Maintenance DNA methylation is essential for regulatory T cell development and stability of suppressive function

J Clin Invest. 2020 Dec 1;130(12):6571-6587. doi: 10.1172/JCI137712.

Abstract

Tregs require Foxp3 expression and induction of a specific DNA hypomethylation signature during development, after which Tregs persist as a self-renewing population that regulates immune system activation. Whether maintenance DNA methylation is required for Treg lineage development and stability and how methylation patterns are maintained during lineage self-renewal remain unclear. Here, we demonstrate that the epigenetic regulator ubiquitin-like with plant homeodomain and RING finger domains 1 (Uhrf1) is essential for maintenance of methyl-DNA marks that stabilize Treg cellular identity by repressing effector T cell transcriptional programs. Constitutive and induced deficiency of Uhrf1 within Foxp3+ cells resulted in global yet nonuniform loss of DNA methylation, derepression of inflammatory transcriptional programs, destabilization of the Treg lineage, and spontaneous inflammation. These findings support a paradigm in which maintenance DNA methylation is required in distinct regions of the Treg genome for both lineage establishment and stability of identity and suppressive function.

Keywords: Autoimmune diseases; Autoimmunity; Epigenetics; Immunology; T cells.

Publication types

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

MeSH terms

  • Animals
  • CCAAT-Enhancer-Binding Proteins / genetics
  • CCAAT-Enhancer-Binding Proteins / immunology*
  • DNA Methylation / immunology*
  • Forkhead Transcription Factors / genetics
  • Forkhead Transcription Factors / immunology*
  • Mice
  • Mice, Transgenic
  • T-Lymphocytes, Regulatory / immunology*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / immunology*

Substances

  • CCAAT-Enhancer-Binding Proteins
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Ubiquitin-Protein Ligases
  • Uhrf1 protein, mouse