Reperfusion damage following focal ischemia: Pathophysiology and therapeutic windows

Clinical Neuroscience

Volumn 4, Issue 4, 1997, Pages 199-212

  Kuroda, Satoshi ^f   Siesjö, Bo K ^a,b,c,d,e  

^a LUND UNIVERSITY   (Sweden)

^b Stroke Council

^c AMERICAN HEART ASSOCIATION   (United States)

^d American Neurological Association   (United States)

^e LUND UNIVERSITY HOSPITAL   (Sweden)

^f NONE

Author keywords

Calcium; Focal ischemia; Free radicals; Mitochondria; PBN; Reperfusion injury

Indexed keywords

INTERCELLULAR ADHESION MOLECULE 1; REACTIVE OXYGEN METABOLITE;

BRAIN ISCHEMIA; HUMAN; MITOCHONDRIAL MEMBRANE; NEUROPATHOLOGY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; REVIEW;

ANIMALS; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; MITOCHONDRIA; REPERFUSION INJURY;

EID: 0030976784     PISSN: 10656766     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (190)

1. Abdul-Rahman A, Agardh C-D, Siesjö BK (1980): Local cerebral blood flow in the rat during severe hypoglycemia and in the recovery period following glucose injection. Acta Physiol Scand 109:307-314.
2. Aliev M, Saks V (1993): Quantitative analysis of the "phosphocreatine shuttle": I. A probability approach to the description of phosphocreatine production in the coupled creatine kinase-ATP/ADP translocase-oxidative phosphorylation reactions in heart mitochondria. Biochim Biophysic Acta 1143:291-300.
3. Almeida A, Allen K, Bates TE, Clark J (1995): Effects of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory-chain in the gerbil brain. J Neurochem 65:1698-1703.
4. Ambrosio G, Zweier J, Duilio C, Kuppusamy P, Santoro G, Elia P, Tritto I, Cirillo P, Condorelli M, Chiariello M, Flaherty J (1993): Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabitt heart subjected to ischemia and reflow. J Biol Chem 25:18532-18541.
5. Astrup J (1982): Energy-requiring cell functions in the ischemic brain. Their critical supply and possible inhibition in protective therapy. J Neurosurg 56:482-497.
6. + at critical levels of brain ischemia. Stroke 8:51-57.
7. Astrup J, Siesjö B, Symon L (1981): Thresholds in cerebral ischemia: The ischemic penumbra. Stroke 12:723-725.
8. Back T, Kohno K, Hossmann K-A (1994): Cortical negative DC deflections following middle cerebral artery occlusion and KCl-induced spreading depression: Effect on blood flow, tissue oxygenation and electroencephalogram. J Cereb Blood Flow Metab 14:12-19.
9. Back T, Ginsberg M, Dietrich W, Watson B (1996): Induction of spreading depression in the ischemic hemisphere following experimental middle cerebral artery occlusion: Effect on infarct morphology. J Cereb Blood Flow Metab 16:202-213.
10. Baird A, Donman G, Austin M, Fitt G, Davis S, McKay W (1994): Reperfusion after thrombolytic therapy in ischemic stroke measured by single-photon emission computed tomography. Stroke 25: 79-85.
11. Barone F, Schmidt B, Hillegass L, Price W, White R, Feuerstein G, Clark R, Lee E, Griswold D, Sarau H (1992): Reperusion increases neutrophils and leukotrien B4 receptor binding in rat focal ischemia. Stroke 23:1337-1348.
12. Bazan NG, Allan G (1996): Platelet-activating factor is both a modulator of synaptic function and a mediator of cerebral injury and inflammation. In Siesjö BK, Wieloch T (eds): Advances in Neurology 71. Philadelphia: Lippincott-Raven Publishers, pp 475-484.
13. Bazan NG, Squinto SP, Braquet P, Panette T, Marcheselli VL (1991): Platelet-activating factor and polyunsaturated fatty acids in cerebral ischaemia or convulsions: Intracellular PAF-binding sites and activation of a FOS/JUN/AP-1 transcriptional signaling system. Lipids 26:1236-1242.
14. Beckman JS (1991): The double-edge role of nitric oxide in brain function and superoxide-mediated injury. J Dev Physiol 15:53-59.
15. Beckman JS, Ye X Chen J, Conger K (1996): The interactions of nitric oxide with oxygen radicals and scavengers in cerebral ischaemic injury. In Siesjö BK, Wieloch T (eds): Advances in Neurology 71. New York: Raven Press, pp 339-351.
16. Bernardi P, Broekemeier KM, Pfeiffer DR (1994): Recent progress on regulation of the mitochondrial permeability transition pore: A cyclosporin-sensitive pore in the inner mitochondrial membrane. J Bioenerg Biomembr 26:509-517.
