EZH2-DNMT1-mediated epigenetic silencing of miR-142-3p promotes metastasis through targeting ZEB2 in nasopharyngeal carcinoma

Cell Death Differ. 2019 Jun;26(6):1089-1106. doi: 10.1038/s41418-018-0208-2. Epub 2018 Oct 23.

Abstract

Human nasopharyngeal carcinoma (NPC) has the highest metastatic rate in head and neck. However, the mechanisms underlying NPC metastasis remain unclear. Here using propensity-score-matched miRNA microarray analysis, miR-142-3p is identified to be the most correlated with distant-metastasis-free survival and downregulated in paraffin-embedded NPC with distant metastasis, which is validated in both internal cohort and external GEO dataset from Canada. miR-142 locus hypermethylation was observed and found to be associated with miR-142-3p downregulation in metastatic NPC. Furthermore, miR-142-3p was epigenetically silenced by EZH2-recruited DNMT1 and suppressed NPC cell metastasis and EMT. Intersecting PCR array gene profiling with bioinformatic prediction, we identify ZEB2 as a direct and functional target of miR-142-3p in NPC. Reversal of miR-142-3p silencing efficiently suppresses NPC cell invasion and metastasis. Moreover, epigenetic miR-142 hypermethylation is correlated with unfavorable prognosis in both training and validation cohorts. This study identifies miR-142-3p as a key suppressive regulator in NPC metastasis and reveals a DNMT1-mediated epigenetic mechanism for miR-142-3p silencing, providing a potential prognostic marker and therapeutic target to combat NPC metastasis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism*
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Epigenesis, Genetic / genetics
  • Gene Silencing
  • Humans
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Nasopharyngeal Carcinoma / genetics
  • Nasopharyngeal Carcinoma / metabolism*
  • Nasopharyngeal Carcinoma / pathology
  • Nasopharyngeal Neoplasms / genetics
  • Nasopharyngeal Neoplasms / metabolism*
  • Nasopharyngeal Neoplasms / pathology
  • Oligonucleotide Array Sequence Analysis
  • Zinc Finger E-box Binding Homeobox 2 / metabolism*

Substances

  • MIRN142 microRNA, human
  • MicroRNAs
  • ZEB2 protein, human
  • Zinc Finger E-box Binding Homeobox 2
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNMT1 protein, human
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein