FTO mediates cell-autonomous effects on adipogenesis and adipocyte lipid content by regulating gene expression via 6mA DNA modifications

J Lipid Res. 2018 Aug;59(8):1446-1460. doi: 10.1194/jlr.M085555. Epub 2018 Jun 22.

Abstract

SNPs in the first intron of α-ketoglutarate-dependent dioxygenase (FTO) convey effects on adiposity by mechanisms that remain unclear, but appear to include modulation of expression of FTO itself, as well as other genes in cisFTO expression is lower in fibroblasts and iPSC-derived neurons of individuals segregating for FTO obesity risk alleles. We employed in vitro adipogenesis models to investigate the molecular mechanisms by which Fto affects adipocyte development and function. Fto expression was upregulated during adipogenesis, and was required for the maintenance of CEBPB and Cebpd/CEBPD expression in murine and human adipocytes in vitro. Fto knockdown decreased the number of 3T3-L1 cells that differentiated into adipocytes as well as the amount of lipid per mature adipocyte. This effect on adipocyte programming was conveyed, in part, by modulation of CCAAT enhancer binding protein (C/ebp)β-regulated transcription. We found that Fto also affected Cebpd transcription by demethylating DNA N6-methyldeoxyadenosine in the Cebpd promoter. Fto is permissive for adipogenesis and promotes maintenance of lipid content in mature adipocytes by enabling C/ebpβ-driven transcription and expression of Cebpd These findings are consistent with the loss of fat mass in mice segregating for a dominant-negative Fto allele.

Keywords: adipose tissue; diabetes; genetics; messenger ribonucleic acid; methylation; obesity; α-ketoglutarate-dependent dioxygenase.

Publication types

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

MeSH terms

  • 3T3-L1 Cells
  • Adenosine / analogs & derivatives*
  • Adenosine / metabolism
  • Adipocytes / cytology*
  • Adipocytes / metabolism
  • Adipogenesis / genetics*
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO / deficiency
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO / genetics
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO / metabolism*
  • Animals
  • DNA / genetics
  • DNA / metabolism*
  • DNA Methylation
  • Extracellular Matrix Proteins / metabolism
  • Gene Knockdown Techniques
  • Lipid Metabolism / genetics*
  • Mice
  • Neoplasm Proteins / metabolism
  • Phosphorylation / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3 / metabolism
  • Signal Transduction / genetics

Substances

  • Extracellular Matrix Proteins
  • Neoplasm Proteins
  • SPON2 protein, human
  • DNA
  • N-methyladenosine
  • FTO protein, mouse
  • Alpha-Ketoglutarate-Dependent Dioxygenase FTO
  • FTO protein, human
  • Proto-Oncogene Proteins c-akt
  • Receptor-Like Protein Tyrosine Phosphatases, Class 3
  • Adenosine