Augmentation of response to chemotherapy by microRNA-506 through regulation of RAD51 in serous ovarian cancers

J Natl Cancer Inst. 2015 May 20;107(7):djv108. doi: 10.1093/jnci/djv108. Print 2015 Jul.

Abstract

Background: Chemoresistance is a major challenge in cancer treatment. miR-506 is a potent inhibitor of the epithelial-to-mesenchymal transition (EMT), which is also associated with chemoresistance. We characterized the role of miR-506 in chemotherapy response in high-grade serous ovarian cancers.

Methods: We used Kaplan-Meier and log-rank methods to analyze the relationship between miR-506 and progression-free and overall survival in The Cancer Genome Atlas (TCGA) (n = 468) and Bagnoli (n = 130) datasets, in vitro experiments to study whether miR-506 is associated with homologous recombination, and response to chemotherapy agents. We used an orthotopic ovarian cancer mouse model (n = 10 per group) to test the effect of miR-506 on cisplatin and PARP inhibitor sensitivity. All statistical tests were two-sided.

Results: MiR-506 was associated with better response to therapy and longer progression-free and overall survival in two independent epithelial ovarian cancer patient cohorts (PFS: high vs low miR-506 expression; Bagnoli: hazard ratio [HR] = 3.06, 95% confidence interval [CI] = 1.90 to 4.70, P < .0001; TCGA: HR = 1.49, 95% CI = 1.00 to 2.25, P = 0.04). MiR-506 sensitized cells to DNA damage through directly targeting the double-strand DNA damage repair gene RAD51. Systemic delivery of miR-506 in 8-12 week old female athymic nude mice statistically significantly augmented the cisplatin and olaparib response (mean tumor weight ± SD, control miRNA plus cisplatin vs miR-506 plus cisplatin: 0.36±0.05g vs 0.07±0.02g, P < .001; control miRNA plus olaparib vs miR-506 plus olaparib: 0.32±0.13g vs 0.05±0.02g, P = .045, respectively), thus recapitulating the clinical observation.

Conclusions: MiR-506 is a robust clinical marker for chemotherapy response and survival in serous ovarian cancers and has important therapeutic value in sensitizing cancer cells to chemotherapy.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols / administration & dosage
  • Antineoplastic Combined Chemotherapy Protocols / pharmacology*
  • Biomarkers, Tumor / metabolism*
  • Blotting, Western
  • Cell Line, Tumor
  • Cisplatin / administration & dosage
  • Cisplatin / pharmacology
  • Cystadenocarcinoma, Serous / drug therapy*
  • Cystadenocarcinoma, Serous / genetics
  • Cystadenocarcinoma, Serous / metabolism
  • Cystadenocarcinoma, Serous / pathology
  • DNA Damage / drug effects*
  • DNA Damage / genetics
  • DNA, Neoplasm / drug effects*
  • Drug Synergism
  • Epithelial-Mesenchymal Transition
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • HeLa Cells
  • Humans
  • Immunohistochemistry
  • Kaplan-Meier Estimate
  • Mice
  • Mice, Nude
  • MicroRNAs / metabolism
  • MicroRNAs / pharmacology*
  • Microscopy, Fluorescence
  • Neoplasm Grading
  • Neoplasm Transplantation
  • Neoplasms, Experimental
  • Odds Ratio
  • Ovarian Neoplasms / drug therapy*
  • Ovarian Neoplasms / genetics
  • Ovarian Neoplasms / metabolism
  • Ovarian Neoplasms / pathology
  • Phthalazines / administration & dosage
  • Phthalazines / pharmacology
  • Piperazines / administration & dosage
  • Piperazines / pharmacology
  • Poly(ADP-ribose) Polymerase Inhibitors
  • Rad51 Recombinase / drug effects
  • Rad51 Recombinase / metabolism*
  • Real-Time Polymerase Chain Reaction
  • Tissue Array Analysis
  • Tumor Stem Cell Assay

Substances

  • Biomarkers, Tumor
  • DNA, Neoplasm
  • MIRN506 microRNA, human
  • MicroRNAs
  • Phthalazines
  • Piperazines
  • Poly(ADP-ribose) Polymerase Inhibitors
  • RAD51 protein, human
  • Rad51 Recombinase
  • Cisplatin
  • olaparib