Mitochondrial dysfunction is a primary event in glutamate neurotoxicity

Journal of Neuroscience

Volumn 16, Issue 19, 1996, Pages 6125-6133

  Schinder, Alejandro F ^a   Olson, Eric C ^a   Spitzer, Nicholas C ^a   Montal, Mauricio ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

calcium; cyolosporin; excitotoxicity; imaging; mitochondria; neuronal death; NMDA receptor

Indexed keywords

CALCIUM ION; CITRININ; CYCLOSPORIN A; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OLIGOMYCIN; RECEPTOR SUBTYPE;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CONTROLLED STUDY; EMBRYO; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRIAL ENERGY TRANSFER; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0029810095     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-19-06125.1996     Document Type: Article

References (57)

1. Akerman KE (1978) Changes in membrane potential during calcium ion influx and efflux across the mitochondrial membrane. Biochim Biophys Acta 502:359-366.
2. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
3. Beal MF (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann Neurol 31:119-130.
4. 2+ by mitochondria. J Biol Chem 255:8663-8671.
5. Bernardi P, Broekemeier KM, Pfeiffer DR (1994) Recent progress on regulation of the mitochondrial permeability transition pore, a cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26:509-517.
6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/ superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162-7166.
7. Brouillet E, Hantraye P, Ferrante RJ, Dolan R, Leroy-Willig A, Kowall NW, Beal MF (1995) Chronic mitochondrial energy impairment produces selective striatal degeneration and abnormal choreiform movements in primates. Proc Natl Acad Sci USA 92:7105-7109.
8. Brown Jr RH (1995) Amyotrophic lateral sclerosis, recent insights from genetics and transgenic mice. Cell 80:687-692.
9. 2+ homeostasis. J Neurochem 66:403-411.
10. Choi DW (1987) Ionic dependence of glutamate neurotoxicity. J Neurosci 7:369-379.
11. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
12. Choi DW (1995) Calcium: still center-stage in hypoxic-ischemic neuronal death. Trends Neurosci 18:58-60.
13. Choi DW, Koh JY, Peters S (1988) Pharmacology of glutamate neurotoxicity in cortical cell culture: attenuation by NMDA. J Neurosci 8:185-196.
14. Coyle JT, Puttfarcken P (1993) Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689-695.
15. Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH (1991) Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88:6368-6371.
16. Dawson TM, Steiner JP, Dawson VL, Dinerman JL, Uhl GR, Snyder SH (1993) Immunosuppressant FK506 enhances phosphorylation of nitric oxide synthase and protects against glutamate neurotoxicity. Proc Natl Acad Sci USA 90:9808-9812.
17. 2+ dynamics after toxic doses of glutamate in cerebellar granule cells. Proc Natl Acad Sci USA 87:8017-8021.
18. Dubinsky JM, Rothman SM (1991) Intracellular calcium concentrations during "chemical hypoxia" and excitotoxic neuronal injury. J Neurosci 11:2545-2551.
19. Dykens JA, Stern A, Trenkner E (1987) Mechanism of kainate toxicity to cerebellar neurons in vitro is analogous to reperfusion tissue injury. J Neurochem 49:1222-1228.
20. Farkas DL, Wei MD, Febbroriello P, Carson JH, Loew LM (1989) Simultaneous imaging of cell and mitochondrial membrane potentials. Biophys J 56:1053-1069.
21. Gunter TE, Pfeiffer DR (1990) Mechanisms by which mitochondria transport calcium. Am J Physiol 258:C755-C786.
22. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, pp 86-188. Oxford: Clarendon.
23. Hartley DM, Choi DW (1989) Delayed rescue of N-methyl-D-aspartate receptor-mediated neuronal injury in cortical culture. J Pharmacol Exp Ther 250:752-758.
24. Hoek JB, Farber JL, Thomas AP, Wang X (1995) Calcium ion-dependent signalling and mitochondrial dysfunction: mitochondrial calcium uptake during hormonal stimulation in intact liver cells and its implication for the mitochondrial permeability transition. Biochim Biophys Acta 1271:93-102.
25. Jouaville LS, Ichas F, Holmuhamedov EL, Camacho P, Lechleiter JD (1995) Synchronization of calcium waves by mitochondrial substrates in Xenopus laevis oocytes. Nature 377:438-441.
26. Kao JP, Harootunian AT, Tsien RY (1989) Photochemically generated cytosolic calcium pulses and their detection by Fluo-3. J Biol Chem 264:8179-8184.
