Energy failure in astrocytes increases the vulnerability of neurons to spreading depression

European Journal of Neuroscience

Volumn 19, Issue 9, 2004, Pages 2446-2454

  Lian, Xiao Yuan ^a   Stringer, Janet L ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

6 bisphosphate; Aconitase; ATP; Deferoxamine; Dimethyl sulfoxide; Fluorocitrate; Fructose 1; Isocitrate; Rat

Indexed keywords

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; DEFEROXAMINE; DIMETHYL SULFOXIDE; FRUCTOSE 1,6 BISPHOSPHATE; HEAT SHOCK PROTEIN 72; HYDROXYL RADICAL; IRON CHELATING AGENT; ISOCITRIC ACID; NEUROPROTECTIVE AGENT; SCAVENGER;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL LEVEL; CELL VIABILITY; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG EFFICACY; ENZYME ACTIVITY; IMMUNOREACTIVITY; IN VIVO STUDY; NERVE CELL LESION; NEUROMODULATION; NEUROPATHOLOGY; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SILVER STAINING; STATISTICAL SIGNIFICANCE; STRESS;

ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CELL SURVIVAL; CEREBRAL CORTEX; CITRATES; DEFEROXAMINE; DIMETHYL SULFOXIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION ROUTES; FRUCTOSEDIPHOSPHATES; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMINE; HEAT-SHOCK PROTEINS; HSP72 HEAT-SHOCK PROTEINS; IMMUNOHISTOCHEMISTRY; IRON CHELATING AGENTS; ISOCITRATES; MALE; MITOCHONDRIA; NEURONS; POTASSIUM CHLORIDE; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING; SPREADING CORTICAL DEPRESSION;

EID: 2442426349     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0953-816X.2004.03289.x     Document Type: Article

References (74)

