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Volume 16, Number 18, Issue of September 15, 1996 pp. 5688-5697
Copyright ©1996 Society for Neuroscience

Mitochondrial Depolarization in Glutamate-Stimulated Neurons: An Early Signal Specific to Excitotoxin Exposure

Received April 26, 1996; revised June 26, 1996; accepted June 28, 1996.

R. James White and Ian J. Reynolds

Center for Neuroscience and Department of Pharmacology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261

A brief exposure to high concentrations of glutamate kills cultured forebrain neurons by an excitotoxic process that is dependent on Ca2+ influx through the NMDA receptor. In this study, we have measured striking changes in mitochondrial function during and immediately after intense glutamate receptor activation. Using indo-1 microfluorometry and a specific inhibitor of the mitochondrial Na+/Ca2+ exchanger, CGP-37157, we have demonstrated that mitochondria accumulate large quantities of Ca2+ during a toxic glutamate stimulus and further that Ca2+ efflux from mitochondria contributes to the prolonged [Ca2+]i elevation after glutamate removal. We then used JC-1 (5,5',6,6'-tetrachloro-1,1',3,3'-tetraethylbenzimidazolocarbocyanine iodide), a ratiometric indicator of mitochondrial membrane potential (Delta psi ), to show that Ca2+ accumulation within the organelle dissipates Delta psi . The abrupt loss of Delta psi after glutamate stimulation did not occur in the presence of MK801 or in the absence of extracellular Ca2+. The mitochondrial depolarization was also cyclosporin A-sensitive, indicating a probable role for the permeability transition pore. Hence mitochondrial Ca2+ accumulation and the subsequent permeability transition may be a critical early event specific to the NMDA receptor-mediated excitotoxic cascade.

Key words: intracellular calcium; permeability transition pore; NMDA; excitotoxicity; forebrain neurons; CGP-37157




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S. Schuchmann, W. Muller, and U. Heinemann
Altered Ca2+ Signaling and Mitochondrial Deficiencies in Hippocampal Neurons of Trisomy 16 Mice: A Model of Down's Syndrome
J. Neurosci., September 15, 1998; 18(18): 7216 - 7231.
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H. Friberg, M. Ferrand-Drake, F. Bengtsson, A. P. Halestrap, and T. Wieloch
Cyclosporin A, But Not FK 506, Protects Mitochondria and Neurons against Hypoglycemic Damage and Implicates the Mitochondrial Permeability Transition in Cell Death
J. Neurosci., July 15, 1998; 18(14): 5151 - 5159.
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D. Murchison and W. H. Griffith
Increased Calcium Buffering in Basal Forebrain Neurons During Aging
J Neurophysiol, July 1, 1998; 80(1): 350 - 364.
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J. N. Keller, Q. Guo, F. W. Holtsberg, A. J. Bruce-Keller, and M. P. Mattson
Increased Sensitivity to Mitochondrial Toxin-Induced Apoptosis in Neural Cells Expressing Mutant Presenilin-1 Is Linked to Perturbed Calcium Homeostasis and Enhanced Oxyradical Production
J. Neurosci., June 15, 1998; 18(12): 4439 - 4450.
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V. P. Bindokas, C. C. Lee, W. F. Colmers, and R. J. Miller
Changes in Mitochondrial Function Resulting from Synaptic Activity in the Rat Hippocampal Slice
J. Neurosci., June 15, 1998; 18(12): 4570 - 4587.
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 Mol. Pharmacol.Home page
T.-I Peng and J. T. Greenamyre
Privileged Access to Mitochondria of Calcium Influx through N-Methyl-D-Aspartate Receptors
Mol. Pharmacol., June 1, 1998; 53(6): 974 - 980.
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G. P. Davey, S. Peuchen, and J. B. Clark
Energy Thresholds in Brain Mitochondria. POTENTIAL INVOLVEMENT IN NEURODEGENERATION
J. Biol. Chem., May 22, 1998; 273(21): 12753 - 12757.
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K. R Hoyt, A. K Stout, J. M Cardman, and I. J Reynolds
The role of intracellular Na+ and mitochondria in buffering of kainate-induced intracellular free Ca2+ changes in rat forebrain neurones
J. Physiol., May 15, 1998; 509(1): 103 - 116.
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I. Marzo, C. Brenner, N. Zamzami, S. A. Susin, G. Beutner, D. Brdiczka, R. Remy, Z.-H. Xie, J. C. Reed, and G. Kroemer
The Permeability Transition Pore Complex: A Target for Apoptosis Regulation by Caspases and Bcl-2-related Proteins
J. Exp. Med., April 20, 1998; 187(8): 1261 - 1271.
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P. B Simpson and J. T Russell
Mitochondrial Ca2+ uptake and release influence metabotropic and ionotropic cytosolic Ca2+ responses in rat oligodendrocyte progenitors
J. Physiol., April 15, 1998; 508(2): 413 - 426.
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M. Gonzalez-Zulueta, L. M. Ensz, G. Mukhina, R. M. Lebovitz, R. M. Zwacka, J. F. Engelhardt, L. W. Oberley, V. L. Dawson, and T. M. Dawson
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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Q. Chen, J. W. Olney, P. D. Lukasiewicz, T. Almli, and C. Romano
Ca2+-Independent Excitotoxic Neurodegeneration in Isolated Retina, an Intact Neural Net: A Role for Cl- and Inhibitory Transmitters
Mol. Pharmacol., March 1, 1998; 53(3): 564 - 572.
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 Am. J. Physiol. Cell Physiol.Home page
R. A. Padua, K. T. Baron, B. Thyagarajan, C. Campbell, and S. A. Thayer
Reduced Ca2+ uptake by mitochondria in pyruvate dehydrogenase-deficient human diploid fibroblasts
Am J Physiol Cell Physiol, March 1, 1998; 274(3): C615 - C622.
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J. N. Keller, M. S. Kindy, F. W. Holtsberg, D. K. St. Clair, H.-C. Yen, A. Germeyer, S. M. Steiner, A. J. Bruce-Keller, J. B. Hutchins, and M. P. Mattson
Mitochondrial Manganese Superoxide Dismutase Prevents Neural Apoptosis and Reduces Ischemic Brain Injury: Suppression of Peroxynitrite Production, Lipid Peroxidation, and Mitochondrial Dysfunction
J. Neurosci., January 15, 1998; 18(2): 687 - 697.
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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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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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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.
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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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H. Kindmark, M. Kohler, G. Brown, R. Branstrom, O. Larsson, and P.-O. Berggren
Glucose-induced Oscillations in Cytoplasmic Free Ca2+ Concentration Precede Oscillations in Mitochondrial Membrane Potential in the Pancreatic beta -Cell
J. Biol. Chem., September 7, 2001; 276(37): 34530 - 34536.
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 Proc. Natl. Acad. Sci. USAHome page
A. Almeida, J. Almeida, J. P. Bolanos, and S. Moncada
Different responses of astrocytes and neurons to nitric oxide: The role of glycolytically generated ATP in astrocyte protection
PNAS, December 18, 2001; 98(26): 15294 - 15299.
[Abstract] [Full Text] [PDF]


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