Loss of miR-100 enhances migration, invasion, epithelial-mesenchymal transition and stemness properties in prostate cancer cells through targeting Argonaute 2

Int J Oncol. 2014 Jul;45(1):362-72. doi: 10.3892/ijo.2014.2413. Epub 2014 Apr 30.

Abstract

Evidence in literature has demonstrated that some microRNAs (miRNAs) play a pivotal role in most solid tumor metastasis. Previous studies have showed that miR-100 is downregulated in human prostate cancer tissue compared to normal prostate and also significantly decreased in bone metastatic prostate cancer samples compared with primary prostate cancer. Argonaute 2 (AGO2) is the core effector protein of the miRNA-induced silencing complex and overexpression of AGO2 might enhance tumor metastasis. However, it is unknown whether and how miR-100 and AGO2 regulates metastasis of prostate cancer. Here, we report that miR-100 negatively regulated migration, invasion, epithelial-mesenchymal transition (EMT), colony formation, spheroid formation and expression of the stemness factors c-Myc, Oct4 and Klf4 in PC-3 and DU145 cells. Furthermore, miR-100 expression was negatively correlated with bone metastasis of prostate cancer patients. Notably, luciferase assay showed that AGO2 was a direct target of miR-100. Downregulation of AGO2 repressed migration, invasion, EMT and stemness of prostate cancer cells, and reversed the effects seen with miR-100 downregulation. Downregulation of AGO2 enhanced expression of miR-34a and miR-125b which can suppress migration, invasion, EMT and stemness of cancer cells. Taken together, our findings indicate that loss of miR-100 promotes the metastatic ability of prostate cancer cells at least partially by upregulating AGO2 expression through modulating migration, invasion, EMT and stemness of cancer cells, and suggest that miR-100/AGO2 may play an important role in regulating the metastasis of prostate cancer and is a potential target of prevention and therapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Aged, 80 and over
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism*
  • Bone Neoplasms / pathology
  • Bone Neoplasms / secondary*
  • Cell Line, Tumor
  • Epithelial-Mesenchymal Transition*
  • Humans
  • Kruppel-Like Factor 4
  • Male
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Neoplasm Invasiveness / genetics*
  • Neoplasm Invasiveness / pathology
  • Neoplastic Stem Cells / metabolism
  • Neoplastic Stem Cells / pathology*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / pathology*

Substances

  • AGO2 protein, human
  • Argonaute Proteins
  • KLF4 protein, human
  • Kruppel-Like Factor 4
  • MIRN100 microRNA, human
  • MIRN1225 microRNA, human
  • MIRN34 microRNA, human
  • MicroRNAs