Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect

J Biol Chem. 2004 Sep 24;279(39):40462-9. doi: 10.1074/jbc.M407258200. Epub 2004 Jul 20.

Abstract

Recent reports emphasize the importance of mitochondria in white adipose tissue biology. In addition to their crucial role in energy homeostasis, mitochondria are the main site of reactive oxygen species generation. When moderately produced, they function as physiological signaling molecules. Thus, mitochondrial reactive oxygen species trigger hypoxia-dependent gene expression. Therefore the present study tested the implication of mitochondrial reactive oxygen species in adipocyte differentiation and their putative role in the hypoxia-dependent effect on this differentiation. Pharmacological manipulations of mitochondrial reactive oxygen species generation demonstrate a very strong and negative correlation between changes in mitochondrial reactive oxygen species and adipocyte differentiation of 3T3-F442A preadipocytes. Moreover, mitochondrial reactive oxygen species positively and specifically control expression of the adipogenic repressor CHOP-10/GADD153. Hypoxia (1% O2) strongly increased reactive oxygen species generation, hypoxia-inducible factor-1 and CHOP-10/GADD153 expression, and inhibited adipocyte differentiation. All of these hypoxia-dependent effects were partly prevented by antioxidants. By using hypoxia-inducible factor-1alpha (HIF-1alpha)-deficient mouse embryonic fibroblasts, HIF-1alpha was shown not to be required for hypoxia-mediated CHOP-10/GADD153 induction. Moreover, the comparison of hypoxia and CoCl2 effects on adipocyte differentiation of wild type or HIF-1alpha deficient mouse embryonic fibroblasts suggests the existence of at least two pathways dependent or not on the presence of HIF-1alpha. Together, these data demonstrate that mitochondrial reactive oxygen species control CHOP-10/GADD153 expression, are antiadipogenic signaling molecules, and trigger hypoxia-dependent inhibition of adipocyte differentiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 3T3 Cells
  • Adipocytes / metabolism*
  • Animals
  • Antimycin A / analogs & derivatives*
  • Antimycin A / pharmacology
  • Antioxidants / pharmacology
  • Blotting, Northern
  • Blotting, Western
  • CCAAT-Enhancer-Binding Proteins / biosynthesis*
  • Cell Differentiation
  • Fibroblasts / metabolism
  • Glycerolphosphate Dehydrogenase / metabolism
  • Hypoxia*
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Mice
  • Mitochondria / metabolism*
  • Mitochondria / pathology
  • Oxygen / metabolism
  • RNA / metabolism
  • Reactive Oxygen Species*
  • Signal Transduction
  • Time Factors
  • Transcription Factor CHOP
  • Transcription Factors / biosynthesis*
  • Transcription Factors / metabolism
  • Triglycerides / metabolism

Substances

  • Antioxidants
  • CCAAT-Enhancer-Binding Proteins
  • Ddit3 protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Reactive Oxygen Species
  • Transcription Factors
  • Triglycerides
  • antimycin
  • Transcription Factor CHOP
  • RNA
  • Antimycin A
  • Glycerolphosphate Dehydrogenase
  • Oxygen