Xenobiotic CAR Activators Induce Dlk1-Dio3 Locus Noncoding RNA Expression in Mouse Liver

Toxicol Sci. 2017 Aug 1;158(2):367-378. doi: 10.1093/toxsci/kfx104.

Abstract

Derisking xenobiotic-induced nongenotoxic carcinogenesis (NGC) represents a significant challenge during the safety assessment of chemicals and therapeutic drugs. The identification of robust mechanism-based NGC biomarkers has the potential to enhance cancer hazard identification. We previously demonstrated Constitutive Androstane Receptor (CAR) and WNT signaling-dependent up-regulation of the pluripotency associated Dlk1-Dio3 imprinted gene cluster noncoding RNAs (ncRNAs) in the liver of mice treated with tumor-promoting doses of phenobarbital (PB). Here, we have compared phenotypic, transcriptional ,and proteomic data from wild-type, CAR/PXR double knock-out and CAR/PXR double humanized mice treated with either PB or chlordane, and show that hepatic Dlk1-Dio3 locus long ncRNAs are upregulated in a CAR/PXR-dependent manner by two structurally distinct CAR activators. We further explored the specificity of Dlk1-Dio3 locus ncRNAs as hepatic NGC biomarkers in mice treated with additional compounds working through distinct NGC modes of action. We propose that up-regulation of Dlk1-Dio3 cluster ncRNAs can serve as an early biomarker for CAR activator-induced nongenotoxic hepatocarcinogenesis and thus may contribute to mechanism-based assessments of carcinogenicity risk for chemicals and novel therapeutics.

Keywords: Dlk1-Dio3 cluster; cancer risk assessment; chlordane; constitutive androstane receptor (CAR); noncoding RNAs; nongenotoxic carcinogenesis (NGC); phenobarbital.

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Calcium-Binding Proteins
  • Chlordan / toxicity
  • Constitutive Androstane Receptor
  • Gene Expression / drug effects*
  • Intercellular Signaling Peptides and Proteins / genetics*
  • Iodide Peroxidase / genetics*
  • Liver / drug effects*
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Phenobarbital / toxicity
  • RNA, Long Noncoding / genetics*
  • Receptors, Cytoplasmic and Nuclear / agonists*
  • Up-Regulation / drug effects
  • Xenobiotics / toxicity*

Substances

  • Biomarkers
  • Calcium-Binding Proteins
  • Constitutive Androstane Receptor
  • Dlk1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • RNA, Long Noncoding
  • Receptors, Cytoplasmic and Nuclear
  • Xenobiotics
  • Chlordan
  • iodothyronine deiodinase type III
  • Iodide Peroxidase
  • Phenobarbital