17. Bogaert Y, Rosenthal R, Fiskum G (1994): Postischemic inhibition of cerebral cortex pyruvate dehydrogenase. Free Radical Biol Med 6:811-820.
18. Bondy S, LeBel C (1993): The relationship between excitotoxicity and oxidative stress in the central nervous system. Free Radical Biol Med 14:633-642.
19. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton S (1995): 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 culture. Proc Natl Acad Sci USA 92:7162-7166.
20. Branston N, Symon L, Crockard H, Pasztor E (1974): Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp Neurol 45:195-208.
21. Broekemeier KM, Pfeiffer DR (1995): Inhibition of the mitochondrial permeability transition by cyclosporin A during long time frame experiments: Relationship between pore opening and the activity of mitochondrial phospholipases. Biochemistry 34:16440-16449.
22. Brott T, Haley Jr E, Levy D, Barsan W, Broderick J, Sheppard G, Spilker J, Kongable G, Massey S, Reed R, Marier J (1992): Urgent therapy for stroke. Part I. Pilot study of tissue plasminogen activator administered within 90 minutes. Stroke 23:632-640.
23. Buchan A, Xue D, Slivka A (1992): A new model of temporary focal neocortical ischemia in the rat. Stroke 23:273-279.
24. Cao W, Carney J, Duchon A, Floyd R, Chevion M (1988): Oxygen free radical involvement in ischemia and reperfusion injury to brain. Neurosci Lett 88:233-238.
25. Cao X, Phillis J (1994): α-Phenyl-tert-butyl-nitrone reduced cortical infarct and edema in rats subjected to focal ischemia. Brain Res 644:267-272.
26. Carney J, Floyd R (1991): Protection against oxidative damage to CNS by α-phenyl-tert-butyl nitrone (PBN) and other spin trapping agents: A novel series of nonlipid free radical scavengers. J Mol Neurosci 3:47-57.
27. Cazevieille C, Muller A, Meynier F, Bonne C (1993): Superoxide and nitric oxide cooperation in hypoxia/reoxygenation-induced neuron injury. Free Radical Biol Med 14:389-395.
28. Chen J, Weinstein P, Graham S (1995): Attenuation of postischemic brain hypoperfusion and reperfusion injury by the cyclooxygenase-lipoxygenase inhibitor BW755C. J Neurosurg 83:99-104.
29. Chopp M, Zhang R, Chen H, Li Y, Jiang Y, Rusche R (1994): Postischemic administration of an anti-Mac-1 antibody reduces ischemic cell damage after transient middle cerebral artery occlusion in rats. Stroke 25:869-876.
30. Christensen T, Bruhn T, Balchen T, Diemer NH (1994): Evidence for formation of hydroxyl radicals during reperfusion after global cerebral ischaemia in rats using salicylate trapping and microdialysis. Neurobiol Dis 1:131-138.
31. Cleeter M, Cooper J, Darley-Usmar V, Moncada S, Schapira A (1994): Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. FEBS Lett 345:50-54.
32. Connolly EJ, Winfree C, Springer T, Naka Y, Liao H, Yan S, Stern D, Solomon R, Gutierretz-Ramos J, Pinsky D (1996): Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest 97:209-216.
33. Coyle J, Puttfarcken P (1993): Oxidative stress, glutamate, and neurodegenerative disorders. Science 262:689-695.
34. 2+ dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 255:357-360.
35. Daum G (1985): Lipids of mitochondria. Biochim Biophys Acta 822:1-42.
36. Dawson V, Dawson T, London E (1991): Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88:6368-6371.
37. del Zoppo GJ (1994): Microvascular changes during cerebral ischaemia and reperfusion. Cerebrovasc Brain Metab Rev 6:47-96.
38. del Zoppo GJ, Schmid-Schönbein GW, Mori E, Copeland BR, Chang CM (1991): Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke 22:1276-1283.
39. Deshpande JK, Siesjö BK, Wieloch T (1987): Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia. J Cereb Blood Flow Metab 7:89-95.
40. Dezsi L, Greenberg J, Sladky J, Araki N, Hamar J, Reivich M (1994): Prolonged effects of MK-801 in the cat during focal cerebral ischemia and recovery: Survival, EEG activity and histopathology. J Neurol Sci 121:110-120.
41. Dirnagl U (1993): Cerebral ischemia: The microcirculation as trigger and target. In Kogure K, Hossmann K-A, Siesjö BK (eds): Progress in Brain Research, 96. Amsterdam: Elsevier Science Publisher, pp 49-65.
42. Dirnagl U, Lindauer U, Them A, Schreiber S, Pfister H-W, Koedel U, Reszka R, Freyer D, Villringer A (1995): Global cerebral ischemia in the rat: Online monitoring of oxygen free radical production using chemiluminescence in vivo. J Cereb Blood Flow Metab 15:929-940.
