Glutamate Uptake Inhibitor L-Trans-Pyrrolidine 2,4-Dicarboxylate Becomes Neurotoxic in the Presence of Subthreshold Concentrations of Mitochondrial Toxin 3-Nitropropionate: Involvement of Mitochondrial Reducing Activity and ATP Production

Journal of Neuroscience Research

Volumn 74, Issue 6, 2003, Pages 956-966

  García, Octavio ^a   Massieu, Lourdes ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Cell death; Energy substrates; Mitochondrial activity

Indexed keywords

2,4 PYRROLIDINEDICARBOXYLIC ACID; 3 NITROPROPIONIC ACID; ACETOACETIC ACID; ADENOSINE TRIPHOSPHATE; DIZOCILPINE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N TERT BUTYL ALPHA PHENYLNITRONE; PYRUVIC ACID; SUCCINATE DEHYDROGENASE;

ANIMAL CELL; ARTICLE; BRAIN ISCHEMIA; CELL MEMBRANE; CELL NUCLEUS; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENERGY; ENZYME SUBSTRATE; GRANULE CELL; MITOCHONDRION; NERVE CELL LESION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; REDUCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELLS, CULTURED; CEREBELLUM; DICARBOXYLIC ACIDS; GLUTAMIC ACID; MITOCHONDRIA; NEUROTRANSMITTER UPTAKE INHIBITORS; NITRO COMPOUNDS; PROPIONIC ACIDS; PYRROLIDINES; RATS; RATS, WISTAR;

EID: 0344980746     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10825     Document Type: Article

References (62)

