miR-17-92 cluster targets phosphatase and tensin homology and Ikaros Family Zinc Finger 4 to promote TH17-mediated inflammation

J Biol Chem. 2014 May 2;289(18):12446-56. doi: 10.1074/jbc.M114.550723. Epub 2014 Mar 18.

Abstract

The miR-17-92 cluster regulates a broad spectrum of biological processes of T cell immunity. This cluster was found to facilitate T cell proliferation, enhance antitumor activities and promote T cell-dependent antibody responses. However, little is known about the role of this miRNA cluster in the development of autoimmune diseases. Multiple sclerosis is a neuro-destructive autoimmune disease caused by the pathogenicity of TH17 cells, whose differentiation is tightly controlled by a variety of transcriptional and post-transcriptional regulators. Our study unveils the critical role of miR-17-92 in TH17 differentiation: T cell-specific miR-17-92 deficiency reduced TH17 differentiation and ameliorated experimental autoimmune encephalomyelitis (EAE) symptoms. We demonstrated that miR-17 and miR-19b are the two miRNAs in this cluster responsible for promoting TH17 responses. MiR-19b represses the expression of Phosphatase and Tensin Homology (PTEN), thereby augmenting the PI3K-AKT-mTOR axis essential for proper TH17 differentiation. Meanwhile, miR-17 enhances TH17 polarization by inhibiting a novel target, Ikaros Family Zinc Finger 4 (IKZF4). By establishing the miR-17-92 cluster as a key driver of TH17 responses, our data identify this miRNA cluster as a potential therapeutic target for the clinical intervention of multiple sclerosis.

Keywords: Autoimmunity; Cell Differentiation; IKZF4; Inflammation; MicroRNA; Pten; T Cell; Th17; miR-17-92.

Publication types

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

MeSH terms

  • Animals
  • Blotting, Western
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology
  • Carrier Proteins / metabolism
  • Cell Differentiation / genetics
  • Cell Differentiation / immunology
  • Cells, Cultured
  • Colitis / genetics
  • Colitis / immunology
  • Colitis / metabolism
  • DNA-Binding Proteins
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / metabolism
  • Flow Cytometry
  • Gene Expression Regulation / immunology
  • Ikaros Transcription Factor / genetics
  • Ikaros Transcription Factor / immunology*
  • Ikaros Transcription Factor / metabolism
  • Inflammation / genetics
  • Inflammation / immunology*
  • Inflammation / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics
  • MicroRNAs / immunology*
  • MicroRNAs / metabolism
  • Multigene Family
  • Multiple Sclerosis / genetics
  • Multiple Sclerosis / immunology
  • Multiple Sclerosis / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / immunology
  • Nerve Tissue Proteins / metabolism
  • PTEN Phosphohydrolase / genetics
  • PTEN Phosphohydrolase / immunology*
  • PTEN Phosphohydrolase / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Th17 Cells / immunology*
  • Th17 Cells / metabolism

Substances

  • Carrier Proteins
  • DNA-Binding Proteins
  • MIRN17-92 microRNA, mouse
  • MIRN19 microRNA, mouse
  • MicroRNAs
  • Mirn17 microRNA, mouse
  • Nerve Tissue Proteins
  • Zfpn1a4 protein, mouse
  • Ikaros Transcription Factor
  • PTEN Phosphohydrolase
  • Pten protein, mouse