27. Kunz J, Hall MN (1993) Cyclosporin A, FK506 and rapamycin: more than just immunosuppression. Trends Biochem Sci 18:334-338.
28. Lafon-Cazal M, Pietri S, Culcasi M, Bockaert J (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537.
29. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS (1993) A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 364:626-632.
30. 2+ transients evoke concurrent mitochondrial depolarizations. Proc Natl Acad Sci USA 91:12579-12583.
31. Luft R (1994) The development of mitochondrial medicine. Proc Natl Acad Sci USA 91:8731-8738.
32. Mattson MP, Zhang Y, Bose S (1993) Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose. Exp Neurol 121:1-13.
33. Michaels RL, Rothman SM (1990) Glutamate neurotoxicity in vitro, antagonist pharmacology and intracellular calcium concentrations. J Neurosci 10:283-292.
34. 2+ homeostasis. Prog Neurobiol 37:255-285.
35. Newmeyer DD, Farschon DM, Reed JC (1994) Cell-free apoptosis in Xenopus egg extracts, inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79:353-364.
36. Nicolli A, Basso E, Petronilli V, Wenger RM, Bernardi P (1996) Interactions of cyclophilin with the mitochondrial inner membrane and regulation of the permeability transition pore, a cyclosporin A-sensitive channel. J Biol Chem 271:2185-2192.
37. Petronilli V, Cola C, Bernardi P (1993) Modulation of the mitochondrial cyclosporin A-sensitive permeability transition pore. J Biol Chem 268:1011-1016.
38. Prehn JH, Bindokas VP, Marcuccilli CJ, Krajewski S, Reed JC, Miller RJ (1994) Regulation of neuronal Bcl2 protein expression and calcium homeostasis by transforming growth factor type beta confers wide-ranging protection on rat hippocampal neurons. Proc Natl Acad Sci USA 91:12599-12603.
39. Randall RD, Thayer SA (1992) Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J Neurosci 12:1882-1895.
40. Reynolds IJ, Hastings TG (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15:3318-3327.
41. 3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744-747.
42. Saporito MS, Heikkila RE, Youngster SK, Nicklas WJ, Geller HM (1992) Dopaminergic neurotoxicity of 1-methyl-4-phenylpyridinium analogs in cultured neurons, relationship to the dopamine uptake system and inhibition of mitochondrial respiration. J Pharmacol Exp Ther 260:1400-1409.
43. Schinder AF, Montal M (1993) Two distinct modalities of NMDA-receptor inactivation induced by calcium influx in cultured rat hippocampal neurons. FEBS Lett 332:44-48.
44. Schinder AF, Olson E, Spitzer NC, Montal M (1995) The role of mitochondria in glutamate-induced neurotoxicity. Biophys J 68:A384.
45. Siesjö BK (1992) Pathophysiology and treatment of focal cerebral ischemia. I. Pathophysiology. J Neurosurg 77:169-184.
46. 2+-ATPase. Proc Natl Acad Sci USA 87:2466-2470.
47. Thayer SA, Miller RJ (1990) Regulation of the intracellular free calcium concentration in single rat dorsal root ganglion neurones in vitro. J Physiol (Lond) 425:85-115.
48. Tymianski M, Charlton MP, Carlen PL, Tator CH (1993a) Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J Neurosci 13:2085-2104.
49. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11:221-235.
50. Vayssière JL, Petit PX, Risler Y, Mignotte B (1994) Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc Natl Acad Sci USA 91:11752-11756.
51. Vergara J, DiFranco M (1992) Imaging of calcium transients during excitation-contraction coupling in skeletal muscle fibers. Adv Exp Med Biol 311:227-236.
52. 2+ loads. J Neurophysiol 72:2563-2569.
53. Weiss JH, Yin HZ, Choi DW (1994) Basal forebrain cholinergic neurons are selectively vulnerable to AMPA/kainate receptor-mediated neurotoxicity. Neuroscience 60:659-664.
54. 2+ exchange buffer glutamate-induced calcium loads in cultured cortical neurons. J Neurosci 15:1318-1328.
55. 2+ concentration and subsequent loss of neuronal function in individual neocortical neurons in culture. Proc Natl Acad Sci USA 91:12303-12307.
56. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, Sisodia SS, Cleveland DW, Price DL (1995) An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14:1105-1116.
57. Zamzami N, Marchetti P, Castedo M, Zanin C, Vayssière JL, Petit PX, Kroemer G (1995) Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 181:1661-1672.