Glutamate neurotoxicity is associated with nitric oxide-mediated mitochondrial dysfunction and glutathione depletion

Brain Research

Volumn 790, Issue 1-2, 1998, Pages 209-216

  Almeida, Angeles ^a   Heales, Simon J R ^b   Bolaños, Juan P ^a   Medina, José M ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cell respiration; Glutamate; Glutathione; Mitochondria; Neurotoxicity; Nitric oxide

Indexed keywords

GLUTAMIC ACID; GLUTATHIONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL EXPERIMENT; ARTICLE; CELL METABOLISM; ENERGY METABOLISM; GLUTATHIONE METABOLISM; MITOCHONDRIAL RESPIRATION; NERVE CELL; NEUROTOXICITY; NONHUMAN; OXIDATION REDUCTION REACTION; PHOSPHATE METABOLISM; PRIORITY JOURNAL; RAT;

EID: 0032550199     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(98)00064-X     Document Type: Article

References (54)

1. M. Ankarcrona, J.M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S.A. Lipton, P. Nicotera, Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function, Neuron 15 (1995) 961-973.
2. M.F. Beal, B.T. Hyman, W. Koroshetz, Do defects in mitochondrial energy metabolism underlie the pathology of neurodegenerative diseases?, Trends Neurosci. 16 (1993) 125-131.
3. J.S. Beckman, T.W. Beckman, J. Chen, P.A. Marshall, B.A. Freeman, Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide, Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 1620-1624.
4. K.M. Boje, P.K. Arora, Microglial-produced nitric oxide and reactive nitrogen oxides mediate neuronal cell death, Brain Res. 587 (1992) 250-256.
5. J.P. Bolaños, A. Almeida, V. Stewart, S. Peuchen, J.M. Land, J.B. Clark, S.J.R. Heales, Nitric oxide-mediated mitochondrial damage in the brain: mechanisms and implications for neurodegenerative diseases, J. Neurochem. 68 (1997) 2227-2240.
6. J.P. Bolaños, S.J.R. Heales, J.M. Land, J.B. Clark, Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary cultures, J. Neurochem. 64 (1995) 1965-1972.
7. J.P. Bolaños, S.J.R. Heales, S. Peuchen, J.E. Barker, J.M. Land, J.B. Clark, Nitric oxide-mediated mitochondrial damage: a potential neuroprotective role for glutathione, Free Rad. Biol. Med. 21 (1996) 995-1001.
8. J.P. Bolaños, S. Peuchen, S.J.R. Heales, J.M. Land, J.B. Clark, Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes, J. Neurochem. 63 (1994) 910-916.
9. E. Bonfoco, C. Krainc, M. Ankarcrona, P. Nicotera, S.A. Lipton, 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. U.S.A. 92 (1995) 7162-7166.
10. G.C. Brown, C.E. Cooper, Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase, FEBS Lett. 356 (1994) 295-298.
11. L. Castro, M. Rodríguez, R. Radi, Aconitase is readily inactivated by peroxynitrite, but not by its precursor, nitric oxide, J. Biol. Chem. 269 (1994) 29409-29415.
12. M.W.J. Cleeter, J.M. Cooper, V.M. Darley-Usmar, S. Moncada, A.H. Schapira, Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases, FEBS Lett. 345 (1994) 50-54.
13. D.W. Choi, Glutamate neurotoxicity and diseases of the nervous system, Neuron 1 (1988) 623-634.
14. V.L. Dawson, T.M. Dawson, Nitric oxide neurotoxicity, J. Chem. Neuroanatom. 10 (1996) 179-190.
15. V.L. Dawson, T.M. Dawson, D.A. Bartley, G.R. Uhl, S.H. Snyder, Mechanisms of nitric oxide-mediated neurotoxicity in primary brain cultures, J. Neurosci. 13 (1993) 2651-2661.