43. Duchen M, McGuinness O, Brown L, Crompton M (1993): On the involvement of a cyclosporin A sensitive mitochondrial pore in myocardial reperfusion injury. Cardiovasc Res 27:1790-1794.
44. Dugan L, Sensi S, Canzoniero L, Handran S, Rothman S, Lin T-S, Goldberg M, Choi D (1995): Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J Neurosci 15:6377-6388.
45. Dux E, Mies G, Hossmann K-A, Siklos L (1987): Calcium in the mitochondria following brief ischemia of gerbil brain. Neurosci Lett 78:295-300.
46. +: Implications for neurodegeneration. J Neurochem 63:584-591.
47. Erecinska M, Silver IA (1994): Ions and energy in mammalian brain. In: Progress Neurobiol, 43. New York: Elsevier Science Ltd., pp 37-71.
48. Feuerstein GZ, Liu T, Barone FC (1994): Cytokines, inflammation, and brain injury: Role of tumor necrosis factor-α. Cerebrovasc Brain Metab Rev 6:341-360.
49. Floyd RA (1990): Role of oxygen free radicals in carcinogenesis and brain ischemia. FASEB J 4:2587-2597.
50. Floyd RA, Carney JM (1992): Free radical damage to protein and DNA: Mechanisms involved and relevant observations on brain undergoing oxidative stress. Ann Neurol 32:S22-S27.
51. Folbergrová J, Memezawa H, Smith M-L, Siesjö BK (1992): Focal and perifocal changes in tissue energy state during middle cerebral artery occlusion in normo- and hyperglycemic rats. J Cereb Blood Flow Metab 12:25-33.
52. Folbergrová J, Kiyota Y, Pahlmark K, Memezawa H, Smith M-L, Siesjö BK (1993): Does ischemia with reperfusion lead to oxidative damage to proteins in the brain? J Cereb Blood Flow Metab 13:145-152.
53. Folbergrová J, Zhao Q, Katsura K, Siesjö BK (1995): N-tert-Butyl-α-phenylnitrone improves recovery of brain energy state in rats following transient focal ischemia. Proc Natl Acad Sci USA 92:5057-5061.
54. Garcia JH, Liu K-F, Yoshida Y, Lian J, Chen S, del Zoppo G (1994): Influx of leukocytes and platelets in an evolving brain infarct. Am J Pathol 144:188-199.
55. Garcia JH, Liu K-F, Relton JK (1995): Interleukin-1 receptor antagonist decreases the number of necrotic neurons in rats with middle cerebral artery occlusion. Am J Pathol 147:1477-1486.
56. Gehrmann J, Banati R, Wiessnert C, Hossmann K-A, Kreutzberg G (1995): Reactive microglia in cerebral ischaemia: an early mediator of tissue damage? Neuropathol Appl Neurobiol 21:277-289.
57. Gill R, Andine O, Hillered L, Persson L, Hagberg H (1992): The effect of MK-801 on cortical spreading depression in the penumbra zone following focal ischemia in the rat. J Cereb Blood Flow Metab 12:371-379.
58. Ginsberg M, Busto R (1989): Rodent models of cerebral ischemia. Stroke 20:1627-1642.
59. Griffiths E, Halestrap A (1991): Further evidence that cyclosporin A protects mitochondria from calcium overload by inhibiting a matrix peptidyl-prolyl cis-trans isomerase. Implication for the immunosuppressive and toxic effects of cyclosporin. Biochem J 274:611-614.
60. Gunter T, Pfeiffer D (1990): Mechanisms by which mitochondria transport calcium. Am J Physiol 258:C755-786.
61. Hakim AM (1987): The cerebral ischemia penumbra. Can J Neurol Sci 14:557-559.
62. Haley Jr E, Levy D, Brott T, Sheppard G, Wong M, Kongable G, Torner J, Marler J (1992): Urgent therapy for stroke. Part II. Pilot study of tissue plasminogen activator administered 91-180 minutes from onset. Stroke 23:641-645.
63. Hall E, Braughler J (1989): Central nervous system trauma and stroke. II. Physiological and pharmacological evidence for involvement of oxygen radicals and lipid peroxidation. Free Radic Biol Med 6:303-313.
64. Hallenbeck JM (1996): Inflammatory reactions at the blood-endothelial interface in acute stroke. In Siesjö BK, Wieloch T (eds): Advances in Neurology, 71. Philadelphia: Lippincott-Raven Publishers, pp 281-300.
65. Halliwell B (1992): Reactive oxygen species and the central nervous system. J Neurochem 59:1609-1623.
66. Halliwell B, Gutteridge JMC (1985): Oxygen radicals and the nervous system. Trends Neurosci 8:22-26.
67. Hansen AJ (1985): Effect of anoxia on ion distribution in the brain. Physiol Rev 65:101-148.
68. Harris R, Symon L (1984): Extracellular pH, potassium, and calcium activities in progressive ischaemia of rat cortex. J Cereb Blood Flow Metab 4:178-186.
