Therapeutic synergy between microRNA and siRNA in ovarian cancer treatment

Cancer Discov. 2013 Nov;3(11):1302-15. doi: 10.1158/2159-8290.CD-13-0159. Epub 2013 Sep 3.

Abstract

Development of improved RNA interference-based strategies is of utmost clinical importance. Although siRNA-mediated silencing of EphA2, an ovarian cancer oncogene, results in reduction of tumor growth, we present evidence that additional inhibition of EphA2 by a microRNA (miRNA) further "boosts" its antitumor effects. We identified miR-520d-3p as a tumor suppressor upstream of EphA2, whose expression correlated with favorable outcomes in two independent patient cohorts comprising 647 patients. Restoration of miR-520d-3p prominently decreased EphA2 protein levels, and suppressed tumor growth and migration/invasion both in vitro and in vivo. Dual inhibition of EphA2 in vivo using 1,2-dioleoyl-sn-glycero-3-phosphatidylcholine (DOPC) nanoliposomes loaded with miR-520d-3p and EphA2 siRNA showed synergistic antitumor efficiency and greater therapeutic efficacy than either monotherapy alone. This synergy is at least in part due to miR-520d-3p targeting EphB2, another Eph receptor. Our data emphasize the feasibility of combined miRNA-siRNA therapy, and will have broad implications for innovative gene silencing therapies for cancer and other diseases.

Significance: This study addresses a new concept of RNA inhibition therapy by combining miRNA and siRNA in nanoliposomal particles to target oncogenic pathways altered in ovarian cancer. Combined targeting of the Eph pathway using EphA2-targeting siRNA and the tumor suppressor miR-520d-3p exhibits remarkable therapeutic synergy and enhanced tumor suppression in vitro and in vivo compared with either monotherapy alone.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use*
  • Cell Line, Tumor
  • Cohort Studies
  • Drug Therapy, Combination
  • Female
  • Gene Silencing
  • Humans
  • Mice
  • Mice, Nude
  • MicroRNAs / pharmacology
  • MicroRNAs / therapeutic use*
  • Molecular Targeted Therapy
  • Ovarian Neoplasms / drug therapy*
  • Ovarian Neoplasms / metabolism
  • Ovarian Neoplasms / pathology
  • Phosphatidylcholines / pharmacology
  • RNA, Small Interfering / pharmacology
  • RNA, Small Interfering / therapeutic use*
  • Receptor, EphA2 / antagonists & inhibitors*
  • Receptor, EphA2 / genetics
  • Receptor, EphA2 / metabolism
  • Receptor, EphB2 / antagonists & inhibitors*
  • Receptor, EphB2 / genetics
  • Receptor, EphB2 / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • MIRN520 microRNA, human
  • MicroRNAs
  • Phosphatidylcholines
  • RNA, Small Interfering
  • Receptor, EphA2
  • Receptor, EphB2
  • 1,2-oleoylphosphatidylcholine