1. Almeida A, Bolaños JP. 2001. A transient inhibition of mitochondrial ATP synthesis by nitric oxide synthase activation triggered apoptosis in primary cortical neurons. J Neurochem 77:676-690.
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. Arias C, Montiel T, Quiroz-Baez R, Massieu L. 2002. β-Amyloid neurotoxicity is exacerbated during glycolysis inhibition and mitochondrial impairment in the rat hippocampus in vivo and in isolated nerve terminals: implications for Alzheimer's disease. Exp Neurol 176:163-174.
4. Beal MF. 1992. Mechanisms of excitotoxicity in neurologic diseases. FASEB J 6:3338-3344.
5. Beal MF. 2000. Energetics in the pathogenesis of neurodegenerative diseases. Trends Neurosci 23:298-304.
6. Benveniste H, Drejer J, Schousboe A, Diemer NH. 1984. Elevation of the extracellular concentrations of glutamate and aspartate in the rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43:1369-1374.
7. Bernas T, Dobrucki J. 2002. Mitochondrial and non-mitochondrial reduction of MTT: interaction of MTT with TMRE, JC-1 and NAO mitochondrial fluorescent probes. Cytometry 47:236-242.
8. Berridge MV, Tan AS. 1993. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolim bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 303:474-482.
9. Bezvenyuk Z, Miettinen R, Solovyan V. 2003. Chromatin condensation during glutamate-induced excitotoxicity of cerebellar granule neurons precedes disintegration of nuclear DNA into high molecular weight DNA fragments. Brain Res Mol Brain Res 110:140-146.
10. Bittigau P, Ikonomidou C, 1997. Glutamate in neurologic diseases. J Child Neurol 12:471-485.
11. Blitzblau R, Gupta S, Djali S, Robinson MB, Rosenberg PA. 1996. The glutamate transport inhibitor L-trans-pyrrolidine-2, 4-dicarboxylace indirectly evokes NMDA receptor mediated neurotoxicity in rat cortical cultures. Eur J Neurosci 8:1840-1852.
12. Bolaños JP, Heales SP, Land JM, Clark JB. 1995. Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurons and astrocytes in primary culture. J Neurochem 64:1965-1972.
13. Bradford, MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
14. Bridges RJ, Stanley MS, Anderson MW, Cotman CW, Chamberlin AR. 1991. Conformationally defined neurotransmitter analogs. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereomer. J Med Chem 34:717-725.
15. Brorson JR, Schumacker PT, Zhang H. 1999. Nitric oxide acutely inhibits neuronal energy production. J Neurosci 19:147-158.
16. Bruhn T, Christensen T, Diemer NH. 2001. In vivo cellular uptake of glutamate is impaired in the rat hippocampus during and after transient cerebral ischemia: a microdialysis extraction study. J Neurosci Res 66:1118-1126.
17. Budd SL, Nicholls DG. 1996. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells. J Neurochem 67:2282-2291.
18. Cebers G, Cebere A, Wagner A, Liljequist S. 1999. Prolonged inhibition of glutamate reuptake down-regulates NMDA receptor functions in cultured cerebellar granule cells. J Neurochem 72:2181-2190.
19. Chan PH. 2001. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21:2-14.
20. Cheung NS, Pascoe CJ, Giardina SF, John CA, Beart PM. 1998. Micromolar L-glutamate induces extensive apoptosis in an apoptotic-necrotic continuum of insult-dependent, excitotoxic injury in cultured cortical neurons. Neuropharmacology 37:1419-1429.
21. Choi DW. 1996. Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol 6:667-672.
22. Craig ET. 1997. Nitrone spin traps as protectants against oxidative damage. In: Bär PR, Beal MF, editors. Neuroprotection in CNS diseases. New York: Marcel Dekker, Inc. p 183-204.
23. Dawson LA, Djali S, Gonzales C, Vinegra MA, Zaleska MM. 2000. Characterization of transient focal ischemia-induced increases in extracellular glutamate and aspartate in spontaneously hypertensive rats. Brain Res Bull 53:767-776.
24. Fiskum G, Murphy AN, Beal MF. 1999. Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J Cereb Blood Flow Metab 19:351-369.
25. García O, Massieu L. 2001. Strategies for neuroprotection against trans-2,4-pyrrolidine dicarboxylate-induced neuronal damage during energy impairment in vitro. J Neurosci Res 64:418-428.
26. Graham SH, Chen J. 2001. Programmed cell death in cerebellar ischemia. J Cereb Blood Flow Metab 21:99-109.
27. Halestrap AP. 1975. The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors. Biochem J 148:85-96.
28. Himi T, Ikeda M, Yasuhara T, Murota S. 2003. Oxidative neuronal death caused by glutamate uptake inhibition in cultured hippocampal neurons. J Neurosci Res 71:679-688.
29. Izumi Y, Benz AM, Katsuki H, Zorumski CF. 1997. Endogenous monocarboxylates sustain hippocampal synaptic function and morphological integrity during energy deprivation. J Neurosci 17:9448-9457.
30. Kerr JFR, Harmon BV. 1991. Definition and incidence of apoptosis: an historical perspective. In: Tomei LD, Cope FO, editors. Apoptosis: the molecular basis of cell death. New York: Cold Spring Harbor Laboratory Press. p 5-29.
31. Lafón-Cazal M, Pietri S, Culcasi M, Bockaert J. 1993. NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537.
32. Lee JY, Kim YH, Koh JY. 2001. Protection by pyruvate against transient forebrain ischemia in rats. J Neurosci 21:1-6.