69. Hillered L, Ernster L (1983): Respiratory activity of isolated rat brain mitochondria following in vitro exposure to oxygen radicals. J Cereb Blood Flow Metab 3:207-214.
70. Hillered L, Smith ML, Siesjö BK (1985): Lactic acidosis and recovery of mitochondrial function following forebrain ischemia in the rat. J Cereb Blood Flow Metab 5:259-266.
71. Hoehn-Berlage M, Norris D, Kohno K, Mies G, Leibfritz D, K-A H (1995): Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: The relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances. J Cereb Blood Flow Metab 15:1002-1011.
72. Hossmann K-A (1993): Disturbances of cerebral protein synthesis and ischemic cell death. Prog Brain Res 96:161-177.
73. Hossmann K-A (1994a): Glutamate-mediated injury in focal cerebral ischemia: The excitotoxin hypothesis revised. Brain Pathol 4:23-36.
74. Hossmann K-A (1994b): Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557-565.
75. Huang Z, Huang P, Panahian N, Dalkara T, Fishman M, Moskowitz M (1994): Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265:1883-1885.
76. Iadecola C, Zhang F, Xu S, Casey R, Ross M (1995): Inducible nitric oxide synthase gene expression in brain following cerebral ischemia. J Cereb Blood Flow Metab 15:378-384.
77. Iijima T, Mies C, Hossmann K-A (1992): Repeated negative DC deflections in rat cortex following middle cerebral artery occlusion are abolished by MK-801: Effect on volume of ischemic injury. J Cereb Blood Flow Metab 12:727-733.
78. Kägström E, Smith M-L, Siesjö BK (1983): Recirculation in the rat brain following incomplete ischaemia. J Cereb Blood Flow Metab 3:170-182.
79. Kaplan B, Brint S, Tanabe J, Jacewicz M, Wang X-J, Pulsinelli W (1991): Temporal thresholds for neocortical infarction in rats subjected to reversible focal cerebral ischemia. Stroke 22:1-8.
80. Katayama Y, Welsh F (1989): Effect of dichloroacetate on regional energy metabolites and pyruvate dehydrogenase activity during ischemia and reperfusion in gerbil brain. J Neurochem 52: 1817-1822.
81. Kirino T (1982): Delayed neuronal death in the gerbil hippocampus following transient ischemia. Brain Res 239:57-69.
82. Kochanek PM, Hallenbeck JM (1992): Polymorphonuclear leukocytes and monocytes/macrophages in the pathogenesis of cerebral ischemia and stroke. Stroke 23:1367-1379.
83. Kohno K, Back T, Hoehn-Berlage M, Hossmann K-A (1995a): A modified rat model of middle cerebral artery thread occlusion under electrophysiological control for magnetic resonance investigations. Magn Reson Imaging 13:65-71.
84. Kohno K, Hoehn-Berlage M, Mies G, Back T, Hossmann K-A (1995b): Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction. Magn Reson Imaging 13:73-80.
85. Kontos H (1985): Oxygen radicals in cerebral vascular injury. Circ Res 57:508-516.
86. Kristían T, Siesjö BK (1996): Calcium-related damage in ischemia. Life Sci 59:357-367.
87. Kristían T, Gidö G, Siesjö BK (1995): Temporal profile of extracellular ion concentrations after transient middle cerebral artery occlusion in the rats. In: Abstracts of 25th Annual Meeting of Society of Neuroscience Part 1, pp 216.
88. Kuroda S, Katsura K, Tsuchidate R, Siesjö BK (1996a): Secondary bioenergetic failure after transient focal ischemia is due to mitochondrial injury. Acta Physiol Scand 156:149-150.
89. Kuroda S, Katsura K, Hillered L, Bates TE, Siesjö BK (1996b): Delayed treatment with α-phenyl-N-tert-butyl nitrone (PBN) attenuates secondary mitochondrial dysfunction after transient focal cerebral ischemia in the rat. Neurobiol Dis 3:149-157.
90. Kuroiwa T, Shibutani M, Okeda R (1988): Blood-brain barrier disruption and exacerbation of ischemic brain edema after restoration of blood flow in experimental focal cerebral ischemia. Acta Neuropathol 76:62-70.
91. Kurup C, Kumaroo K, Dutka A (1990): Influence of cerebral ischemia and post-ischemic reperfusion on mitochondrial oxidative phosphorylation. J Bioenerget Biomembr 22:61-78.
92. Lafon-Cazal M, Pietri S, Culcasi M, Bockaert J (1993): NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537.
93. Lindvall O, Ernfors P, Bengzon J, Kokaia Z, Smith M-L, Siesjö BK (1992): Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in adult rat brain following cerebral ischemia and hypoglycemia coma. Proc Natl Acad Sci USA 89:648-652.
