Transient inhibition of glutamate uptake in vivo induces neurodegeneration when energy metabolism is impaired

Journal of Neurochemistry

Volumn 72, Issue 1, 1999, Pages 129-138

  Sánchez Carbente, Ma Del Rayo ^a   Massieu, Lourdes ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Energy depletion; Excitotoxicity; Glutamate transport; L trans Pyrrolidine 2,4 dicarboxylate

Indexed keywords

2,4 PYRROLIDINEDICARBOXYLIC ACID; GLUTAMIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; ELECTRON TRANSPORT; ENERGY TRANSFER; MALE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIHYPERTENSIVE AGENTS; ASPARTIC ACID; BIOLOGICAL TRANSPORT; BRAIN CHEMISTRY; CORPUS STRIATUM; DICARBOXYLIC ACIDS; ENERGY METABOLISM; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICRODIALYSIS; NERVE DEGENERATION; NEUROTOXINS; NEUROTRANSMITTER UPTAKE INHIBITORS; NITRO COMPOUNDS; PROPIONIC ACIDS; PYRROLIDINES; RATS; RATS, WISTAR;

ANIMALIA;

EID: 0344450761     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0720129.x     Document Type: Article

References (39)

1. Attwell D., Barbour B., and Szatkowski M. (1993) Nonvesicular release of neurotransmitter. Neuron 11, 401-407.
2. Bazzett T. J., Falik R. C., Becker J. B., and Albin R. L. (1996) Synergistic effects of chronic exposure to subthreshold concentrations of quinolinic acid and malonate in the rat striatum. Brain Res. 718, 228-232.
3. Beal M. F. (1992) Does impairment of energy metabolism result in excitotoxic neuronal death in neurodegenerative illnesses? Ann. Neurol. 32, 119-130.
4. Beal M. F., Brouillet E., Jenkins B. G., Ferrante R. J., Kowall N. W., Miller J. M., Storey E., Srivastava R., Rosen B. R., and Hyman B. T. (1993a) Neurochemical and histologic characterization of striatal excitotoxic lesions produced by the mitochondrial toxin 3-nitropropionic acid. J. Neurosci. 13, 4181-4192.
5. Beal M. F., Brouillet E., Jenkins B., Henshaw R., Rosen B., and Hyman B. T. (1993b) Age-dependent striatal lesions produced by the endogenous mitochondrial inhibitor malonate. J. Neurochem. 61, 1147-1150.
6. Benveniste H., Drejer J., Schousboe A., and Diemer N. H. (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J. Neurochem. 43, 1369-1374.
7. Blitzblau R., Gupta S., Djali S., Robinson M. B., and Rosenberg P. A. (1996) The glutamate transport inhibitor L-trans-pyrrolidine-2.4-dicarboxylate indirectly evokes NMDA receptor mediated neurotoxicity in rat cortical cultures. Eur. J. Neurosci. 8, 1840-1852.
8. Brouillet E., Guyot M.-C., Mittoux V., Altairae S., Condé F., Palfi S., and Hantraye P. (1998) Partial inhibition of brain succinate dehydrogenase by 3-nitropropionic acid is sufficient to initiate striatal degeneration in rat. J. Neurochem. 70, 794-805.
9. Choi D. W., Maulucci-Gedde M. A., and Kriegstein A. R. (1987) Glutamate neurotoxicity in cortical cell culture. J. Neurosci. 7, 357-368.
10. Gill R., Foster A. C., and Woodruff G. N. (1987) Systemic administration of MK-801 protects against ischemia-induced hippocampal neurodegeneration in the gerbil. J. Neurosci. 7, 3343-3349.
11. Greene J. G. and Greenamyre J. T. (1995) Exacerbation of NMDA, AMPA, and L-glutumate excitotoxicity by the succinate dehydrogenase inhibitor malonate. J. Neurochem. 64, 2332-2338.
12. Greene J. G. and Greenamyre J. T. (1996) Bioenergetics and glutamate excitotoxicity. Prog. Neurobiol. 48, 613-634.
13. Greene J. G., Porter R. H. P., Eller R. V., and Greenamyre J. T. (1993) Inhibition of succinate dehydrogenase by malonic acid produces an "excitotoxic" lesion in rat striatum. J. Neurochem. 61, 1151-1154.
14. Greene J. G., Shieu S. S., Gross R. A., and Greenamyre J. T. (1997) 3-Nitropropionic acid exacerbates N-methyl-D-aspartate toxicity in striatal culture by multiple mechanisms. Neuroscience 84, 503-510.
15. Guyot M. C., Hantraye P., Dolan R., Palfi S., Maziére M., and Brouillet E. (1997) Quantifiable bradykinesia, gait abnormalities and Huntington's disease-like striatal lesions in rats chronically treated with 3-nitropropionic acid. Neuroscience 79, 45-56.
16. Hamilton B. F. and Gould D. H. (1987) Nature and distribution of brain lesions in rats intoxicated with 3-nitropropionic acid: a type of hypoxic (energy deficient) brain damage. Acta Neuropathol. 72, 286-297.
