Peroxisome proliferator-activated receptors γ/mitochondrial uncoupling protein 2 signaling protects against seizure-induced neuronal cell death in the hippocampus following experimental status epilepticus

J Neuroinflammation. 2012 Jul 31:9:184. doi: 10.1186/1742-2094-9-184.

Abstract

Background: Status epilepticus induces subcellular changes that may lead to neuronal cell death in the hippocampus. However, the mechanism of seizure-induced neuronal cell death remains unclear. The mitochondrial uncoupling protein 2 (UCP2) is expressed in selected regions of the brain and is emerged as an endogenous neuroprotective molecule in many neurological disorders. We evaluated the neuroprotective role of UCP2 against seizure-induced hippocampal neuronal cell death under experimental status epilepticus.

Methods: In Sprague-Dawley rats, kainic acid (KA) was microinjected unilaterally into the hippocampal CA3 subfield to induce prolonged bilateral seizure activity. Oxidized protein level, translocation of Bcl-2, Bax and cytochrome c between cytosol and mitochondria, and expression of peroxisome proliferator-activated receptors γ (PPARγ) and UCP2 were examined in the hippocampal CA3 subfield following KA-induced status epilepticus. The effects of microinjection bilaterally into CA3 area of a PPARγ agonist, rosiglitazone or a PPARγ antagonist, GW9662 on UCP2 expression, induced superoxide anion (O(·2)(-)) production, oxidized protein level, mitochondrial respiratory chain enzyme activities, translocation of Bcl-2, Bax and cytochrome c, and DNA fragmentation in bilateral CA3 subfields were examined.

Results: Increased oxidized proteins and mitochondrial or cytosol translocation of Bax or cytochrome c in the hippocampal CA3 subfield was observed 3-48 h after experimental status epilepticus. Expression of PPARγ and UCP2 increased 12-48 h after KA-induced status epilepticus. Pretreatment with rosiglitazone increased UCP2 expression, reduced protein oxidation, O(·2)(-) overproduction and dysfunction of mitochondrial Complex I, hindered the translocation of Bax and cytochrome c, and reduced DNA fragmentation in the CA3 subfield. Pretreatment with GW9662 produced opposite effects.

Conclusions: Activation of PPARγ upregulated mitochondrial UCP2 expression, which decreased overproduction of reactive oxygen species, improved mitochondrial Complex I dysfunction, inhibited mitochondrial translocation of Bax and prevented cytosolic release of cytochrome c by stabilizing the mitochondrial transmembrane potential, leading to amelioration of apoptotic neuronal cell death in the hippocampus following status epilepticus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Death / physiology
  • Hippocampus / metabolism*
  • Hippocampus / pathology
  • Ion Channels / physiology*
  • Male
  • Mitochondrial Proteins / physiology*
  • Neurons / metabolism
  • Neurons / pathology*
  • PPAR gamma / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species
  • Seizures / metabolism*
  • Seizures / pathology
  • Seizures / prevention & control
  • Signal Transduction / physiology*
  • Status Epilepticus / metabolism*
  • Status Epilepticus / pathology
  • Status Epilepticus / prevention & control
  • Uncoupling Protein 2

Substances

  • Ion Channels
  • Mitochondrial Proteins
  • PPAR gamma
  • Reactive Oxygen Species
  • Ucp2 protein, rat
  • Uncoupling Protein 2