94. Malinski T, Bailey F, Zhang Z, Chopp M (1993): Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 13:335-338.
95. Margaill I, Parmentier S, Callebert J, Allix M, Boulu R, Plotkine M (1996): Short therapeutic window for MK-801 in transient focal cerebral ischemia in normotensive rats. J Cereb Blood Flow Metab 16:107-113.
96. Matsumoto K, Lo E, Pierce A, Halpern E, Newcomb R (1996): Secondary elevation of extracellular neurotransmitter amino acids in the reperfusion phase following focal cerebral ischemia. J Cereb Blood Flow Metab 16:114-124.
97. Matsuo Y, Onodera H, Shiga Y, Nakamura M, Ninomiya M, Kihara T, Kogure K (1994a): Correlation between myeloperoxidase-quantified neutrophil accumulation and ischemic brain injury in the rat. Effects of neutrophil depletion. Stroke 25:1469-1475.
98. Matsuo Y, Onodera H, Shiga Y, Shozuhara H, Ninomiya M, Kihara T, Tamatani T, Miyasaka M, Kogure K (1994b): Role of cell adhesion molecules in brain injury after transient middle cerebral artery occlusion in the rat. Brain Res 656:344-352.
99. Matsuo Y, Kihara T, Ikeda M, Ninomiya M, Onodera H, Kogure K (1995): Role of neutrophils in radical production during ischemia and reperfusion of the rat brain: Effect of neurtrophil depletion on extracellular ascorbyl radical formation. J Cereb Blood Flow Metab 15:941-947.
100. McCord J (1985): Oxygen-derived free radicals in postischaemic tissue injury. N Engl J Med 312:159-163.
101. McNamara J, Fridovich I (1993): Did radicals strike Lou Gehrig? Nature 362: 20-21.
102. Memezawa H, Minamisawa H, Smith M-L, Siesjö BK (1992a): Ischemic penumbra in a model of reversible middle cerebral artery occlusion in the rat. Exp Brain Res 89:67-78.
103. Memezawa H, Smith M-L, Siesjö BK (1992b): Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke 23:552-559.
104. Memezawa H, Zhao Q, Smith M, Siesjö B (1995): Hyperthermia nullifies the ameliorating effect of dizocilpine maleate (MK-801) in focal cerebral ischemia. Brain Res 670:48-52.
105. Mori E, Yoneda Y, Tabuchi M, Yoshida T, Ohkawa S, Ohsumi Y, Kitano K, Tsutsumi A, Yamadori A (1992): Intravenous recombinant tissue plasminogen activator in acute carotid artery territory stroke. Neurology 42:976-982.
106. Morimoto T, Globus M-T, Busto R, Martinez E, Ginsberg M (1996): Simultaneous measurement of salicylate hydroxylation and glutamate release in the penumbral cortex following transient middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 16:92-99.
107. Nagasawa H, Kogure K (1989): Correlation between cerebral blood flow and histologic changes in a new rat model of middle cerebral artery occlusion. Stroke 20:1037-1043.
108. Nagasawa H, Kogure K (1990): Uncoupling of blood flow and glucose metabolism in the neighboring postischemic edematous brain area. In Long DEA (ed): Advances in Neurology, 52. New York: Raven Press, pp 63-71.
109. Nakahara I, Kikuchi H, Taki W, Nishi S, Kito M, Yonekawa Y, Goto Y, Ogata N (1992): Changes in major phospholipids of mitochondria during postischemic reperfusion in rat brain. J Neurosurg 76:244-250.
110. Nakai H, Yamomoto Y, Diksic M, Worsley K, Takara E (1988): Triple-tracer autoradiography demonstrates effects of hyperglycemia on cerebral blood flow, pH, and glucose utilization in cerebral ischemia of rats. Stroke 19:764-772.
111. Nakashima M, Yamashita K, Kataoka Y, Yamashita Y, Niwa M (1995): Time course of nitric oxide synthase activity in neuronal, glial, and endothelial cells of rat striatum following focal cerebral ischemia. Cell Mol Neurobiol 15:341-349.
112. Nedergaard M, Astrup J (1986): Infarct rim: Effect of hyperglycemia on direct current potential and [14C]2-deoxyglucose phosphorylation. J Cereb Blood Flow Metab 6:607-615.
113. Nedergaard M, Hansen AJ (1993): Characterization of cortical depolarizations evoked in focal cerebral ischemia. J Cereb Blood Flow Metab 13:568-574.
114. Nedergaard M, Jakobsen J, Diemer N (1988): Autoradiographic determination of cerebral glucose content, blood flow, and glucose utilization in focal ischemia of the rat brain: Influence of the plasma glucose concentration. J Cereb Blood Flow Metab 8:100-108.
115. Nelson C, Wei E, Povlishock J, Kontos H, Moskowitz M (1992): Oxygen radicals in cerebral ischemia. Am J Physiol 263: H1356-H1362.
