Loss of TLE3 promotes the mitochondrial program in beige adipocytes and improves glucose metabolism

Genes Dev. 2019 Jul 1;33(13-14):747-762. doi: 10.1101/gad.321059.118. Epub 2019 May 23.

Abstract

Prolonged cold exposure stimulates the recruitment of beige adipocytes within white adipose tissue. Beige adipocytes depend on mitochondrial oxidative phosphorylation to drive thermogenesis. The transcriptional mechanisms that promote remodeling in adipose tissue during the cold are not well understood. Here we demonstrate that the transcriptional coregulator transducin-like enhancer of split 3 (TLE3) inhibits mitochondrial gene expression in beige adipocytes. Conditional deletion of TLE3 in adipocytes promotes mitochondrial oxidative metabolism and increases energy expenditure, thereby improving glucose control. Using chromatin immunoprecipitation and deep sequencing, we found that TLE3 occupies distal enhancers in proximity to nuclear-encoded mitochondrial genes and that many of these binding sites are also enriched for early B-cell factor (EBF) transcription factors. TLE3 interacts with EBF2 and blocks its ability to promote the thermogenic transcriptional program. Collectively, these studies demonstrate that TLE3 regulates thermogenic gene expression in beige adipocytes through inhibition of EBF2 transcriptional activity. Inhibition of TLE3 may provide a novel therapeutic approach for obesity and diabetes.

Keywords: TLE3; adipocytes; beige adipocytes; development; diabetes; metabolism; thermogenesis.

Publication types

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

MeSH terms

  • Adipocytes, Beige / metabolism*
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cells, Cultured
  • Co-Repressor Proteins / genetics*
  • Co-Repressor Proteins / metabolism*
  • Diet, High-Fat
  • Energy Metabolism / genetics
  • Gene Deletion
  • Gene Expression Regulation / genetics
  • Genome-Wide Association Study
  • Glucose / metabolism*
  • Insulin Resistance / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Thermogenesis / genetics

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Co-Repressor Proteins
  • Ebf2 protein, mouse
  • Tle3 protein, mouse
  • Glucose