16. M. Erecinska, D. Nelson, J.M. Vanderkooi, Effects of NO-generating compounds on synaptosomal energy metabolism, J. Neurochem. 65 (1995) 2699-2705.
17. A. Frandsen, J. Drejer, A. Schousboe, Direct evidence that excitotoxicity in cultured neurons is mediated via N-methyl-D-aspartate (NMDA) as well as non-NMDA receptors, J. Neurochem. 53 (1989) 297-299.
18. J. Garthwaite, S.L. Charles, R. Chess-Williams, Endothelium-derived relaxing factor release on activation of NMDA receptors suggests a role as intercellular messenger in the brain, Nature 336 (1988) 385-387.
19. A. Hausladen, I. Fridovich, Superoxide and peroxynitrite inactivate aconitases, but nitric oxide does not, J. Biol. Chem. 269 (1994) 29405-29408.
20. S.J.R. Heales, J.E. Barker, V.C. Stewart, M.P. Brand, M.P. Brand, I.P. Hargreaves, P. Foppa, J.M. Land, J.B. Clark, J.P. Bolaños, Nitric oxide, energy metabolism and neurological disease, Biochem. Soc. Trans. 25 (1997) 861-865.
21. S.J.R. Heales, J.P. Bolaños, J.M. Land, J.B. Clark, Trolox protects mitochondrial complex IV from nitric oxide-mediated damage in astrocytes, Brain Res. 668 (1994) 243-245.
22. T.E. King, Preparation of succinate cytochrome c reductase and the cytochrome b-c1 particle, and reconstitution of succinate cytochrome c reductase, Methods Enzymol. 10 (1967) 216-225.
23. J.Y. Koh, D.W. Choi, Quantitative determination of glutamate mediated cortical neuronal injury in cell culture by lactate dehydrogenase efflux assay, J. Neurosci. Methods 20 (1987) 83-90.
24. M. Lafon-Cazal, S. Pietri, M. Culcasi, J. Bockaert, NMDA-dependent superoxide production and neurotoxicity, Nature 364 (1993) 535-537.
25. X. Liu, C.N. Kim, J. Yang, R. Jemmerson, X. Wang, Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c, Cell 86 (1996) 147-157.
26. I. Lizasoain, M.A. Moro, R.G. Knowles, V. Darley-Usmar, S. Moncada, Nitric oxide and peroxynitrite exert distinct effects on mitochondrial respiration which are differentially blocked by glutathione or glucose, Biochem. J. 314 (1996) 877-880.
27. O.H. Lowry, N.J. Rosebrough, A. Lewis-Farr, R.J. Randall, Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193 (1951) 265-275.
28. D. Meldrum, J. Garthwaite, Excitatory amino acid neurotoxicity and neurodegenerative disease, Trends Pharmacol. Sci. 11 (1990) 379-387.
29. J. Merrill, L.J. Ignarro, M.P. Sherman, J. Melinek, T.E. Lane, Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide, J. Immunol. 151 (1993) 2132-2141.
30. L. Molina y Vedia, B. McDonald, B. Reep, B. Brüne, M. Di Silvio, T.R. Billiar, E.G. Lapentina, Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosilation, J. Biol. Chem. 267 (1992) 24929-24932.
31. S. Moncada, R.M.J. Palmer, E.A. Higgs, Nitric oxide: physiology, pathophysiology and pharmacology, Pharmacol. Rev. 43 (1991) 109-142.
32. P. Rieder, E. Sofic, W. Rausch, B. Scmidt, G.P. Reynolds, K. Jellinger, M.B.H. Youdim, Transition metals, ferritin, glutathione and ascorbic acid in Parkinsonian brains, J. Neurochem. 52 (1989) 512-520.
33. J.B. Schulz, R.T. Matthews, M.F. Beal, Role of nitric oxide in neurodegenerative diseases, Curr. Opin. Neurol. 8 (1995) 480-486.