116. Nikolics K, Hefti F, Thomas GR, Gluckman PD (1996): Trophic factors and their role in postischemic brain. In Siesjö BK, Wieloch T (eds): Advances in Neurology, 71. Philadelphia: Lippincott-Raven Publishers, pp 389-403.
117. Nowak TS Jr (1990): Protein synthesis and the heat shock/stress response after ischemia. Cerebrovasc Brain Metab Rev 2:345-366.
118. Okada Y, Copeland B, Mori E, Tung M-M, Thomas W, del Zoppo GJ (1994): P-selectin and intracellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 25:202-211.
119. Oliver C, Starke-Reed P, Stadtman E, Liu G, Carney J, Floyd R (1990): Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia/ reperfusion-induced injury to gerbil brain. Proc Natl Acad Sci USA 87:5144-5147.
120. Orrenius S, Burkitt MJ, Kass GEN, Dypbukt JM, Nicotera P (1992): Calcium ions and oxidative cell injury. Ann Neurol 32:533-S42.
121. Packer M, Murphy M (1995): Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin-A-sensitive mitochondrial calcium efflux and depolarisation. Eur J Biochem 234:231-239.
122. Pahlmark K, Siesjö BK (1997): Effects of the spin trap α-phenyl-N-tert-butyl nitrone (PBN) in transient forebrain ischaemia in the rat. Acta Physiol Scand. (in press)
123. Pahlmark K, Folbergrová J, Smith M-L, Siesjö BK (1993): Effects of dimethylthiourea on selective neuronal vulnerability in forebrain ischemia in rats. Stroke 24:731-737.
124. Pettigrew LC, Grotta JC, Rhoades HM, Wu KK (1989): Effect of thromboxane synthase inhibition on eicosanoid levels and blood flow in ischemic rat brain. Stroke 20:627-632.
125. Phillis J, Clough-Helfman C (1990): Protection from cerebral ischemic injury in gerbils with the spin trap agent N-tert-butyl-α-phenylnitrone (PBN). Neurosci Lett 116:315-319.
126. Piantadosi C, Zhang J (1996): Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke 27:327-332.
127. Pulsinelli WA, Levy D, Duffy T (1982): Regional cerebral blood flow and glucose metabolism following transient forebrain ischemia. Ann Neurol 11:499-509.
128. Radi R, Rodriguez M, Castro L, Telleri R (1994): Inhibition of mitochondrial electron transport by peroxynitrite. Arch Biochem Biophys 308:89-95.
129. Rehncrona S, Mela L, Siesjö BK (1979): Recovery of brain mitochondrial function in the rat after complete and incomplete cerebral ischemia. Stroke 10:437-446.
130. Relton J, Rothwell N (1992): Interleukin-1 receptor antagonist inhibits ischemic and excitotoxic neuronal damage in the rat. Brain Res Bull 29:243-246.
131. Reynolds I, Hastings T (1995): Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J Neurosci 15:3318-3327.
132. 2+ homeostasis, cell death, proliferation, and differentiation. Chem-Biol Interact 77:1-23.
133. 2t: Their relationship to apoptosis and oncogenesis. FEBS Lett 325:104-107.
134. Richter C, Gogvadze V, Schlapbach R, Schweizer M, Schlegel J (1994): Nitric oxide kills hepatocytes by mobilizing mitochondrial calcium. Biochem Biophysic Res Commun 205:1143-1150.
135. Richter C, Gogvadze V, Laffranchi R, Schlapbach R, Schweizer M, Suter M, Walter P, Yaffee M (1995): Oxidants in mitochondria: From physiology to diseases. Biochim Biophys Acta 1271:67-74.
136. 2) activity in gerbil brain: Enhanced activities of cytosolic, mitochondrial, and microsomal forms after ischemia and reperfusion. J Neurosci 11: 1829-1836.
137. Schulz J, Henshaw D, Siwek D, Jenkins B, Ferrante R, Cipolloni P, Kowall N, Rosen B, Beal M (1995a): Involvement of free radicals in excitotoxicity in vivo. J Neurochem 64:2239-2247.
138. Schulz J, Matthews R, Jenkins B, Brar P, MF B (1995b): Improved therapeutic window for treatment of histotoxic hypoxia with a free radical spin trap. J Cereb Blood Flow Metab 15:948-952.
139. Schweizer M, Richter C (1994): Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension. Biochem Biophysic Res Commun 204:169-175.
140. Selman W, Crumrine R, Ricci A, LaManna J, Ratcheson R, Lust W (1990a): Impairment of metabolic recovery with increasing periods of middle cerebral artery occlusion in rats. Stroke 21:467-471.
141. Selman W, Ricci A, Crumrine R, LaManna J, Ratcheson R, Lust W (1990b): The evolution of focal ischemic damage: A metabolic analysis. Metabol Brain Dis 5:33-44.
