Blockade of ionotropic glutamate receptors produces neuronal apoptosis through the Bax-cytochrome C-caspase pathway: the causative role of Ca2+ deficiency

J Neurochem. 2003 Apr;85(2):525-33. doi: 10.1046/j.1471-4159.2003.01724.x.

Abstract

Blockade of ionotropic glutamate receptors induces neuronal cell apoptosis. We investigated if mitochondria-mediated death signals would contribute to neuronal apoptosis following administration of glutamate antagonists. The administration of MK-801 and CNQX (MK-801/CNQX), the selective antagonists of N-methyl-d-aspartate (NMDA) and alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptors, produced widespread neuronal death in neonatal rat brain and cortical cell cultures. MK-801/CNQX-induced neuronal apoptosis was prevented by zVAD-fmk, a broad inhibitor of caspases, but insensitive to inhibitors of calpain or cathepsin D. Activation of caspase-3 was observed within 6-12 h and sustained over 36 h after exposure to MK-801/CNQX, which cleaved PHF-1 tau, the substrate for caspase-3. Activation of caspase-3 was blocked by high K+ and mimicked by BAPTA-AM, a selective Ca2+ chelator. Reducing extracellular Ca2+, but not Na+, activated caspase-3, suggesting an essential role of Ca2+ deficiency in MK-801/CNQX-induced activation of caspases. Cortical neurons treated with MK-801/CNQX triggered activation of caspase-9, release of cytochrome c from mitochondria, and translocation of Bax into mitochondria. The present study suggests that blockade of ionotropic glutamate receptors causes caspase-3-mediated neuronal apoptosis due to Ca2+ deficiency that is coupled to the sequential mitochondrial death pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 6-Cyano-7-nitroquinoxaline-2,3-dione / pharmacology
  • Animals
  • Apoptosis / drug effects
  • Apoptosis / physiology*
  • Calcium / deficiency*
  • Calcium / metabolism
  • Caspase 3
  • Caspase 9
  • Caspase Inhibitors
  • Caspases / metabolism
  • Cells, Cultured
  • Cerebral Cortex / cytology
  • Chelating Agents / pharmacology
  • Cytochrome c Group / metabolism
  • Dizocilpine Maleate / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Excitatory Amino Acid Antagonists / pharmacology
  • Mice
  • Neurons / cytology
  • Neurons / drug effects*
  • Neurons / metabolism*
  • Potassium / pharmacology
  • Protein Transport / drug effects
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-bcl-2*
  • Rats
  • Rats, Sprague-Dawley
  • Receptors, AMPA / antagonists & inhibitors
  • Receptors, AMPA / metabolism
  • Receptors, Glutamate / drug effects*
  • Receptors, Glutamate / metabolism
  • Receptors, N-Methyl-D-Aspartate / antagonists & inhibitors
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • bcl-2-Associated X Protein

Substances

  • Bax protein, mouse
  • Bax protein, rat
  • Caspase Inhibitors
  • Chelating Agents
  • Cytochrome c Group
  • Enzyme Inhibitors
  • Excitatory Amino Acid Antagonists
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Receptors, AMPA
  • Receptors, Glutamate
  • Receptors, N-Methyl-D-Aspartate
  • bcl-2-Associated X Protein
  • Dizocilpine Maleate
  • 6-Cyano-7-nitroquinoxaline-2,3-dione
  • Casp3 protein, mouse
  • Casp3 protein, rat
  • Casp9 protein, mouse
  • Casp9 protein, rat
  • Caspase 3
  • Caspase 9
  • Caspases
  • Potassium
  • Calcium