Ligand-activated peroxisome proliferator-activated receptor-gamma protects against ischemic cerebral infarction and neuronal apoptosis by 14-3-3 epsilon upregulation

Circulation. 2009 Mar 3;119(8):1124-34. doi: 10.1161/CIRCULATIONAHA.108.812537. Epub 2009 Feb 16.

Abstract

Background: Thiazolidinediones have been reported to protect against ischemia-reperfusion injury. Their protective actions are considered to be peroxisome proliferator-activated receptor-gamma (PPAR-gamma)-dependent; however, it is unclear how PPAR-gamma activation confers resistance to ischemia-reperfusion injury.

Methods and results: We evaluated the effects of rosiglitazone or PPAR-gamma overexpression on cerebral infarction in a rat model and investigated the antiapoptotic actions in the N2-A neuroblastoma cell model. Rosiglitazone or PPAR-gamma overexpression significantly reduced infarct volume. The protective effect was abrogated by PPAR-gamma small interfering RNA. In mice with knock-in of a PPAR-gamma dominant-negative mutant, infarct volume was enhanced. Proteomic analysis revealed that brain 14-3-3epsilon was highly upregulated in rats treated with rosiglitazone. Upregulation of 14-3-3epsilon was abrogated by PPAR-gamma small interfering RNA or antagonist. Promoter analysis and chromatin immunoprecipitation revealed that rosiglitazone induced PPAR-gamma binding to specific regulatory elements on the 14-3-3epsilon promoter and thereby increased 14-3-3epsilon transcription. 14-3-3epsilon Small interfering RNA abrogated the antiapoptotic actions of rosiglitazone or PPAR-gamma overexpression, whereas 14-3-3epsilon recombinant proteins rescued brain tissues and N2-A cells from ischemia-induced damage and apoptosis. Elevated 14-3-3epsilon enhanced binding of phosphorylated Bad and protected mitochondrial membrane potential.

Conclusions: Ligand-activated PPAR-gamma confers resistance to neuronal apoptosis and cerebral infarction by driving 14-3-3epsilon transcription. 14-3-3epsilon Upregulation enhances sequestration of phosphorylated Bad and thereby suppresses apoptosis.

Publication types

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

MeSH terms

  • 14-3-3 Proteins / biosynthesis
  • 14-3-3 Proteins / genetics*
  • 14-3-3 Proteins / physiology
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / physiology*
  • Brain Ischemia / metabolism
  • Brain Ischemia / pathology
  • Brain Ischemia / prevention & control*
  • Cell Line, Tumor
  • Cerebral Infarction / metabolism
  • Cerebral Infarction / pathology
  • Cerebral Infarction / prevention & control
  • Ligands
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Neurons / drug effects
  • Neurons / metabolism*
  • Neurons / pathology
  • PPAR gamma / biosynthesis
  • PPAR gamma / genetics
  • PPAR gamma / physiology*
  • Rats
  • Rosiglitazone
  • Thiazolidinediones / pharmacology
  • Thiazolidinediones / therapeutic use
  • Transcription, Genetic / drug effects
  • Transcription, Genetic / physiology
  • Up-Regulation / drug effects
  • Up-Regulation / physiology*

Substances

  • 14-3-3 Proteins
  • Ligands
  • PPAR gamma
  • Thiazolidinediones
  • Rosiglitazone

Grants and funding