142. Sen S, Phillis J (1993): Alpha-phenyl-tert-butyl-nitrone (PBN) attenuates hydroxy radical production during ischemia-reperfusion injury of rat brain: A EPR study. Free Radic Res Comm 19:255-265.
143. Shigeno T, Teasdale G, McCulloch J, Graham D (1985): Recirculation model following MCA occlusion in rats. Cerebral blood flow, cerebrovascular permeability, and brain edema. J Neurosurg 63:272-277.
144. Shug A, Subramanian R (1987): Modulation of adenine nucleotide translocase activity during myocardial ischemia. Z Kardiol 76 (Suppl. 5):26-33.
145. Siesjö BK (1992a): Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J Neurosurg 77:169-184.
146. Siesjö BK (1992b): Pathophysiology and treatment of focal cerebral ischemia. Part II: Mechanisms of damage and treatment. J Neurosurg 77:337-354.
147. Siesjö BK, Bengtsson F (1989): Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: A unifying hypothesis. J Cereb Blood Flow Metab 9:127-140.
148. Siesjö BK, Bendek G, Koide T, Westerberg E, Wieloch T (1985): Influence of acidosis on lipid peroxidation in brain tissues in vitro. J Cereb Blood Flow Metab 5:253-258.
149. Siesjö BK, Ekholm A, Katsura K, Memezawa H, Ohta S, Smith M-L (1990): The type of ischemia determines the pathophysiology of brain lesions and the therapeutic response to calcium channel blockade. In Krieglstein J, Oberpichler H (eds): Pharmacology of Cerebral Ischemia. Stuttgart: Wissenschaftliche Verlagsgessellschaft GmbH., pp 79-88.
150. Siesjö BK, Katsura K, Kristian T (1995a): The biochemical basis of cerebral ischemic damage. J Neurosurg Anesthesiol 7:47-52.
151. Siesjö BK, Katsura K, Zhao Q, Folbergrova J, Pahlmark K, Siesjo P, Smith M-L (1995b): Mechanisms of secondary brain damages in global and focal ischemia: A speculative synthesis. J Neurotrauma 12:943-956.
152. Siesjö BK, Zhao Q, Pahlmark K, Siesjo P, Katsura K, Folbergrova J (1995c): Glutamate, calcium, and free radicals as mediators of ischemic brain damage. Ann Thorac Surg 59:1316-1320.
153. Siesjö BK, Kristian T, Katsura K (1995d): The role of calcium in delayed postischemic brain damage. In Moskowitz MA, Caplan LR (eds): Cerebrovascular Diseases. Nineteenth Princeton Stroke Conference. New York: Raven Press, pp 353-370.
154. + in the hippocampus during recovery from short-term, transient ischemia. J Cereb Blood Flow Metab 12:759-772.
155. Sims N (1991): Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. J Neurochem 56:1836-1844.
156. Sims N, Pulsinelli W (1987): Altered mitochondrial respiration in selectively vulnerable brain subregions following transient forebrain ischemia in the rat. J Neurochem 49:1367-1374.
157. Smith M-L, Auer R, Siesjö BK (1984): The density and distribution of ischemic brain injury in the rat following 2-10 min of forebrain ischemia. Acta Neuropathol (Berl) 64:319-332.
158. Soussi B, Idstrom-JP, Schersten T, Bylund-Fellenius A (1990): Cytochrome c oxidase and caardiolipin alterations in response to skeletal muscle ischemia and reperfusion. Acta Physiol Scand 138:107-114.
159. Strong AJ, Venables GS, Gibson G (1983): The cortical ischaemic penumbra associated with occlusion of the middle cerebral artery in the cat. I. Topography of changes in blood flow, potassium ion activity, and EEG. J Cereb Blood Flow Metab 3:86-96.
160. Sun D, Gilboe D (1994): Ischemia-induced changes in cerebral mitochondrial free fatty acids, phospholipids, and respiration in the rat. J Neurochem 62:1921-1928.
161. Sundt TM, Michenfelder JD (1972): Focal transient cerebral ischemia in the squirrel monkey. Effect of brain adenosine triphosphate and lactate levels with electrocorticographic and pathologic correlation. Circ Res 30:703-712.
162. Symon L, Pasztor E, Branston N (1974): The distribution and density of reduced cerebral blood flow following acute middle cerebral artery occlusion: An experimental study by the technique of hydrogen clearance in baboons. Stroke 5:355-364.
163. 14C]iodoantipyrine autoradiographic study. Brain Res 691:160-168.
164. 14C-iodoantypyrine autoradiography following middle cerebral artery occlusion. J Cereb Blood Flow Metab 1:61-69.
165. Tsuchidate R, He Q-P, Smith M-L, Siesjö BK (1996): Regional cerebral blood flow during and following 2 hours of middle cerebral artery occlusion in the rat (submitted). J Cereb Blood Flow Metab
