miR-154* and miR-379 in the DLK1-DIO3 microRNA mega-cluster regulate epithelial to mesenchymal transition and bone metastasis of prostate cancer

Clin Cancer Res. 2014 Dec 15;20(24):6559-69. doi: 10.1158/1078-0432.CCR-14-1784. Epub 2014 Oct 16.

Abstract

Purpose: MicroRNAs in the delta-like 1 homolog-deiodinase, iodothyronine 3 (DLK1-DIO3) cluster have been shown to be critical for embryonic development and epithelial to mesenchymal transition (EMT). DLK1-DIO3 cluster miRNAs are elevated in the serum of patients with metastatic cancer. However, the biologic functions of these miRNAs in the EMT and metastasis of cancer cells are poorly understood. We previously demonstrated the oncogenic and metastatic role of miR-409-3p/5p, a member of this cluster, in prostate cancer. In this study, we defined the role of miR-154* and miR-379, two key members of this cluster, in prostate cancer progression and bone metastasis in both cell line models and clinical specimens.

Experimental design: Genetic manipulation of miR-154* and miR-379 was performed to determine their role in tumor growth, EMT, and bone metastasis in mouse models. We determined the expression of miR-154* in prostate cancer clinical samples and bone metastasis samples using in situ hybridization and quantum dot labeling.

Results: Elevated expression of miR-154* and miR-379 was observed in bone metastatic prostate cancer cell lines and tissues, and miR-379 expression correlated with progression-free survival of patients with prostate cancer. Intracardiac inoculation (to mimic systemic dissemination) of miR-154* inhibitor-treated bone metastatic ARCaPM prostate cancer cells in mice led to decreased bone metastasis and increased survival.

Conclusion: miR-154* and miR-379 play important roles in prostate cancer biology by facilitating tumor growth, EMT, and bone metastasis. This finding has particular translational importance because miRNAs in the DLK1-DIO3 cluster can be attractive biomarkers and possible therapeutic targets to treat bone metastatic prostate cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bone Neoplasms / secondary*
  • Calcium-Binding Proteins
  • Cell Line, Tumor
  • Disease Models, Animal
  • Epithelial-Mesenchymal Transition / genetics*
  • Gene Expression
  • Gene Regulatory Networks
  • Heterografts
  • Humans
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Iodide Peroxidase / genetics*
  • Male
  • Membrane Proteins / genetics*
  • Mice
  • MicroRNAs / genetics*
  • Multigene Family
  • Neoplasm Grading
  • Neoplasm Metastasis
  • Prostatic Neoplasms / genetics*
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology*
  • RNA Interference

Substances

  • Calcium-Binding Proteins
  • DLK1 protein, human
  • Intercellular Signaling Peptides and Proteins
  • MIRN154 microRNA, human
  • MIRN379 microRNA, human
  • Membrane Proteins
  • MicroRNAs
  • iodothyronine deiodinase type III
  • Iodide Peroxidase