Potentiation of 3-hydroxyglutarate neurotoxicity following induction of astrocytic iNOS in neonatal rat hippocampal cultures

Eur J Neurosci. 2001 Jun;13(11):2115-22. doi: 10.1046/j.0953-816x.2001.01595.x.

Abstract

Neuronal damage in glutaryl-CoA dehydrogenase deficiency (GDD) has previously been addressed to N-methyl-D-aspartate (NMDA) receptor-mediated neurotoxicity of the accumulating neurotoxic metabolite 3-hydroxyglutarate. However, acute encephalopathic crises in GDD patients are typically precipitated by febrile illness or even routine vaccinations, suggesting a potentiating role of inflammatory cytokines. In the present study we investigated the effect of interleukin-1beta and interferon-gamma on 3-hydroxyglutarate toxicity in rat cortical astrocyte cultures and neonatal rat hippocampal cultures. A cotreatment of both culture systems with interleukin-1beta and interferon-gamma induced the protein expression of astrocytic inducible nitric oxide synthase (iNOS), resulting in increased nitric oxide (NO) production. Cytokine pretreatment alone had no effect on cell viability but potentiated 3-hydroxyglutarate neurotoxicity. NOS inhibition by aminoguanidine and L-NAME prevented an iNOS-mediated potentiation of 3-hydroxyglutarate neurotoxicity but failed to protect neurons against 3-hydroxyglutarate alone. In contrast, superoxide dismutase/catalase as well as MK-801 prevented toxicity of 3-hydroxyglutarate alone as well as its potentiation by iNOS, supporting a central role of NMDA receptor stimulation with subsequently increased superoxide anion production. It is concluded that the potentiation of 3-hydroxyglutarate neurotoxicity is most probably due to an induction of astrocytic iNOS and concomitantly increased NO production, enabling enhanced peroxynitrite formation. Thus, we provide evidence for a neuroimmunological approach to the precipitation of acute encephalopathic crises in GDD by inflammatory cytokines.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Astrocytes / drug effects*
  • Astrocytes / enzymology
  • Astrocytes / pathology
  • Brain Diseases, Metabolic, Inborn / enzymology*
  • Brain Diseases, Metabolic, Inborn / pathology
  • Brain Diseases, Metabolic, Inborn / physiopathology
  • Cell Survival / drug effects
  • Cell Survival / physiology
  • Cells, Cultured / drug effects
  • Cells, Cultured / enzymology
  • Cells, Cultured / pathology
  • Cerebral Cortex / drug effects
  • Cerebral Cortex / enzymology
  • Cerebral Cortex / pathology
  • Cytokines / metabolism*
  • Cytokines / pharmacology
  • Drug Interactions / physiology
  • Enzyme Inhibitors / pharmacology
  • Glutarates / metabolism*
  • Glutarates / pharmacology
  • Glutaryl-CoA Dehydrogenase
  • Hippocampus / drug effects
  • Hippocampus / enzymology
  • Hippocampus / pathology
  • Interferon-gamma / metabolism
  • Interferon-gamma / pharmacology
  • Interleukin-1 / metabolism
  • Interleukin-1 / pharmacology
  • Neurons / drug effects
  • Neurons / enzymology
  • Neurons / pathology
  • Neuroprotective Agents / pharmacology
  • Neurotoxins / metabolism*
  • Neurotoxins / pharmacology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / biosynthesis*
  • Nitric Oxide Synthase / drug effects
  • Oxidoreductases / deficiency*
  • Oxidoreductases Acting on CH-CH Group Donors*
  • Rats
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism

Substances

  • 3-hydroxyglutaric acid
  • Cytokines
  • Enzyme Inhibitors
  • Glutarates
  • Interleukin-1
  • Neuroprotective Agents
  • Neurotoxins
  • Receptors, N-Methyl-D-Aspartate
  • Nitric Oxide
  • Interferon-gamma
  • Oxidoreductases
  • Nitric Oxide Synthase
  • Oxidoreductases Acting on CH-CH Group Donors
  • Glutaryl-CoA Dehydrogenase