Glucose and NADPH oxidase drive neuronal superoxide formation in stroke

Annals of Neurology

Volumn 64, Issue 6, 2008, Pages 654-663

  Suh, Sang Won ^a   Shin, Byung Seop ^a   Ma, Hualong ^a   Van Hoecke, Michaël ^a   Brennan, Angela M ^a   Yenari, Midori A ^a   Swanson, Raymond A ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOCYNIN; DEOXYGLUCOSE; ETHIDIUM; GLUCOSE; PROTEIN P47; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL CULTURE; CEREBROVASCULAR ACCIDENT; CONTROLLED STUDY; FOREBRAIN; GENE DISRUPTION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HEXOSE MONOPHOSPHATE SHUNT; HYPERGLYCEMIA; MALE; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; CELL DEATH; CELLS, CULTURED; GLUCOSE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; STROKE; SUPEROXIDES;

EID: 58149268010     PISSN: 03645134     EISSN: 15318249     Source Type: Journal    
DOI: 10.1002/ana.21511     Document Type: Article

References (43)

1. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 1995;333:1581-1587.
2. Zivin JA, Lyden PD, DeGirolami U, et al. Tissue plasminogen activator. Reduction of neurologic damage after experimental embolic stroke. Arch Neurol 1988;45:387-391.
3. Aronowski J, Strong R, Grotta JC. Reperfusion injury: demonstration of brain damage produced by reperfusion after transient focal ischemia in rats. J Cereb Blood Flow Metab 1997;17:1048-1056.
4. Hallenbeck JM, Dutka AJ. Background review and current concepts of reperfusion injury. Arch Neurol 1990;47:1245-1254.
5. Martini SR, Kent TA. Hyperglycemia in acute ischemic stroke: a vascular perspective. J Cereb Blood Flow Metab 2007;27:435-451.
6. Myers RE, Yamaguchi S. Nervous system effects of cardiac arrest in monkeys. Preservation of vision. Arch Neurol 1977;34:65-74.
7. Parsons MW, Barber PA, Desmond PM, et al. Acute hyperglycemia adversely affects stroke outcome: a magnetic resonance imaging and spectroscopy study. Ann Neurol 2002;52:20 -28.
8. Plum F. What causes infarction in ischemic brain? The Robert Wartenberg Lecture. Neurology 1983;33:222-223.
9. Newell DW, Barth A, Papermaster V, Malouf AT. Glutamate and non-glutamate receptor mediated toxicity caused by oxygen and glucose deprivation in organotypic hippocampal cultures. J Neurosci 1995;15:7702-7711.
10. Rytter A, Cronberg T, Asztely F, et al. Mouse hippocampal organotypic tissue cultures exposed to in vitro "ischemia" show selective and delayed CA1 damage that is aggravated by glucose. J Cereb Blood Flow Metab 2003;23:23-33.
11. Park WS, Chang YS, Lee M. Effects of hyperglycemia or hypoglycemia on brain cell membrane function and energy metabolism during the immediate reoxygenation-reperfusion period after acute transient global hypoxia-ischemia in the newborn piglet. Brain Res 2001;901:102-108.
12. D'Alecy LG, Lundy EF, Barton KJ, Zelenock GB. Dextrose containing intravenous fluid impairs outcome and increases death after eight minutes of cardiac arrest and resuscitation in dogs. Surgery 1986;100:505-511.
13. Venables GS, Miller SA, Gibson G, et al. The effects of hyperglycaemia on changes during reperfusion following focal cerebral ischaemia in the cat. J Neurol Neurosurg Psychiatry 1985;48:663-669.
14. Ribo M, Molina C, Montaner J, et al. Acute hyperglycemia state is associated with lower tPA-induced recanalization rates in stroke patients. Stroke 2005;36:1705-1709.
15. Bruno A, Biller J, Adams HP Jr, et al. Acute blood glucose level and outcome from ischemic stroke. Trial of ORG 10172 in Acute Stroke Treatment (TOAST) Investigators. Neurology 1999;52:280-284.
16. Sugawara T, Chan PH. Reactive oxygen radicals and pathogenesis of neuronal death after cerebral ischemia. Antioxid Redox Signal 2003;5:597-607.
17. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245-313.
