Oxygen-inducible glutamate oxaloacetate transaminase as protective switch transforming neurotoxic glutamate to metabolic fuel during acute ischemic stroke

Antioxidants and Redox Signaling

Volumn 14, Issue 10, 2011, Pages 1777-1785

  Rink, Cameron ^a   Gnyawali, Surya ^a   Peterson, Laura ^a   Khanna, Savita ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ASPARTATE AMINOTRANSFERASE; GLUTAMIC ACID; OXYGEN; SMALL INTERFERING RNA;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN TISSUE; CELL RESPIRATION; CELL SURVIVAL; CITRIC ACID CYCLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; GENE VECTOR; HYPOGLYCEMIA; IMMUNOHISTOCHEMISTRY; ISCHEMIA; LENTIVIRINAE; METABOLISM; MOUSE; NERVE DEGENERATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXYGENATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STROKE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ANOXIA; ASPARTATE AMINOTRANSFERASE, CYTOPLASMIC; ASPARTATE AMINOTRANSFERASES; BRAIN; CELL SURVIVAL; CELLS, CULTURED; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MAGNETIC RESONANCE IMAGING; MICE; OXYGEN; POLYMERASE CHAIN REACTION; RATS; RATS, SPRAGUE-DAWLEY; RNA, SMALL INTERFERING; STROKE;

HARNESS; RODENTIA;

EID: 79954580911     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2011.3930     Document Type: Article

References (45)