1. Anderson, M.E. & Meister, A. (1983) Transport and direct utilization of gamma-glutamylcyst (e) ine for glutathione synthesis. Proc. Natl Acad. Sci. USA, 80, 707-711.
2. Bannai, S. (1984) Transport of cystine and cysteine in mammalian cells. Biochim. Biophys. Acta, 779, 289-306.
3. Berg, J.M., Tymoczko, J.L. & Stryer, L. (2002) Biochemistry. W.H. Freeman Co, New York, NY.
4. Bondarenko, A. & Chesler, M. (2001) Rapid astrocyte death induced by transient hypoxia, acidosis, and extracellular ion shifts. Glia, 34, 134-142.
5. Bradford, M. (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.
6. Broer, S. & Brookes, N. (2001) Transfer of glutamine between astrocytes and neurons. J. Neurochem., 77, 705-719.
7. Chae, H.Z., Chung, S.J. & Rhee, S.G. (1994) Thioredoxin-dependent peroxide reductase from yeast. J. Biol. Chem., 269, 27670-27678.
8. Chen, Y. & Swanson, R.A. (2003) Astrocytes and brain injury. J. Cereb. Blood Flow Metab. 23, 137-149.
9. Chen, Y., Vartiainen, N.E., Ying, W., Chan, P.M., Koistinaho, J. & Swanson, R.A. (2001) Astrocytes protect neurons from nitric oxide toxicity by a glutathione-dependent mechanism. J. Neurochem., 11, 1601-1610.
10. Davey, G.P., Peuchen, S. & Clark, J.B. (1998) Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J. Biol. Chem., 273, 12753-12757.
11. De Cristobal, J., Moro, M.A., Davalos, A., Castillo, J., Leza, J.C., Camarero, J., Colado, M.I., Lorenzo, P. & Lizasoain, I. (2001) Neuroprotective effect of aspirin by inhibition of glutamate release after permanent focal cerebral ischaemia in rats. J. Neurochem., 79, 456-459.
12. Espanol, M.T., Litt, L., Hasegawa, K., Chang, L.H., Macdonald, J.M., Gregory, G., James, T.L. & Chan, P.H. (1998) Fructose-1,6-bisphosphate preserves adenosine triphosphate but not intracellular pH during hypoxia in respiring neonatal rat brain slices. Anesthesiology, 88, 461-472.
13. Flint, D.H., Tuminello, J.F. & Emptage, M.H. (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide. J. Biol. Chem., 268, 22369-22376.
14. Fonnum, F., Johnsen, A. & Hassel, B. (1997) Use of fluorocitrate and fluoroacetate in the study of brain metabolism. Glia, 21, 106-113.
15. Gallyas, F., Wolff, J.R., Bottcher, H. & Zaborszky, L. (1980) A reliable and sensitive method to localize terminal degeneration and lysosomes in the central nervous system. Stain Technol., 55, 299-306.
16. Gardner, P.R., Raineri, I., Epstein, L.B. & White, C.W. (1995) Superoxide radical and iron modulate aconitase activity in mammalian cells. J. Biol. Chem., 270, 13399-13405.
17. Giffard, R.G., Monyer, H. & Choi, D.W. (1990) Selective vulnerability of cultured cortical glia to injury by extracellular acidosis. Brain Res., 530, 138-141.
18. Gupta, R.C., Milatovic, D. & Dettbarn, W.D. (2001) Depletion of energy metabolites following acetylcholinesterase inhibitor-induced status epilepticus: protection by antioxidants. Neurotoxicology, 22, 271-282.
19. Gupta, R.C., Milatovic, D., Zivin, M. & Dettbarn, W.D. (2000) Seizure-induced changes in energy metabolites and effects of N-tert-butyl-alpha-phenylnitrone (PNB) and vitamin E in rats. Pflugers Arch., 440, R160-R162.
20. Harrison, P.M. & Arosio, P. (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochem. Biophys. Acta, 1275, 161-203.
21. Hassel, B., Paulsen, R.E., Johnsen, A. & Fonnum, F. (1992) Selective inhibition of glial cell metabolism in vivo by fluorocitrate. Brain Res., 576, 120-124.
22. Herreras, O., Largo, C., Ibarz, J.M., Somjen, G.G. & Martin Del Rio, R. (1994) Role of neuronal synchronizing mechanisms in the propagation of spreading depression in the in vivo hippocampus. J. Neurosci., 14, 7087-7098.
23. + in neuronal cell death during and after anoxia/ischemia. Neurosci. Biobehav. Rev., 21, 129-134.
24. Kelleher, J.A., Chan, P.H., Chan, T.Y. & Gregory, G.A. (1995) Energy metabolism in hypoxic astrocytes: protective mechanism of fructose-1,6- bisphosphate. Neurochem. Res., 20, 785-792.
25. Kelleher, J.A., Chan, T.Y., Chan, P.H. & Gregory, G.A. (1996) Protection of astrocytes by fructose 1,6-bisphosphate and citrate ameliorates neuronal injury under hypoxic conditions. Brain Res., 726, 167-173.
26. Keyser, D.O. & Pellmar, T.C. (1994) Synaptic transmission in the hippocampus: critical role for glial cells. Glia, 10, 237-243.
