Paradoxical induction of growth arrest and apoptosis by EGF via the up-regulation of PTEN by activating Redox factor-1/Egr-1 in human lung cancer cells

Oncotarget. 2017 Jan 17;8(3):4181-4195. doi: 10.18632/oncotarget.13809.

Abstract

Epidermal growth factor (EGF) signaling promotes cell proliferation and survival in several types of cancer. Here, however, we showed that EGF inhibits proliferation and promotes programmed cell death in non-small cell lung cancer (NSCLC) cells. In A549 cells, EGF increased redox factor-1 (Ref-1) expression and the association of Ref-1 with zinc finger-containing transcriptional regulator (EGR1) via activation of p22phox, RAC1, and an NADPH oxidase subunit. EGF increased p22phox and RAC1 expression through activation of purinergic receptors (P2Y). Elevated Ref-1/EGR1 levels increased phosphatase and tensin homolog (PTEN) levels, leading to inhibition of the Akt pathway. EGF-induced PTEN upregulation increased apoptosis and autophagy-induced damage in A549 cells, whereas Ref-1 knockdown blocked EGF-induced PTEN upregulation in an NADPH oxidase p22phox subunit-independent manner. In addition, p22phox knockdown restored EGF-induced effects, implying that changes in P2Y activity caused by EGF, which activates NADPH oxidase via RAC1, influenced Ref-1-mediated redox regulation. Finally, EGF similarly attenuated cell proliferation and promoted autophagy and apoptosis in vivo in a xenograft model using A549 cells. These findings reveal that EGF-induced redox signaling is linked to Ref-1-induced death in NSCLC cells.

Keywords: epidermal growth factor (EGF); phosphatase and tensin homolog (PTEN); purinergic receptor 2(P2Y); redox factor-1(Ref-1); zinc finger-containing transcriptional regulator 1(EGR1).

MeSH terms

  • A549 Cells
  • Animals
  • Apoptosis
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • DNA-(Apurinic or Apyrimidinic Site) Lyase / genetics
  • DNA-(Apurinic or Apyrimidinic Site) Lyase / metabolism*
  • Early Growth Response Protein 1 / genetics
  • Early Growth Response Protein 1 / metabolism*
  • Epidermal Growth Factor / administration & dosage*
  • Epidermal Growth Factor / pharmacology
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism
  • Mice
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / metabolism*
  • Signal Transduction / drug effects
  • Up-Regulation*
  • Xenograft Model Antitumor Assays

Substances

  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Epidermal Growth Factor
  • NADPH Oxidases
  • CYBA protein, human
  • PTEN Phosphohydrolase
  • PTEN protein, human
  • APEX1 protein, human
  • DNA-(Apurinic or Apyrimidinic Site) Lyase