1. Ahmed N, Nasman P, and Wahlgren NG. Effect of intravenous nimodipine on blood pressure and outcome after acute stroke. Stroke 31: 1250-1255, 2000. (Pubitemid 30351241)
2. Ajito K, Han C, and Torimitsu K. Detection of glutamate in optically trapped single nerve terminals by Raman spectroscopy. Anal Chem 76: 2506-2510, 2004. (Pubitemid 38585716)
3. Appelberg KS, Hovda DA, and Prins ML. The effects of a ketogenic diet on behavioral outcome after controlled cortical impact injury in the juvenile and adult rat. J Neurotrauma 26: 497-506, 2009.
4. Benveniste H, Drejer J, Schousboe A, and Diemer NH. 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, 1984. (Pubitemid 15205893)
5. Campos F, Sobrino T, Ramos-Cabrer P, Argibay B, Agulla J, Perez-Mato M, Rodriguez-Gonzalez R, Brea D, and Castillo J. Neuroprotection by glutamate oxaloacetate transaminase in ischemic stroke: an experimental study. J Cereb Blood Flow Metab Off J Int Soc Cereb Blood Flow Metab, 2011 [Epub ahead of print]; DOI: 10.1038/jcbfm.2011.3.
6. Choi DW. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci Lett 58: 293-297, 1985. (Pubitemid 15230671)
7. Choi DW. Ionic dependence of glutamate neurotoxicity. J Neurosci 7: 369-379, 1987. (Pubitemid 17017466)
8. Collingridge GL and Watkins JC. The NMDA Receptor. Oxford, New York: Oxford University Press, 1994, xii, 503 pp.
9. Curtis DR, Phillis JW, and Watkins JC. Chemical excitation of spinal neurones. Nature 183: 611-612, 1959.
10. D'Aniello A, Fisher G, Migliaccio N, Cammisa G, D'Aniello E, and Spinelli P. Amino acids and transaminases activity in ventricular CSF and in brain of normal and Alzheimer patients. Neurosci Lett 388: 49-53, 2005. (Pubitemid 41569369)
11. Dirnagl U, Iadecola C, and Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22: 391-397, 1999. (Pubitemid 29453643)
12. Eisenberg HM. What do stroke and brain trauma have in common? West J Med 148: 696-697, 1988.
13. Faden AI, Demediuk P, Panter SS, and Vink R. The role of excitatory amino acids and NMDA receptors in traumatic brain injury. Science 244: 798-800, 1989. (Pubitemid 19163864)
14. Fogelholm R, Erila T, Palomaki H, Murros K, and Kaste M. Effect of nimodipine on final infarct volume after acute ischemic stroke. Cerebrovasc Dis 10: 189-193, 2000. (Pubitemid 30219245)
15. Fogelholm R, Palomaki H, Erila T, Rissanen A, and Kaste M. Blood pressure, nimodipine, and outcome of ischemic stroke. Acta Neurol Scand 109: 200-204, 2004. (Pubitemid 38270876)
16. Goldberg MP, Weiss JH, Pham PC, and Choi DW. N-methyl-D-aspartate receptors mediate hypoxic neuronal injury in cortical culture. J Pharmacol Exp Ther 243: 784-791, 1987. (Pubitemid 18011570)
17. Gouix E, Leveille F, Nicole O, Melon C, Had-Aissouni L, and Buisson A. Reverse glial glutamate uptake triggers neuronal cell death through extrasynaptic NMDA receptor activation. Mol Cell Neurosci 40: 463-473, 2009.
18. Haslam RJ and Krebs HA. The metabolism of glutamate in homogenates and slices of brain cortex. Biochem J 88: 566-578, 1963.
19. Henry PG, Adriany G, Deelchand D, Gruetter R, Marjanska M, Oz G, Seaquist ER, Shestov A, and Ugurbil K. In vivo 13C NMR spectroscopy and metabolic modeling in the brain: a practical perspective. Magn Reson Imaging 24: 527-539, 2006.
20. Hirono C, Ito I, Yamagishi S, and Sugiyama H. Characterization of glutamate receptors induced in Xenopus oocytes after injection of rat brain mRNA. Neurosci Res 6: 106-114, 1988. (Pubitemid 19005228)
21. Hsu SS, Meno JR, Gronka R, Kushmerick M, and Winn HR. Moderate hyperglycemia affects ischemic brain ATP levels but not intracellular pH. Am J Physiol 266: H258-H262, 1994.
22. Khanna S, Roy S, Maurer M, Ratan RR, and Sen CK. Oxygen-sensitive reset of hypoxia-inducible factor transactivation response: prolyl hydroxylases tune the biological normoxic set point. Free Radic Biol Med 40: 2147-2154, 2006. (Pubitemid 43903101)
23. Khanna S, Roy S, Park HA, and Sen CK. Regulation of c-Src activity in glutamate-induced neurodegeneration. J Biol Chem 282: 23482-23490, 2007. (Pubitemid 47311965)
24. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, Ratan RR, and Sen CK. Molecular basis of vitamin E action: tocotrienol modulates 12-lipoxygenase, a key mediator of glutamateinduced neurodegeneration. J BiolChem278: 43508-43515, 2003. (Pubitemid 37345974)
25. Khanna S, Roy S, Slivka A, Craft TK, Chaki S, Rink C, Notestine MA, DeVries AC, Parinandi NL, and Sen CK. Neuroprotective properties of the natural vitamin E alphatocotrienol. Stroke 36: 2258-2264, 2005. (Pubitemid 41429256)
26. Khanna S, Venojarvi M, Roy S, and Sen CK. Glutamateinduced c-Src activation in neuronal cells. Methods Enzymol 352: 191-198, 2002. (Pubitemid 41103183)
27. Koppaka SS, Puchowicz, LaManna JC, and Gatica JE. Effect of alternate energy substrates on mammalian brain metabolism during ischemic events. Adv Exp Med Biol 614: 361-370, 2008.
28. Krogsgaard-Larsen P, and Hansen JJ. Excitatory Amino Acid Receptors: Design of Agonists and Antagonists. New York: E. Horwood, 1992, 382 pp.
29. Lee SG, Su ZZ, Emdad L, Gupta P, Sarkar D, Borjabad A, Volsky DJ, and Fisher PB. Mechanism of ceftriaxone induction of excitatory amino acid transporter-2 expression and glutamate uptake in primary human astrocytes. J Biol Chem 283: 13116-13123, 2008.
30. McIlwain H. Glutamic acid and glucose as substrates for mammalian brain. J Ment Sci 97: 674-680, 1951.
31. Murphy TH, Schnaar RL, and Coyle JT. Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake. FASEB J 4: 1624-1633, 1990.
32. Nakanishi S. Molecular diversity of glutamate receptors and implications for brain function. Science 258: 597-603, 1992.
33. Park HA, Khanna S, Rink C, Gnyawali S, Roy S, and Sen CK. Glutathione disulfide induces neural cell death via a 12-lipoxygenase pathway. Cell Death Differ 16: 1167-1179, 2009.
34. Prins ML. Cerebral metabolic adaptation and ketone metabolism after brain injury. J Cereb Blood Flow Metab 28: 1-16, 2008.
35. Rink C, Roy S, Khan M, Ananth P, Kuppusamy P, Sen CK, and Khanna S. Oxygen-sensitive outcomes and gene expression in acute ischemic stroke. J Cereb Blood Flow Metab 30: 1275-1287, 2010.
36. Roy S, Patel D, Khanna S, Gordillo GM, Biswas S, Friedman A, and Sen CK. Transcriptome-wide analysis of blood vessels laser captured from human skin and chronic woundedge tissue. Proc Natl Acad Sci USA 104: 14472-14477, 2007. (Pubitemid 350003285)
37. Sen CK, Khanna S, Roy S, and Packer L. Molecular basis of vitamin E action. Tocotrienol potently inhibits glutamateinduced pp60(c-Src) kinase activation and death of HT4 neuronal cells. J Biol Chem 275: 13049-13055, 2000. (Pubitemid 30241466)
38. Settergren G, Lindblad BS, and Persson B. Cerebral blood flow and exchange of oxygen, glucose, ketone bodies, lactate, pyruvate and amino acids in infants. Acta Paediatr Scand 65: 343-353, 1976.
39. Shigemoto R, Nakanishi S, and Mizuno N. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridization study in adult and developing rat. J Comp Neurol 322: 121-135, 1992.
40. Shigemoto R, Ohishi H, Nakanishi S, and Mizuno N. Expression of the mRNA for the rat NMDA receptor (NMDAR1) in the sensory and autonomic ganglion neurons. Neurosci Lett 144: 229-232, 1992.
41. Stern JR, Eggleston LV, Hems R, and Krebs HA. Accumulation of glutamic acid in isolated brain tissue. Biochem J 44: 410-418, 1949.
42. Sugiyama H, Ito I, and Hirono C. A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature 325: 531-533, 1987. (Pubitemid 17056734)
43. Wahlgren NG, and Lyden P. Neuroprotectants in the treatment of stroke-an overview. J Stroke Cerebrovasc Dis 9: 32-35, 2000.
44. Watkins JC, Collingridge GL, and British Pharmacological Society. The NMDA Receptor. Oxford, New York: IRL Press at Oxford University Press, 1989, xviii, 242 pp.
45. Weil-Malherbe H. Studies on brain metabolism: the metabolism of glutamic acid in brain. Biochem J 30: 665-676, 1936.