17. 2+ accumulation in cortical cell culture correlates with subsequent neuronal degeneration. J. Neurosci. 13, 1993-2000.
18. Henneberry R. C. (1989) The role of neuronal energy in the neurotoxicity of excitatory amino acids. Neurobiol. Aging 10, 611-613.
19. Liévens J. C., Duterte M., Forni C., Salin P., and Kerkerian-Le Goff L. (1997) Continuous administration of the glutamate uptake inhibitor L-trans-pyrrolidine-2.4-dicarboxylate produces striatal lesion. Mol. Brain Res. 50, 181-189.
20. Lucas D. R. and Newhouse J. P. (1957) The toxic effect of sodium L-glutamate on the inner layers of the retina. Arch. Ophthalmol. 58, 193-201.
21. Ludolph A. C., Seelig M., Ludolph A. G., Sabri M. I., and Spencer P. S. (1992) ATP deficits and neuronal degeneration induced by 3-nitropropionic acid. Ann. NY Acad. Sci. 648, 300-302.
22. Massieu L. and Tapia R. (1997) Glutamate uptake impairment and neuronal damage in young and aged rats in vivo. J. Neurochem. 69, 1151-1160.
23. Massieu L., Morales-Villagrán A., and 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.
24. Messam C. A., Greene J. C., Greenamyre J. T., and Robinson M. B. (1995) Intrastriatal injections of the succinate dehydrogenase inhibitor, malonate, cause a rise in extracellular amino acids. Brain Res. 684, 221-224.
25. Michaels R. L. and Rothman S. M. (1990) Glutamate neurotoxicity in vitro: antagonists, pharmacology and intracellular calcium concentrations. J. Neurosci. 10, 283-292.
26. Novelli A., Reilly J. A., Lysko P. G., and Henneberry R. C. (1988) Glutamate becomes neurotoxic via the NMDA receptor when intracellular energy levels are reduced. Brain Res. 451, 205-212.
27. Olney J. W. (1969) Brain lesions, obesity and other disturbances in mice treated with monosodium glutamate. Science 164, 719-721.
28. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney.
29. Randall R. D. and Thayer S. A. (1992) Glutamate-induced calcium transients trigger delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12, 1882-1895.
30. Rothstein J. D., Dykes-Hoberg M., Pardo C. A., Bristol L. A., Jin L., Kuncl R. W., Kanai Y., Hediger M. A., Wang Y., Schielke J. P., and Welly D. F. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16, 675-686.
31. Salazar P., Montiel T., Brailowsky S., and Tapia R. (1994) Decrease of glutamate decarboxylase activity after in vivo cortical infusion of γ-aminobutyric acid. Neurochem. Int. 24, 363-368.
32. Schinder A. F., Olson E. C., Spitzer N. C., and Montal M. (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16, 6125-6133.
33. Simon R. P., Swan J. H., Griffiths T., and Meldrum B. S. (1984) Blockade of N-methyl-D-aspartate receptors may protect against ischemic damage in the brain. Science 226, 850-852.
34. Simpson J. R. and Isacson O. (1993) Mitochondrial impairment reduces the threshold for in vivo NMDA-mediated neuronal death in the striatum. Exp. Neurol. 121, 57-64.
35. Tanaka K., Watase K., Manabe T., Yamada K., Watanabe M., Takahashi K., Iwama H., Nishikawa T., Ichihara N., Kikuchi T., Okuyama S., Kawashima N., Hori S., Takimoto M., and Wada K. (1997) Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-I. Science 276, 1699-1702.
36. Velasco I., Tapia R., and Massieu L. (1996) Inhibition of glutamate uptake induces progressive accumulation of extracellular glutamate and neuronal damage in rat cortical cultures. J. Neurosci. Res. 44, 551-561.
37. Volterra A., Bezzi P., Rizzini B. L., Trotti D., Ullensvang K., Danbolt N. C., and Racagni G. (1996) The competitive transport inhibitor L-trans-pyrrolidine-2,4-dicarboxylate triggers excitotoxicity in rat cortical neuron-astrocyte co-cultures via glulamate release rather than uptake inhibition. Eur. J. Neurosci. 8, 2019-2028.
38. Zeevalk G. D. and Nicklas W. J. (1990) Chemically induced hypoglycemia and anoxia: relationship to glutamate receptor-mediated toxicity in retina. J. Pharmacol. Exp. Ther. 253, 1285-1292.
39. 2+ block at the N-methyl-D-aspartate receptor underlies receptor activation during inhibition of neuronal metabolism. J. Neurochem. 59, 1211-1220.