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Volume 16, Number 19, Issue of October 1, 1996 pp. 6125-6133
Copyright ©1996 Society for Neuroscience

Mitochondrial Dysfunction Is a Primary Event in Glutamate Neurotoxicity

Received May 15, 1996; revised July 17, 1996; accepted July 19, 1996.

Alejandro F. Schinder1, Eric C. Olson1, Nicholas C. Spitzer1, 2, and Mauricio Montal1

1 Department of Biology and 2 Center for Molecular Genetics, University of California at San Diego, La Jolla, California 92093-0366

Excitotoxic neuronal death, associated with neurodegenerative disorders and hypoxic insults, results from excessive exposure to excitatory neurotransmitters. Glutamate neurotoxicity is triggered primarily by massive Ca2+ influx arising from overstimulation of the NMDA subtype of glutamate receptors. The underlying mechanisms, however, remain elusive. We have tested the hypothesis that mitochondria are primary targets in excitotoxicity by confocal imaging of intracellular Ca2+ ([Ca2+]i) and mitochondrial membrane potential (Delta Psi ) on cultured rat hippocampal neurons. Sustained activation of NMDA receptors (20 min) elicits reversible elevation of [Ca2+]i. Longer activation (50 min) renders elevation of [Ca2+]i irreversible (Ca2+ overload). Susceptibility to NMDA-induced Ca2+ overload is increased when the 20 min stimuli are applied to neurons pretreated with electron transport chain inhibitors, thereby implicating mitochondria in [Ca2+]i homeostasis during excitotoxic challenges. Remarkably, Delta Psi exhibits prominent and persistent depolarization in response to NMDA, which closely parallels the incidence of neuronal death. Blockade of the mitochondrial permeability transition pore by cyclosporin A allows complete recovery of Delta Psi and prevents cell death. These results suggest that early mitochondrial damage plays a key role in induction of glutamate neurotoxicity.

Key words: calcium; cyclosporin; excitotoxicity; imaging; mitochondria; NMDA receptor; neuronal death




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