27. Koponen, S., Keinanen, R., Roivainen, R., Hirvonen, T., Narhi, M., Chan, P.H. & Koistinaho, J. (1999) Spreading depression induces expression of calcium-independent protein kinase C subspecies in ischaemia-sensitive cortical layers: regulation by N-methyl-D-aspartate receptors and glucocorticoids. Neuroscience, 93, 985-993.
28. Kushnareva, Y., Murphy, A.N. & Andreyev, A. (2002) Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD (P) + oxidation-reduction state. Biochem. J., 368, 545-553.
29. Kwon, S.J., Park, J.W., Choi, W.K., Kim, I.H. & Kim, K. (1994) Inhibition of metal-catalyzed oxidation systems by a yeast protector protein in the presence of thioredoxin. Biochem. Biophys. Res. Commun., 201, 8-15.
30. Li, Q.Y., Pedersen, C., Day, B.J. & Patel, M. (2001) Dependence of excitotoxic neurodegeneration on mitochondrial aconitase inactivation. J. Neurochem., 78, 746-755.
31. Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J.A. & Robinson, J.P. (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem., 278, 8516-8525.
32. Liang, L.P., Ho, Y.S. & Patel, M. (2000) Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience, 101, 563-570.
33. Liu, Y., Fiskum, G. & Schubert, D. (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem., 80, 780-787.
34. Magestretti, P.J., Pellerin, L., Rothman, D.L. & Shulman, R.G. (1999) Energy on demand. Science, 283, 496-497.
35. Meister, A. (1991) Glutathione deficiency produced by inhibition of its synthesis, and its reversal; application in research and therapy. Pharmacol. Ther, 51, 155-194.
36. Milligan, E.D., Twining, C., Chacur, M., Biedenkapp, J., O'Connor, K., Poole, S., Tracey, K., Martin, D., Maier, S.F. & Watkins, L.R. (2003) Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci., 23, 1026-1040.
37. Minotti, G., Recalcati, S., Mordente, A., Liberi, G., Calafiore, A.M., Mancuso, C., Preziosi, P. & Cairo, G. (1998) The secondary alcohol metabolite of doxorubicin irreversibly inactivates aconitase/iron regulatory protein-1 in cytosolic fractions from human myocardium. FASEB J., 12, 541-552.
38. Nadler, J.V. & Evenson, D.A. (1983) Use of excitatory amino acids to make axon-sparing lesions of hypothalamus. Meth. Enzymol., 103, 393-400.
39. Nedergaard, M. & Hansen, A.J. (1988) Spreading depression is not associated with neuronal injury in the normal brain. Brain Res., 449, 395-398.
40. Obeidat, A.S. & Andrew, R.D. (1998) Spreading depression determines acute cellular damage in the hippocampal slice during oxygen/glucose deprivation. Eur. J. Neurosci., 10, 3451-3461.
41. 2/glucose deprivation in the hippocampal slice. J. Cereb. Blood Flow Metab., 20, 412-422.
42. Obrenovitch, T.P. (1995) The Ischaemic penumbra: twenty years on. Cerebrovasc. Brain Metab. Rev., 7, 297-323.
43. Olah, L., Wecker, S. & Hoehn, M. (2001) Relation of apparent diffusion coefficient changes and metabolic disturbances after 1 hour of focal cerebral ischemia and at different reperfusion phases in rats. J. Cereb. Blood Flow Metab., 21, 430-439.
44. Paschen, W., Olah, L. & Mies, G. (2000) Effect of transient focal ischemia of mouse brain on energy state and NAD levels: no evidence that NAD depletion plays a major role in secondary disturbances of energy metabolism. J. Neurochem., 75, 1675-1680.
45. Patel, M., Day, B.J., Crapo, J.D., Fridovich, I. & McNamara, J.O. (1996) Requirement for superoxide in excitotoxic cell death. Neuron, 16, 345-355.
46. Patel, M. & Li, Q.Y. (2003) Age dependence of seizure-induced oxidative stress. Neuroscience, 118, 431-437.
47. Patel, A.B., Rothman, D.L., Cline, G.W. & Behar, K.L. (2001) Glutamine is the major precursor for GABA synthesis in rat neocortex in vivo following acute GABA-transaminase inhibition. Brain Res., 919, 207-220.
48. Paulsen, R.E., Contestabile, A., Villani, L. & Fonnum, F. (1987) An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: the use of fluorocitrate. J. Neurochem., 48, 1377-1385.
49. +-evoked release of transmitter amino acids investigated by microdialysis. J. Neurochem., 52, 1823-1829.
50. Pereira, C., Santos, M.S. & Oliveira, C. (1999) Involvement of oxidative stress on the impairment of energy metabolism induced by A beta peptides on PC12 cells: protection by antioxidants. Neurobiol. Dis., 6, 209-219.
