Genetic mutation of p53 and suppression of the miR-17∼92 cluster are synthetic lethal in non-small cell lung cancer due to upregulation of vitamin D Signaling

Cancer Res. 2015 Feb 15;75(4):666-75. doi: 10.1158/0008-5472.CAN-14-1329. Epub 2014 Dec 17.

Abstract

Lung cancer is the leading cause of cancer-related fatalities. Recent success developing genotypically targeted therapies, with potency only in well-defined subpopulations of tumors, suggests a path to improving patient survival. We used a library of oligonucleotide inhibitors of microRNAs, a class of posttranscriptional gene regulators, to identify novel synthetic lethal interactions between miRNA inhibition and molecular mechanisms in non-small cell lung cancer (NSCLC). Two inhibitors, those for miR-92a and miR-1226*, produced a toxicity distribution across a panel of 27 cell lines that correlated with loss of p53 protein expression. Notably, depletion of p53 was sufficient to confer sensitivity to otherwise resistant telomerase-immortalized bronchial epithelial cells. We found that both miR inhibitors cause sequence-specific downregulation of the miR-17∼92 polycistron, and this downregulation was toxic only in the context of p53 loss. Mechanistic studies indicated that the selective toxicity of miR-17∼92 polycistron inactivation was the consequence of derepression of vitamin D signaling via suppression of CYP24A1, a rate-limiting enzyme in the 1α,25-dihydroxyvitamin D3 metabolic pathway. Of note, high CYP24A1 expression significantly correlated with poor patient outcome in multiple lung cancer cohorts. Our results indicate that the screening approach used in this study can identify clinically relevant synthetic lethal interactions and that vitamin D receptor agonists may show enhanced efficacy in p53-negative lung cancer patients.

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

  • Carcinoma, Non-Small-Cell Lung / genetics*
  • Carcinoma, Non-Small-Cell Lung / pathology
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic
  • Humans
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / biosynthesis
  • Mutation
  • Receptors, Calcitriol / biosynthesis*
  • Receptors, Calcitriol / genetics
  • Signal Transduction
  • Telomerase / genetics
  • Tumor Suppressor Protein p53 / biosynthesis*
  • Tumor Suppressor Protein p53 / genetics
  • Vitamin D / genetics*
  • Vitamin D / metabolism
  • Vitamin D3 24-Hydroxylase / biosynthesis

Substances

  • MIRN1226 microRNA, human
  • MIRN92 microRNA, human
  • MicroRNAs
  • Receptors, Calcitriol
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • Vitamin D
  • CYP24A1 protein, human
  • Vitamin D3 24-Hydroxylase
  • Telomerase