Early Epigenetic Downregulation of microRNA-192 Expression Promotes Pancreatic Cancer Progression

Cancer Res. 2016 Jul 15;76(14):4149-59. doi: 10.1158/0008-5472.CAN-15-0390. Epub 2016 May 23.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) is characterized by very early metastasis, suggesting the hypothesis that metastasis-associated changes may occur prior to actual tumor formation. In this study, we identified miR-192 as an epigenetically regulated suppressor gene with predictive value in this disease. miR-192 was downregulated by promoter methylation in both PDAC and chronic pancreatitis, the latter of which is a major risk factor for the development of PDAC. Functional studies in vitro and in vivo in mouse models of PDAC showed that overexpression of miR-192 was sufficient to reduce cell proliferation and invasion. Mechanistic analyses correlated changes in miR-192 promoter methylation and expression with epithelial-mesenchymal transition. Cell proliferation and invasion were linked to altered expression of the miR-192 target gene SERPINE1 that is encoding the protein plasminogen activator inhibitor-1 (PAI-1), an established regulator of these properties in PDAC cells. Notably, our data suggested that invasive capacity was altered even before neoplastic transformation occurred, as triggered by miR-192 downregulation. Overall, our results highlighted a role for miR-192 in explaining the early metastatic behavior of PDAC and suggested its relevance as a target to develop for early diagnostics and therapy. Cancer Res; 76(14); 4149-59. ©2016 AACR.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cadherins / analysis
  • Carcinoma, Pancreatic Ductal / etiology*
  • Carcinoma, Pancreatic Ductal / genetics
  • Carcinoma, Pancreatic Ductal / mortality
  • Carcinoma, Pancreatic Ductal / pathology
  • Cell Line, Tumor
  • DNA Methylation
  • Disease Progression
  • Down-Regulation
  • Epigenesis, Genetic*
  • Epithelial-Mesenchymal Transition
  • Humans
  • Mice
  • MicroRNAs / physiology*
  • Neoplasm Invasiveness
  • Pancreatic Neoplasms / etiology*
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / mortality
  • Pancreatic Neoplasms / pathology
  • Plasminogen Activator Inhibitor 1 / genetics
  • Vimentin / analysis

Substances

  • Cadherins
  • MIRN192 microRNA, human
  • MicroRNAs
  • Plasminogen Activator Inhibitor 1
  • SERPINE1 protein, human
  • Vimentin