33. Lee WT, Yin HS, Shen YZ. 2002a. The mechanisms of neuronal death produced by mitochondrial toxin 3-nitropropionic acid: the roles of N-methyl-D-aspartate glutamate receptors and mitochondrial calcium overload. Neuroscience 112:707-716.
34. Lee WT, Itoh T, Pleasure D. 2002b. Acute and chronic alterations in calcium homeostasis in 3-nitropropionic acid-treated human NT2-N neurons. Neuroscience 113:699-708.
35. Leist M, Single B, Nauman H, Fava E, Simon B, Kühnle S, Nicotera P. 1999. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 249:396-403.
36. Lipton P. 1999. Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568.
37. Liu Y, Peterson DA, Kimura H, Schubert D. 1997. Mechanism of cellular 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) reduction. J Neurochem 69:581-593.
38. +. Neuroscience 93:285-292.
39. Madl JE, Burgesser K. 1993. Adenosine triphosphate depletion reverses sodium-dependent neuronal uptake of glutamate in rat hippocampal slices. J Neurosci 13:4429-4444.
40. Marcaida G, Miñana MD, Grisolía S, Felipo V. 1997. Determination of intracellular ATP in primary cultures of neurons. Brain Res Protoc 1:75-78.
41. Martin LJ, Al-Abdulla NA, Brambrink AM, Kirsch JR, Sieber FE, Portera-Cailliau C. 1998. Neurodegeneration in excitotoxicity, global cerebral ischemia and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res Bull 46:281-309.
42. Massieu L, Del Río P, Montiel T. 2001. Neurotoxicity of glutamate uptake inhibition in vivo: correlation with succinate dehydrogenase activity and prevention by energy substrates. Neuroscience 106:669-677.
43. Massieu L, Gómez-Román N, Montiel T. 2000. In vivo potentiation of glutamate-mediated neuronal damage after chronic administration of the glycolysis inhibitor iodoacetate. Exp Neurol 165:257-267.
44. Massieu L, Haces ML, Montiel T, Hernández-Fonseca K. 2003. Acetoacetate protects hippocampal neurons against glutamate-mediated neuronal damage during glycolysis inhibition. Neuroscience 120:365-378.
45. Massieu L, Morales-Villagrán A, Tapia R. 1995. Accumulation of extracellular glutamate by inhibition of its uptake is not sufficient for inducing neuronal damage: an in vivo microdialysis study. J Neurochem 64:2262-2272.
46. Matts M, Marin P, Israël M, Glowinski J, Prémont J. 1999. Pyruvate and lactate protect striatal neurons against N-methyl-D-aspartate-induced neurotoxicity. Eur J Neurosci 11:3215-3224.
47. Mosmann T. 1983. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
48. Nasr P, Gursahani HI, Pang Z, Bondada V, Lee J, Hadley RW, Geddes JW. 2003. Influence of cytosolic and mitochondrial Ca2+, ATP, mitochondrial membrane potential, and calpain activity on the mechanism of neuron death induced by 3-nitropropionic acid. Neurochem Int 43:89-99.
49. Nicholls DG, Budd SL. 1998. Mitochondria and neuronal glutamate excitotoxicity. Biochem Biophys Acta 1366:97-112.
50. Pang Z, Geddes JW. 1997. Mechanisms of cell death induced by the mitochondrial toxin 3-nitropropionic acid: acute excitotoxic necrosis and delayed apoptosis. J Neurosci 17:3064-3073.
51. Rosenbaum DM, Michaelson M, Batter DK, Doshi P, Kessler JA. 1994. Evidence for hypoxia-induced, programmed cell death of cultured neurons. Ann Neurol 36:864-870.
52. Rossi DJ, Oshima T, Attwell D. 2000. Glutamate release in severe brain ischaemia is mainly by reversed uptake, Nature 403:316-321.
53. Ruiz F, Alvarez G, Pereira R, Hernández M, Villalba M, Cruz F, Cerdán S, Bogónez E, Satrústegui J. 1998. Protection by pyruvate and malate against glutamate-mediated neurotoxicity. NeuroReport 9:1277-1282.
54. Sánchez-Carbente MR, Massieu L. 1999. Transient inhibition of glutamate uptake in vivo induces neurodegeneration when energy metabolism is impaired. J Neurochem 72:129-138.
55. Schinder AF, Olson EC, Spitzer NC, Montal M. 1996. Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J Neurosci 16:6125-6133.
56. Schulz JB, Henshaw DR, Siwek D, Jenkins BG, Ferrante RJ, Cipolloni PB, Kowall NW, Rosen BR, Beal MF. 1995. Involvement of free radicals in excitotoxicity in vivo. J Neurochem 64:2239-2247.
57. Seki Y, Feustel PJ, Keller RW Jr, Tranmer BI, Kimelberg HK. 1999. Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokainate and an anion channel blocker. Stroke 30:433-440.
58. Simon RP, Swan JH, Griffiths T, Meldrum BS. 1984. Blockade of N-methyl-D-aspartate receptor may protect against ischemic damage in the brain. Science 226:830-852.
59. Suzuki M, Suzuki M, Sato K, Dohi S, Sato T, Matsuura A, Hiraide A. 2001. Effect of β-hydroxybutyrate, a cerebral function improving agent, on cerebral hypoxia, anoxia and ischemia in mice and rats. Jpn J Pharmacol 87:143-150.
60. Tretter L, Adam-Vizi V. 2000. Inhibition of Krebs cycle enzymes by hydrogen peroxide: a key role of α-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress. J Neurosci 20:8972-8979.
61. Vergun O, Keelan J, Khodorov BI, Duchen MR. 1999. Glutamate-induced mitochondnal depolarization and perturbation of calcium homeostasis in cultured rat hippocampal neurons. J Physiol 519:451-466.
62. Volterra A, Bezzi P, Rizzini BL, Trotti D, Ullensvang K, Danbolt NC, Racagni G. 1996. The competitive transport inhibitor L-transpyrrolidine-2,4-dicarboxylate triggers excitotoxicity in rat cortical neuron-astrocyte co-cultures via glutamate release rather than uptake inhibition. Eur J Neurosci 8:2019-2028.