Inhibition of glyceroneogenesis by histone deacetylase 3 contributes to lipodystrophy in mice with adipose tissue inflammation

Endocrinology. 2011 May;152(5):1829-38. doi: 10.1210/en.2010-0828. Epub 2011 Mar 15.

Abstract

We have reported that the nuclear factor-κB (NF-κB) induces chronic inflammation in the adipose tissue of p65 transgenic (Tg) mice, in which the NF-κB subunit p65 (RelA) is overexpressed from the adipocyte protein 2 (aP2) gene promoter. Tg mice suffer a mild lipodystrophy and exhibit deficiency in adipocyte differentiation. To understand molecular mechanism of the defect in adipocytes, we investigated glyceroneogenesis by examining the activity of cytosolic phosphoenolpyruvate carboxykinase (PEPCK) in adipocytes. In aP2-p65 Tg mice, Pepck expression is inhibited at both the mRNA and protein levels in adipose tissue. The mRNA reduction is a consequence of transcriptional inhibition but not alteration in mRNA stability. The Pepck gene promoter is inhibited by NF-κB, which enhances the corepressor activity through activation of histone deacetylase 3 (HDAC3) in the nucleus. HDAC3 suppresses Pepck transcription by inhibiting the transcriptional activators, peroxisome proliferator-activated receptor-γ, and cAMP response element binding protein. The NF-κB activity is abolished by Hdac3 knockdown or inhibition of HDAC3 catalytic activity. In a chromatin immunoprecipitation assay, HDAC3 interacts with peroxisome proliferator-activated receptor-γ and cAMP response element binding protein in the Pepck promoter when NF-κB is activated by TNF-α. These results suggest that HDAC3 mediates NF-κB activity to repress Pepck transcription. This mechanism is responsible for inhibition of glyceroneogenesis in adipocytes, which contributes to lipodystrophy in the aP2-p65 Tg mice.

Publication types

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

MeSH terms

  • 3T3-L1 Cells
  • Adipocytes / cytology
  • Adipocytes / drug effects
  • Adipocytes / metabolism
  • Adipose Tissue / metabolism*
  • Adipose Tissue / pathology
  • Animals
  • Blotting, Western
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • HEK293 Cells
  • Histone Deacetylase Inhibitors / pharmacology
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism*
  • Humans
  • Hydroxamic Acids / pharmacology
  • Inflammation / genetics
  • Inflammation / metabolism*
  • Lipodystrophy / genetics
  • Lipodystrophy / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • PPAR gamma / metabolism
  • Phosphoenolpyruvate Carboxylase / genetics
  • Phosphoenolpyruvate Carboxylase / metabolism*
  • Promoter Regions, Genetic / genetics
  • Protein Binding
  • RNA Interference
  • Reverse Transcriptase Polymerase Chain Reaction
  • Transcription Factor RelA / genetics
  • Transcription Factor RelA / metabolism
  • Triglycerides / biosynthesis*
  • Tumor Necrosis Factor-alpha / pharmacology

Substances

  • Creb1 protein, mouse
  • Cyclic AMP Response Element-Binding Protein
  • Histone Deacetylase Inhibitors
  • Hydroxamic Acids
  • PPAR gamma
  • Transcription Factor RelA
  • Triglycerides
  • Tumor Necrosis Factor-alpha
  • trichostatin A
  • Histone Deacetylases
  • histone deacetylase 3
  • Phosphoenolpyruvate Carboxylase