IFN induces miR-21 through a signal transducer and activator of transcription 3-dependent pathway as a suppressive negative feedback on IFN-induced apoptosis

Cancer Res. 2010 Oct 15;70(20):8108-16. doi: 10.1158/0008-5472.CAN-10-2579. Epub 2010 Sep 2.

Abstract

The microRNA miR-21 is overexpressed in many human cancers, wherein accumulating evidence indicates that it functions as an oncogene. Here, we report that the cytokine IFN rapidly induces miR-21 expression in human and mouse cells. Signal transducer and activator of transcription 3 (STAT3) was implicated in this pathway based on the lack of IFN effect on miR-21 expression in prostate cancer cells with a deletion in the STAT3 gene. STAT3 ablation abrogated IFN induction of miR-21, confirming the important role of STAT3 in regulating miR-21. Chromatin immunoprecipitation analysis showed that STAT3 directly bound the miR-21 promoter in response to IFN. Experiments in mouse embryo fibroblasts with a genetic deletion of the p65 NF-κB subunit showed that IFN-induced miR-21 expression was also dependent on NF-κB. STAT3 silencing blocked both IFN-induced p65 binding to the miR-21 promoter and p65 nuclear translocation. Thus, IFN-induced miR-21 expression is coregulated by STAT3 and NF-κB at the level of the miR-21 promoter. Several cell death regulators were identified as downstream targets of miR-21, including PTEN and Akt. Functional experiments in prostate cancer cells directly showed that miR-21 plays a critical role in suppressing IFN-induced apoptosis. Our results identify miR-21 as a novel IFN target gene that functions as a key feedback regulator of IFN-induced apoptosis.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • DNA Primers
  • DNA, Complementary / genetics
  • Feedback
  • Fibroblasts / physiology
  • Gene Silencing
  • Humans
  • Interferons / pharmacology*
  • Male
  • Mice
  • Mice, Knockout
  • MicroRNAs / genetics*
  • Prostatic Neoplasms / genetics
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / physiology
  • Transcription Factor RelA / deficiency
  • Transcription Factor RelA / genetics

Substances

  • DNA Primers
  • DNA, Complementary
  • MIRN21 microRNA, human
  • MicroRNAs
  • Rela protein, mouse
  • STAT3 Transcription Factor
  • Transcription Factor RelA
  • Interferons