Chitosan nanoparticle-mediated delivery of miRNA-34a decreases prostate tumor growth in the bone and its expression induces non-canonical autophagy

Oncotarget. 2015 Oct 6;6(30):29161-77. doi: 10.18632/oncotarget.4971.

Abstract

While several new therapies are FDA-approved for bone-metastatic prostate cancer (PCa), patient survival has only improved marginally. Here, we report that chitosan nanoparticle-mediated delivery of miR-34a, a tumor suppressive microRNA that downregulates multiple gene products involved in PCa progression and metastasis, inhibited prostate tumor growth and preserved bone integrity in a xenograft model representative of established PCa bone metastasis. Expression of miR-34a induced apoptosis in PCa cells, and, in accord with downregulation of targets associated with PCa growth, including MET and Axl and c-Myc, also induced a form of non-canonical autophagy that is independent of Beclin-1, ATG4, ATG5 and ATG7. MiR-34a-induced autophagy is anti-proliferative in prostate cancer cells, as blocking apoptosis still resulted in growth inhibition of tumor cells. Thus, combined effects of autophagy and apoptosis are responsible for miR-34a-mediated prostate tumor growth inhibition, and have translational impact, as this non-canonical form of autophagy is tumor inhibitory. Together, these results provide a new understanding of the biological effects of miR-34a and highlight the clinical potential for miR-34a delivery as a treatment for bone metastatic prostate cancer.

Keywords: apoptosis; autophagy; bone metastasis; miR-34a; prostate cancer.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Autophagy*
  • Bone Neoplasms / genetics
  • Bone Neoplasms / metabolism
  • Bone Neoplasms / prevention & control*
  • Bone Neoplasms / secondary
  • Cell Line, Tumor
  • Cell Proliferation
  • Chitosan / chemistry*
  • Gene Expression Regulation, Neoplastic
  • Gene Transfer Techniques*
  • Genetic Therapy / methods*
  • Humans
  • Male
  • Mice, Nude
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Nanoparticles*
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology
  • Prostatic Neoplasms / therapy*
  • RNA Interference
  • Signal Transduction
  • Time Factors
  • Transfection
  • Tumor Burden
  • X-Ray Microtomography
  • Xenograft Model Antitumor Assays

Substances

  • MIRN34 microRNA, human
  • MicroRNAs
  • Chitosan