Control of Foxp3 stability through modulation of TET activity

J Exp Med. 2016 Mar 7;213(3):377-97. doi: 10.1084/jem.20151438. Epub 2016 Feb 22.

Abstract

Ten-eleven translocation (TET) enzymes oxidize 5-methylcytosine (5mC) to 5-hydroxymethylcytosine and other oxidized methylcytosines, intermediates in DNA demethylation. In this study, we examine the role of TET proteins in regulating Foxp3, a transcription factor essential for the development and function of regulatory T cells (T reg cells), a distinct lineage of CD4(+) T cells that prevent autoimmunity and maintain immune homeostasis. We show that during T reg cell development in the thymus, TET proteins mediate the loss of 5mC in T reg cell-specific hypomethylated regions, including CNS1 and CNS2, intronic cis-regulatory elements in the Foxp3 locus. Similar to CNS2-deficient T reg cells, the stability of Foxp3 expression is markedly compromised in T reg cells from Tet2/Tet3 double-deficient mice. Vitamin C potentiates TET activity and acts through Tet2/Tet3 to increase the stability of Foxp3 expression in TGF-β-induced T reg cells. Our data suggest that targeting TET enzymes with small molecule activators such as vitamin C might increase induced T reg cell efficacy.

Publication types

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

MeSH terms

  • 5-Methylcytosine / metabolism
  • Animals
  • Ascorbic Acid / pharmacology
  • Cell Differentiation / drug effects
  • Cytosine / metabolism
  • DNA Methylation / drug effects
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / metabolism*
  • Dioxygenases
  • Forkhead Transcription Factors / metabolism*
  • HEK293 Cells
  • Humans
  • Male
  • Mice
  • Protein Stability / drug effects
  • Proto-Oncogene Proteins / deficiency
  • Proto-Oncogene Proteins / metabolism*
  • T-Lymphocytes, Regulatory / immunology

Substances

  • DNA-Binding Proteins
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Proto-Oncogene Proteins
  • 5-Methylcytosine
  • Cytosine
  • Dioxygenases
  • Tet2 protein, mouse
  • Tet3 protein, mouse
  • Ascorbic Acid