Pharmacological induction of heme oxygenase-1 by a triterpenoid protects neurons against ischemic injury

Stroke. 2012 May;43(5):1390-7. doi: 10.1161/STROKEAHA.111.647420. Epub 2012 Mar 29.

Abstract

Background and purpose: Heme oxygenase-1 (HO-1) is an inducible Phase 2 enzyme that degrades toxic heme; its role in cerebral ischemia is not fully understood. We hypothesize that chemically induced HO-1 upregulation with the novel triterpenoid CDDO-Im (2-cyano-3,12 dioxooleana-1,9 dien-28-oyl imidazoline), a robust inducer of Phase 2 genes, protects neurons against ischemic injury.

Methods: Using 3 different models of ischemia, including oxygen-glucose deprivation in neuronal cultures, global ischemia in rats, and focal ischemia in mice, we determined (1) whether CDDO-Im induces HO-1 expression and protects against ischemic injury; and (2) whether HO-1 inhibition disrupts the neuroprotective effect of CDDO-Im.

Results: CDDO-Im treatment (50-300 nmol/L) resulted in 8-fold HO-1 upregulation in cultured neurons and protected against oxygen-glucose deprivation. The protection was abolished when the cultures were transfected with nuclear factor (erythroid-derived 2) like-2-shRNA or coincubated with tin protoporphyrin IX, a specific HO-1 inhibitor. In the rat model of global ischemia, intracerebroventricular infusion of CDDO-Im (0.5-1.5 μg) augmented HO-1 expression in hippocampal neurons and resulted in significant increases in CA1 neuronal survival after global ischemia. To further strengthen the clinical relevance of the CDDO-Im treatment, we tested its effects in the mouse model of temporary focal ischemia (60 minutes). Postischemic intraperitoneal injection of CDDO-Im (10-100 μg) enhanced HO-1 expression and significantly reduced neurological dysfunction and infarct volume. Intracerebroventricular infusion of tin protoporphyrin IX reduced the neuroprotective effect of CDDO-Im against global and focal ischemia.

Conclusions: CDDO-Im confers neuroprotection against ischemic injury by upregulating HO-1, suggesting that enhance of HO-1 expression may be a legitimate strategy for therapeutic intervention of stroke.

Publication types

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

MeSH terms

  • Animals
  • Brain Infarction / pathology
  • Brain Ischemia / etiology
  • Brain Ischemia / metabolism
  • Brain Ischemia / prevention & control*
  • Cells, Cultured
  • Heme Oxygenase-1 / antagonists & inhibitors
  • Heme Oxygenase-1 / metabolism*
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Hypoxia / complications
  • Imidazoles / administration & dosage
  • Imidazoles / pharmacology*
  • Infusions, Intraventricular
  • Injections, Intraperitoneal
  • Mice
  • Models, Animal
  • NF-E2-Related Factor 2 / metabolism
  • Neurons / drug effects*
  • Neurons / metabolism*
  • Neurons / pathology
  • Oleanolic Acid / administration & dosage
  • Oleanolic Acid / analogs & derivatives*
  • Oleanolic Acid / pharmacology
  • Protective Agents / administration & dosage
  • Protective Agents / pharmacology*
  • Protoporphyrins / pharmacology
  • Rats
  • Triterpenes / administration & dosage
  • Triterpenes / pharmacology*
  • Up-Regulation / drug effects

Substances

  • 1-(2-cyano-3,12-dioxooleana-1,9-dien-28-oyl) imidazole
  • Imidazoles
  • NF-E2-Related Factor 2
  • Protective Agents
  • Protoporphyrins
  • Triterpenes
  • Oleanolic Acid
  • protoporphyrin IX
  • Heme Oxygenase-1