Foxp3 expression in induced regulatory T cells is stabilized by C/EBP in inflammatory environments

EMBO Rep. 2018 Dec;19(12):e45995. doi: 10.15252/embr.201845995. Epub 2018 Oct 22.

Abstract

Proper control of immune responses by Foxp3+ regulatory T cells at inflamed sites is crucial for the prevention of immunopathology. TGF-β-induced Foxp3+ regulatory T (Treg) cells are generated in inflammatory environments as well as in steady-state conditions. Inflammatory cytokines such as IFN-γ and IL-4 have an antagonistic effect on Treg cell conversion. However, it is not known how naive CD4+ T cells overcome the inhibitory environment in inflamed sites to differentiate into Treg cells. Here, we show that CCAAT/enhancer-binding protein (C/EBP) functions as a safeguard that enhances Treg cell generation by dampening the inhibitory effect of IFN-γ and IL-4 on Foxp3 expression. We find that C/EBPβ is induced by retinoic acid and binds to the methyl-CRE sequence in the Foxp3 TSDR to sustain its expression. C/EBPβ-transduced iTreg cells show more potent suppressive activity in mouse disease models. We also reveal that C/EBPβ-transduced human iTreg cells exhibit more enhanced suppressor function. These results establish C/EBP as a new molecular target for enhancing the formation and stability of Treg cells in inflammatory environments.

Keywords: C/EBP; Foxp3; iTreg; inflammatory cytokines.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Base Sequence
  • CCAAT-Enhancer-Binding Proteins / metabolism*
  • Colitis / immunology
  • Colitis / pathology
  • Cytokines / pharmacology
  • DNA Methylation / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Forkhead Transcription Factors / metabolism*
  • Humans
  • Inflammation / metabolism*
  • Inflammation / pathology*
  • Mice, Transgenic
  • Protein Binding
  • Response Elements / genetics
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / metabolism*
  • Tretinoin / pharmacology
  • Up-Regulation / drug effects

Substances

  • CCAAT-Enhancer-Binding Proteins
  • Cytokines
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Tretinoin