Differential regulation of the ten-eleven translocation (TET) family of dioxygenases by O-linked β-N-acetylglucosamine transferase (OGT)

J Biol Chem. 2014 Feb 28;289(9):5986-96. doi: 10.1074/jbc.M113.524140. Epub 2014 Jan 6.

Abstract

The ten-eleven translocation (TET) family of dioxygenases (TET1/2/3) converts 5-methylcytosine to 5-hydroxymethylcytosine and provides a vital mechanism for DNA demethylation. However, how TET proteins are regulated is largely unknown. Here we report that the O-linked β-GlcNAc (O-GlcNAc) transferase (OGT) is not only a major TET3-interacting protein but also regulates TET3 subcellular localization and enzymatic activity. OGT catalyzes the O-GlcNAcylation of TET3, promotes TET3 nuclear export, and, consequently, inhibits the formation of 5-hydroxymethylcytosine catalyzed by TET3. Although TET1 and TET2 also interact with and can be O-GlcNAcylated by OGT, neither their subcellular localization nor their enzymatic activity are affected by OGT. Furthermore, we show that the nuclear localization and O-GlcNAcylation of TET3 are regulated by glucose metabolism. Our study reveals the differential regulation of TET family proteins by OGT and a novel link between glucose metabolism and DNA epigenetic modification.

Keywords: DNA Methylation; Glucose Metabolism; Histone Modification; O-GlcNAcylation; Protein Export; TET3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5-Methylcytosine / analogs & derivatives
  • Active Transport, Cell Nucleus / physiology
  • Cell Nucleus / enzymology*
  • Cell Nucleus / genetics
  • Cytosine / analogs & derivatives
  • Cytosine / metabolism
  • DNA Methylation / physiology*
  • Dioxygenases / genetics
  • Dioxygenases / metabolism*
  • Glucose / genetics
  • Glucose / metabolism
  • HeLa Cells
  • Humans
  • N-Acetylglucosaminyltransferases / genetics
  • N-Acetylglucosaminyltransferases / metabolism*

Substances

  • 5-hydroxymethylcytosine
  • 5-Methylcytosine
  • Cytosine
  • Dioxygenases
  • N-Acetylglucosaminyltransferases
  • Glucose