18. Serrano F, Kolluri NS, Wientjes FB, et al. NADPH oxidase immunoreactivity in the mouse brain. Brain Res 2003;988:193-198.
19. Tejada-Simon MV, Serrano F, Villasana LE, et al. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol Cell Neurosci 2005;29:97-106.
20. Rhee SG. Cell signaling. H2O2, a necessary evil for cell signaling. Science 2006;312:1882-1883.
21. Klann E. Cell-permeable scavengers of superoxide prevent longterm potentiation in hippocampal area CA1. J Neurophysiol 1998;80:452-457.
22. Hwang JJ, Choi SY, Koh JY. The role of NADPH oxidase, neuronal nitric oxide synthase and poly(ADP ribose) polymerase in oxidative neuronal death induced in cortical cultures by brain-derived neurotrophic factor and neurotrophin-4/5. J Neurochem 2002;82:894-902.
23. Suh SW, Gum ET, Hamby AM, et al. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest 2007;117:910-918.
24. Decoursey TE, Ligeti E. Regulation and termination of NADPH oxidase activity. Cell Mol Life Sci 2005;62:2173-2193.
25. Gupte SA, Levine RJ, Gupte RS, et al. Glucose-6-phosphate dehydrogenase-derived NADPH fuels superoxide production in the failing heart. J Mol Cell Cardiol 2006;41:340-349.
26. Wellons JC 3rd, Sheng H, Laskowitz DT, et al. A comparison of strain-related susceptibility in two murine recovery models of global cerebral ischemia. Brain Res 2000;868:14-21.
27. Jeffs GJ, Meloni BP, Sokolow S, et al. NCX3 knockout mice exhibit increased hippocampal CA1 and CA2 neuronal damage compared to wild-type mice following global cerebral ischemia. Exp Neurol 2008;210:268-273.
28. Suh SW, Aoyama K, Chen Y, et al. Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J Neurosci 2003;23:10681-10690.
29. Budd SL, Castilho RF, Nicholls DG. Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett 1997;415:21-24.
30. Robinson KM, Janes MS, Pehar M, et al. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A 2006;103:15038-15043.
31. Zhao H, Kalivendi S, Zhang H, et al. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 2003;34:1359-1368.
32. Murakami K, Kondo T, Kawase M, et al. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 1998;18:205-213.
33. Schmued LC, Hopkins KJ. Fluoro-jade B: a high affinity fluorescent marker for the localization of neuronal degeneration. Brain Res 2000;874:123-130.
34. Goldberg MP, Choi DW. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 1993;13:3510-3524.
35. Ikemoto A, Bole DG, Ueda T. Glycolysis and glutamate accumulation into synaptic vesicles. Role of glyceraldehyde phosphate dehydrogenase and 3-phosphoglycerate kinase. J Biol Chem 2003;278:5929-5940.
36. Simons JM, Hart BA, Ip Vai Ching TR, et al. Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils. Free Radic Biol Med 1990;8:251-258.
37. He L, Dinger B, Sanders K, et al. Effect of p47phox gene deletion on ROS production and oxygen sensing in mouse carotid body chemoreceptor cells. Am J Physiol Lung Cell Mol Physiol 2005;289:L916-L924.
38. Kawase M, Murakami K, Fujimura M, et al. Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke 1999;30:1962-1968.
39. Bertoni JM. Competitive inhibition of rat brain hexokinase by 2-deoxyglucose, glucosamine, and metrizamide. J Neurochem 1981;37:1523-1528.
40. Guo ZH, Mattson MP. In vivo 2-deoxyglucose administration preserves glucose and glutamate transport and mitochondrial function in cortical synaptic terminals after exposure to amyloid beta-peptide and iron: evidence for a stress response. Exp Neurol 2000;166:173-179.
41. Chan PH, Kawase M, Murakami K, et al. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 1998;18:8292-8299.
42. Wass CT, Lanier WL. Glucose modulation of ischemic brain injury: review and clinical recommendations. Mayo Clin Proc 1996;71:801-812.
43. Ying W, Han SK, Miller JW, Swanson RA. Acidosis potentiates oxidative neuronal death by multiple mechanisms. J Neurochem 1999;73:1549-1556.