Dicer loss and recovery induce an oncogenic switch driven by transcriptional activation of the oncofetal Imp1-3 family

Genes Dev. 2017 Apr 1;31(7):674-687. doi: 10.1101/gad.296301.117.

Abstract

MicroRNAs (miRNAs) are post-transcriptional regulators of gene expression critical for organismal viability. Changes in miRNA activity are common in cancer, but how these changes relate to subsequent alterations in transcription and the process of tumorigenesis is not well understood. Here, we report a deep transcriptional, oncogenic network regulated by miRNAs. We present analysis of the gene expression and phenotypic changes associated with global miRNA restoration in miRNA-deficient fibroblasts. This analysis uncovers a miRNA-repressed network containing oncofetal genes Imp1, Imp2, and Imp3 (Imp1-3) that is up-regulated primarily transcriptionally >100-fold upon Dicer loss and is resistant to resilencing by complete restoration of miRNA activity. This Dicer-resistant epigenetic switch confers tumorigenicity to these cells. Let-7 targets Imp1-3 are required for this tumorigenicity and feed back to reinforce and sustain expression of the oncogenic network. Together, these Dicer-resistant genes constitute an mRNA expression signature that is present in numerous human cancers and is associated with poor survival.

Keywords: Dicer; Imp1–3; cancer; let-7; miRNA; oncofetal.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antigens, Neoplasm / genetics*
  • Antigens, Neoplasm / metabolism
  • Cell Transformation, Neoplastic / genetics*
  • Cells, Cultured
  • DEAD-box RNA Helicases / genetics*
  • DEAD-box RNA Helicases / physiology*
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Male
  • Mice
  • Mice, Knockout
  • MicroRNAs / genetics*
  • Oncogenes
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • Ribonuclease III / genetics*
  • Ribonuclease III / physiology*
  • Transcriptional Activation

Substances

  • Antigens, Neoplasm
  • IGF2BP2 protein, mouse
  • IMP1 protein, mouse
  • Igf2bp3 protein, mouse
  • MicroRNAs
  • RNA-Binding Proteins
  • mirnlet7 microRNA, mouse
  • oncofetal antigens
  • DICER1 protein, human
  • Dicer1 protein, mouse
  • Ribonuclease III
  • DEAD-box RNA Helicases