MeCP2 reinforces STAT3 signaling and the generation of effector CD4+ T cells by promoting miR-124-mediated suppression of SOCS5

Sci Signal. 2014 Mar 11;7(316):ra25. doi: 10.1126/scisignal.2004824.

Abstract

Methyl CpG binding protein 2 (MeCP2) is an X-linked, multifunctional epigenetic regulator that is best known for its role in the neurological disorder Rett syndrome; however, it is also linked to multiple autoimmune disorders. We examined a potential role for MeCP2 in regulating the responses of CD4+ T cells to stimulation with antigen. MeCP2 was indispensable for the differentiation of naïve CD4+ T cells into T helper type 1 (T(H)1) and T(H)17 cells and for T(H)1- or T(H)17-mediated pathologies in vitro and in vivo. Loss of MeCP2 in CD4+ T cells impaired the expression of the microRNA (miR) miR-124 and consequently relieved miR-124-mediated repression of the translation of suppressor of cytokine signaling 5 (Socs5) mRNA. The resulting accumulation of SOCS5 inhibited the cytokine-dependent activation of signal transducer and activator of transcription 1 (STAT1) and STAT3, which are necessary for the differentiation of T(H)1 and T(H)17 cells, respectively. Upon silencing of MeCP2, primary neurons and astrocytes also failed to respond properly to STAT3-dependent signaling stimulated by neurotrophic factors. Together, these findings suggest that the regulation of STAT3 signaling may represent a common etiology underpinning the roles of MeCP2 in both the nervous and immune systems.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Benzothiazoles
  • Blotting, Western
  • CD4-Positive T-Lymphocytes / immunology*
  • Chromatin Immunoprecipitation
  • Cytokines / metabolism
  • DNA Methylation
  • Diamines
  • Gene Expression Regulation / immunology*
  • Histological Techniques
  • Luciferases
  • Methyl-CpG-Binding Protein 2 / genetics
  • Methyl-CpG-Binding Protein 2 / metabolism*
  • Mice
  • Mice, Knockout
  • MicroRNAs / metabolism*
  • Organic Chemicals
  • Polymerase Chain Reaction
  • Quinolines
  • STAT3 Transcription Factor / metabolism*
  • Signal Transduction / immunology*
  • Suppressor of Cytokine Signaling Proteins / metabolism*

Substances

  • Benzothiazoles
  • Cytokines
  • Diamines
  • Mecp2 protein, mouse
  • Methyl-CpG-Binding Protein 2
  • MicroRNAs
  • Mirn124 microRNA, mouse
  • Organic Chemicals
  • Quinolines
  • STAT3 Transcription Factor
  • Socs5 protein, mouse
  • Stat3 protein, mouse
  • Suppressor of Cytokine Signaling Proteins
  • SYBR Green I
  • Luciferases