51. Rae, C., Hare, N., Bubb, W.A., McEwan, S.R., Broer, A., McQuillan, J.A., Balcar, V.J., Conigrave, A.D. & Broer, S. (2003) Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: further evidence for metabolic compartmentation. J. Neurochem., 85, 503-514.
52. Rao, V.L., Dogan, A., Todd, K.G., Bowen, K.K., Kim, B.T., Rothstein, J.D. & Dempsey, R.J. (2001) Antisense knockdown of the glial glutamate transporter GLT-1, but not the neuronal glutamate transporter EAAC1, exacerbates transient focal cerebral ischemia-induced neuronal damage in rat brain. J. Neurosci., 21, 1876-1883.
53. Raps, S.P., Lai, J.C.K., Hertz, L. & Cooper, A.J.L. (1989) Glutathione is present in high concentrations in cultured astrocytes but not in cultured neurons. Brain Res., 493, 398-401.
54. Rosenberg, P.A. & Aizenman, E. (1989) Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex. Neurosci. Lett., 103, 162-168.
55. 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. & Welty, D.F. (1996) Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron. 16, 675-686.
56. Sagara, J., Miura, K. & Bannai, S. (1993) Maintenance of neuronal glutathione by glial cells. J. Neurochem., 61, 1672-1676.
57. Sandhu, J.K., Pandey, S., Ribecco-Lutkiewicz, M., Monette, R., Borowy-Borowski, H., Walker, P.R. & Sikorska, M. (2003) Molecular mechanisms of glutamate neurotoxicity in mixed cultures of NT2-derived neurons and astrocytes: protective effects of coenzyme Q10. J. Neurosci. Res., 72, 691-703.
58. Shanker, G., Allen, J.W., Mutkus, L.A. & Aschner, M. (2001) The uptake of cysteine in cultured primary astrocytes and neurons. Brain Res., 902, 156-163.
59. Shanker, G. & Aschner, M. (2001) Identification and characterization of uptake systems for cystine and cysteine in cultured astrocytes and neurons: evidence for methylmercury-targeted disruption of astrocyte transport. J. Neurosci. Res., 66, 998-1002.
60. Sipos, I., Tretter, L. & Adam-Vizi, V. (2003) Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J. Neurochem., 84, 112-118.
61. Sloviter, R.S. & Lowenstein, D.H. (1992) Heat shock protein expression in vulnerable cells of the rat hippocampus as an indicator of excitation-induced neuronal stress. J. Neurosci., 12, 3004-3009.
62. Stohs, S.J. & Bagchi, D. (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med., 18, 321-336.
63. Sugaya, E., Takato, M. & Noda, Y. (1975) Neuronal and glial activity during spreading depression in cerebral cortex of cat. J. Neurophysiol., 38, 822-841.
64. Swanson, R.A. & Graham, S.H. (1994) Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res., 664, 94-100.
65. Swanson, R.A., Shiraishi, K., Morton, M.T. & Sharp, F.R. (1990) Methionine sulfoximine reduces cortical infarct size in rats after middle cerebral artery occlusion. Stroke, 21, 322-327.
66. +: role of glia. Brain Res., 542, 259-265.
67. Szerb, J.C. & Issekutz, B. (1987) Increase in the stimulation-induced overflow of glutamate by fluoroacetate, a selective inhibitor of the glial tricarboxylic cycle. Brain Res., 410, 116-120.
68. Tanaka, J., Toku, K., Zhang, B., Ishihara, K., Sakanaka, M. & Maeda, N. (1999) Astrocytes prevent neuronal death induced by reactive oxygen and nitrogen species. Glia, 28, 85-96.
69. Votyakova, T.V. & Reynolds, I.J. (2001) DeltaPsi (m)-dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem., 79, 266-277.
70. Walz, W. (1989) Role of glial cells in the regulation of the brain ion microenvironment. Prog. Neurobiol., 33, 309-333.
71. Wilson, J.X. (1997) Antioxidant defense of the brain: a role for astrocytes. Can. J. Physiol. Pharmacol., 75, 1149-1163.
72. Yamamoto, Y., Kobayashi, Y. Devi, S.R., Rikiishi, S. & Matsumoto, H. (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol., 128, 63-72.
73. Yoshioka, K., Nisimaru, N., Yanai, S., Shimoda, H. & Yamada, K. (2000) Characteristics of monocarboxylates as energy substrates other than glucose in rat brain slices and the effect of selective glial poisoning - a 31P NMR study. Neurosci. Res., 36, 215-226.
74. Yudkoff, M., Pleasure, D., Cregar, L., Lin, Z.P., Nissim, I., Stern, J. & Nissim, I. (1990) Glutathione turnover in cultured astrocytes: studies with [15N]glutamate. J. Neurochem., 55, 137-145.