Insulin reduces cerebral ischemia/reperfusion injury in the hippocampus of diabetic rats: a role for glycogen synthase kinase-3beta

Diabetes. 2009 Jan;58(1):235-42. doi: 10.2337/db08-0691. Epub 2008 Oct 7.

Abstract

Objective: There is evidence that insulin reduces brain injury evoked by ischemia/reperfusion (I/R). However, the molecular mechanisms underlying the protective effects of insulin remain unknown. Insulin is a well-known inhibitor of glycogen synthase kinase-3beta (GSK-3beta). Here, we investigate the role of GSK-3beta inhibition on I/R-induced cerebral injury in a rat model of insulinopenic diabetes.

Research design and methods: Rats with streptozotocin-induced diabetes were subjected to 30-min occlusion of common carotid arteries followed by 1 or 24 h of reperfusion. Insulin (2-12 IU/kg i.v.) or the selective GSK-3beta inhibitor TDZD-8 (0.2-3 mg/kg i.v.) was administered during reperfusion.

Results: Insulin or TDZD-8 dramatically reduced infarct volume and levels of S100B protein, a marker of cerebral injury. Both drugs induced phosphorylation of the Ser9 residue, thereby inactivating GSK-3beta in the rat hippocampus. Insulin, but not TDZD-8, lowered blood glucose. The hippocampi of the drug-treated animals displayed reduced oxidative stress at 1 h of reperfusion as shown by the decreased generation of reactive oxygen species and lipid peroxidation. I/R-induced activation of nuclear factor-kappaB was attenuated by both drug treatments. At 24 h of reperfusion, TDZD-8 and insulin significantly reduced plasma levels of tumor necrosis factor-alpha; neutrophil infiltration, measured as myeloperoxidase activity and intercellular-adhesion-molecule-1 expression; and cyclooxygenase-2 and inducible-NO-synthase expression.

Conclusions: Acute administration of insulin or TDZD-8 reduced cerebral I/R injury in diabetic rats. We propose that the inhibitory effect on the activity of GSK-3beta contributes to the protective effect of insulin independently of any effects on blood glucose.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Glucose / metabolism
  • Blotting, Western
  • Body Weight / drug effects
  • Brain Ischemia / complications*
  • Diabetes Mellitus, Experimental / blood
  • Diabetes Mellitus, Experimental / physiopathology*
  • Enzyme-Linked Immunosorbent Assay
  • Gene Expression / drug effects
  • Glycogen Synthase Kinase 3 / genetics
  • Glycogen Synthase Kinase 3 / metabolism*
  • Hippocampus / drug effects*
  • Hippocampus / metabolism
  • Hormones / metabolism
  • Hypoglycemic Agents / pharmacology
  • Insulin / pharmacology*
  • Lipid Peroxidation / drug effects
  • Male
  • NF-kappa B / metabolism
  • Oxidative Stress / drug effects
  • Phosphorylation / drug effects
  • Rats
  • Rats, Wistar
  • Reperfusion Injury / etiology
  • Reperfusion Injury / metabolism
  • Reperfusion Injury / prevention & control*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Thiadiazoles / pharmacology
  • Tumor Necrosis Factor-alpha / blood

Substances

  • 4-benzyl-2-methyl-1,2,4-thiadiazolidine-3,5-dione
  • Blood Glucose
  • Hormones
  • Hypoglycemic Agents
  • Insulin
  • NF-kappa B
  • Thiadiazoles
  • Tumor Necrosis Factor-alpha
  • Glycogen Synthase Kinase 3