34. J.B. Schulz, R.T. Matthews, B.G. Jenkins, R.J. Ferrante, D. Siwek, D.R. Henshaw, P.B. Cipolloni, P. Mecocci, N.W. Kowall, B.R. Rosen, M.F. Beal, Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo, J. Neurosci. 15 (1995) 8419-8429.
35. S. Murphy, D. Guzybicki, Glial NO. Normal and pathological roles, Neuroscientist 2 (1996) 90-99.
36. T.H. Murphy, M. Miyamoto, A. Sastre, R.L. Schnaar, J.T. Coyle, Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress, Neuron 2 (1989) 1547-1558.
37. T.H. Murphy, R.L. Schnaar, J.T. Coyle, Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake, FASEB J. 4 (1990) 1624-1633.
38. J.F. Parkinson, B. Mitrovic, J.E. Merrill, The role of nitric oxide in multiple sclerosis, J. Mol. Med. 75 (1997) 174-186.
39. M. Patel, B.J. Day, J.D. Crapo, I. Fridowich, J.O. McNamara, Requirement for superoxide in excitotoxic cell death, Neuron 16 (1996) 345-355.
40. R. Radi, J.S. Beckman, K.M. Bush, B.A. Freeman, Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide, J. Biol. Chem. 266 (1991) 4244-4250.
41. R. Radi, M. Rodríguez, L. Castro, R. Telleri, Inhibition of mitochondrial electron transport by peroxynitrite, Arch. Biochem. Biophys. 308 (1994) 89-95.
42. C.I. Ragan, M.T. Wilson, V.M. Darley-Usmar, P.N. Lowe, Subfractionation of mitochondria and isolation of the proteins of oxidative phosphorylation, in: V.M. Darley-Usmar, D. Rickwood, M.T. Wilson (Eds.), Mitochondria. A Practical Approach, IRL Press, London, 1987, pp. 79-112.
43. J.A. Shepherd, P.B. Garland, Citrate synthase from rat liver, Methods Enzymol. 13 (1969) 11-19.
44. M.L. Simmons, S. Murphy, Induction of nitric oxide synthase in glial cells, J. Neurochem. 59 (1992) 897-905.
45. B. Soussi, J. Idstrom, T. Schersten, A. Bylund-Fellenius, Cytochrome c oxidase and cardiolipin alterations in response to skeletal muscle ischaemia and reperfusion, Acta. Physiol. Scand. 138 (1990) 107-114.
46. C. Théry, B. Chamak, M. Mallat, Cytotoxic effect of brain macrophages on developing neurons, Eur. J. Neurosci. 3 (1991) 1155-1164.
47. K. Tsuji, Y. Nakamura, T. Ogata, T. Shibata, K. Kataoka, Rapid decrease in ATP content without recovery phase during glutamate-induced cell death in cultured spinal neurons, Brain Res. 662 (1994) 289-292.
48. A. Vassault, L-Lactate dehydrogenase. UV method with pyruvate and NADH, in: J. Bergmeyer, M. Graß1 (Eds.), Methods of Enzymatic Analysis, Vol. 3, Verlag Chemie, Weinheim, 1983, pp. 118-126.
49. C. Vicario, A. Tabernero, J.M. Medina, Regulation of lactate metabolism by albumin in rat neurons and astrocytes from primary culture, Pediatr. Res. 34 (1993) 709-715.
50. 2+ loads, J. Neurophysiol. 72 (1994) 2563-2569.
51. D.C. Wharton, A. Tzagoloff, Cytochrome oxidase from beef heart mitochondria, Methods Enzymol. 10 (1967) 245-250.
52. R.J. White, I.J. Reynolds, Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxic exposure, J. Neurosci. 16 (1996) 5688-5697.
53. J. Zhang, V.L. Dawson, T.M. Dawson, S.H. Snyder, Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity, Science 263 (1994) 687-689.
54. J. Zhang, S.H. Snyder, Nitric oxide stimulates auto-ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase, Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 9382-9385.