Glioblastoma / enzymology
  • Humans
  • Lung Neoplasms / drug therapy
  • Lung Neoplasms / enzymology
  • MAP Kinase Signaling System
  • Mixed Function Oxygenases / genetics*
  • Mixed Function Oxygenases / metabolism
  • Mutation
  • Oncogenes
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins / genetics*
  • Proto-Oncogene Proteins / metabolism
  • Transcription, Genetic
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism
  • Up-Regulation

Substances

  • Antineoplastic Agents
  • CCAAT-Enhancer-Binding Proteins
  • CEBPA protein, human
  • Protein Kinase Inhibitors
  • Proto-Oncogene Proteins
  • Tumor Suppressor Proteins
  • Mixed Function Oxygenases
  • TET1 protein, human
  • EGFR protein, human
  • ErbB Receptors