EGF-induced C/EBPβ participates in EMT by decreasing the expression of miR-203 in esophageal squamous cell carcinoma cells

J Cell Sci. 2014 Sep 1;127(Pt 17):3735-44. doi: 10.1242/jcs.148759. Epub 2014 Jul 2.

Abstract

Epithelial-mesenchymal transition (EMT) is a developmental program that is associated with esophageal squamous cell carcinoma (ESCC) progression and metastasis. Recently, C/EBPβ has been reported to be an EMT inducer in cancer. However, the detailed molecular mechanisms remain unclear. Here, we report for the first time, that the truncated CCAAT-enhancer-binding protein β (C/EBPβ) LIP isoform is abnormally overexpressed and correlated with cancer metastasis in clinical specimens of human ESCC. Furthermore, we demonstrate that C/EBPβ LIP mediates epithelial growth factor (EGF)-induced EMT and increases migration and invasion of esophageal cancer cells in a manner that is dependent on miR-203 inactivation. Finally, we identified miR-203 as a direct target of C/EBPβ LIP. Disruption of C/EBPβ LIP attenuated the EGF-mediated decrease in miR-203, whereas overexpression of C/EBPβ LIP alone markedly suppressed miR-203. In addition, we demonstrated that C/EBPβ LIP inhibited miR-203 transcription by directly interacting with a conserved distal regulatory element upstream of the miR-203 locus, and in doing so, orchestrated chromatin remodeling. In conclusion, our results have revealed a new regulatory mechanism that involves C/EBPβ-LIP-mediated downregulation of miR-203, which plays a key role in EMT and metastasis.

Keywords: C/EBPβ; ESCC; Epithelial–mesenchymal transition; Metastasis; miR-203.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CCAAT-Enhancer-Binding Protein-beta / genetics*
  • Carcinoma, Squamous Cell / metabolism*
  • Cell Line, Tumor
  • Epidermal Growth Factor / metabolism*
  • Epithelial Cells / metabolism
  • Epithelial-Mesenchymal Transition / genetics*
  • Epithelial-Mesenchymal Transition / physiology
  • Esophageal Neoplasms / metabolism*
  • Esophageal Squamous Cell Carcinoma
  • Gene Expression Regulation, Neoplastic / genetics*
  • Humans
  • MicroRNAs / metabolism*

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • MIRN203 microRNA, human
  • MicroRNAs
  • Epidermal Growth Factor