Mitochondrial Dysfunction Is a Primary Event in Glutamate Neurotoxicity

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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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Manganese Superoxide Dismutase Protects nNOS Neurons from NMDA and Nitric Oxide-Mediated Neurotoxicity
J. Neurosci., March 15, 1998; 18(6): 2040 - 2055.
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T. Kristian and B. K. Siesjo
Calcium in Ischemic Cell Death
Stroke, March 1, 1998; 29(3): 705 - 718.
[Abstract] [Full Text] [PDF]

H. Xiang, Y. Kinoshita, C. M. Knudson, S. J. Korsmeyer, P. A. Schwartzkroin, and R. S. Morrison
Bax Involvement in p53-Mediated Neuronal Cell Death
J. Neurosci., February 15, 1998; 18(4): 1363 - 1373.
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J. L. Perez Velazquez, M. V. Frantseva, and P. L. Carlen
In Vitro Ischemia Promotes Glutamate-Mediated Free Radical Generation and Intracellular Calcium Accumulation in Hippocampal Pyramidal Neurons
J. Neurosci., December 1, 1997; 17(23): 9085 - 9094.
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L. Zhou, A. Chomyn, G. Attardi, and C. A. Miller
Myoclonic Epilepsy and Ragged Red Fibers (MERRF) Syndrome: Selective Vulnerability of CNS Neurons Does Not Correlate with the Level of Mitochondrial tRNAlys Mutation in Individual Neuronal Isolates
J. Neurosci., October 15, 1997; 17(20): 7746 - 7753.
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S. P. Mostafapour, E. A. Lachica, and E. W Rubel
Mitochondrial Regulation of Calcium in the Avian Cochlear Nucleus
J Neurophysiol, October 1, 1997; 78(4): 1928 - 1934.
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P. Marin, K. L. Nastiuk, N. Daniel, J.-A. Girault, A. J. Czernik, J. Glowinski, A. C. Nairn, and J. Premont
Glutamate-Dependent Phosphorylation of Elongation Factor-2 and Inhibition of Protein Synthesis in Neurons
J. Neurosci., May 15, 1997; 17(10): 3445 - 3454.
[Abstract] [Full Text] [PDF]

K. M. Abdel-Hamid and M. Tymianski
Mechanisms and Effects of Intracellular Calcium Buffering on Neuronal Survival in Organotypic Hippocampal Cultures Exposed to Anoxia/Aglycemia or to Excitotoxins
J. Neurosci., May 15, 1997; 17(10): 3538 - 3553.
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Z. Pang and J. W. Geddes
Mechanisms of Cell Death Induced by the Mitochondrial Toxin 3-Nitropropionic Acid: Acute Excitotoxic Necrosis and Delayed Apoptosis
J. Neurosci., May 1, 1997; 17(9): 3064 - 3073.
[Abstract] [Full Text] [PDF]

J. T. Weber, B. A. Rzigalinski, and E. F. Ellis
Traumatic Injury of Cortical Neurons Causes Changes in Intracellular Calcium Stores and Capacitative Calcium Influx
J. Biol. Chem., January 12, 2001; 276(3): 1800 - 1807.
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M. Daniels and D. R. Brown
Astrocytes Regulate N-Methyl-D-aspartate Receptor Subunit Composition Increasing Neuronal Sensitivity to Excitotoxicity
J. Biol. Chem., June 15, 2001; 276(25): 22446 - 22452.
[Abstract] [Full Text] [PDF]