166. Uchino H, Elmer E, Uchino K, Siesjo BK (1995): Cyclosporin A dramatically ameliorates CA1 hippocampal damage following transient forebrain ischaemia in the rat. Acta Physiol Scand 155:469-471.
167. Vlessis A, Widener L, Bartos D (1990): Effect of peroxide, sodium, and calcium on brain mitochondrial respiration in vitro: Potential role in cerebral ischemia and reperfusion. J Neurochem 54:1412-1418.
168. von Kummer R, Hacke W (1992): Safety and efficacy of intravenous tissue plasminogen activator and heparin in acute middle cerebral artery stroke. Stroke 23:646-652.
169. Wagner K, Kleinholz M, Myers R (1990a): Delayed decrease in specific brain mitochondrial electron transfer complex activities and cytochrome concentrations following anoxia/ischemia. J Neurosurg Sci 100:142-151.
170. Wagner K, Kleinholz M, Myers R (1990b): Delayed onset of neurological deterioration following anoxia/ischemia coincides with appearance of impaired brain mitochondrial respiration and decreased cytochrome oxidase activity. J Cereb Blood Flow Metab 10:417-423.
171. Wieloch T, Bergstedt K, Hu BR (1993): Protein phosphorylation and the regulation of mRNA translation following cerebral ischemia. In Kogure K, Hossmann K-A, Siesjö BK (eds): Progress in Brain Research, 96. Amsterdam: Elsevier Science Publishers, pp 179-191.
172. Williams FM (1994): Role of neutrophils in reperfusion injury. In Halliwell PG, William TJ (eds): Immunopharmacology of Neutrophils. London: Academic Press, pp 245-258.
173. Winn RK, Sharar SR, Vedder NB, Harlan JM (1995): Leukocytes and endothelial adhesion molecules in ischaemia/reperfusion injuries. In: Wiley, Chichester Ciba Foundation Symposium, 189: Cell adhesion and human disease, pp 63-76.
174. Yang C-S, Lin N-N, Tsai P-J, Liu L, Kuo J-S (1996): In vivo evidence of hydroxyl radical formation induced by elevation of extracellular glutamate after cerebral ischemia in the cortex of anesthetized rats. Free Radical Biol Med 20:245-250.
175. Yang G, Betz A (1994): Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 25:1658-1665.
176. Yang G, Chan P, cen J, Carlson E, Chen S, Weinstein P, Epstein C, Kamii H (1994a): Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25:165-170.
177. Yang G, Chan P, Chen S, Babuna O, Simon R, Weinstein P (1994b): Reduction of vasogenic edema and infarction by MK-801 in rats after temporary focal cerebral ischemia. Neurosurgery 34:339-345.
178. Zaidan E, Sims N (1993): Selective reductions in the activity of the pyruvate dehydrogenase complex in mitochondria isolated from brain subrogions following forebrain ischemia in rats. J Cereb Blood Flow Metab 13:98-104.
179. Zaidan E, Sims N (1994): The calcium content of mitochondria from brain subregions following short-term forebrain ischemia and recirculation in the rat. J Neurochem 63:1812-1819.
180. Zamzami N, Marchetti P, Castedo M (1995a): Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J Exp Med 81:1661-1672.
181. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin S, Petit P, Mignotte B, Kroemer G (1995b): Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367-377.
182. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G (1996): Mitochondrial control of nuclear apoptosis. J Exp Med 183:1533-1544.
183. Zhang R, Chopp M, Zaloga C, Zhang Z, Jiang N, Guatam S, Tang W, Tsang W, Anderson D, Manning A (1995a): The temporal profiles of ICAM-I protein and mRNA expression after transient MCA occlusion in the rat. Brain Res 682:182-188.
184. Zhang R, Chopp M, Jiang N, Tang W, Prostak J, Manning A, Anderson D (1995b): Anti-intercellular adhesion molecule-1 antibody reduces ischemic cell damage after transient but not permanent middle cerebral artery occlusion in the Wistar rat. Stroke 26:1438-1443.
185. Zhang X Marcillat O, Giulivi C, Ernster L, Davies K (1990): The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J Biol Chem 265:16330-16336.
186. Zhang Z, Chopp M, Zaloga C, Pollock J, Forstermann U (1993): Cerebral endothelial nitric oxide synthase expression after focal cerebral ischemia in rats. Stroke 24:2016-2022.
187. Zhang Z, Chopp M, Tang W, Jiang N, Zhang R (1995): Postischemic treatment (2-4 h) with anti-CD11b and anti-CD18 monoclonal antibodies are neuroprotective after transient (2h) focal cerebral ischemia in the rat. Brain Res 698:79-85.
188. Zhao Q, Pahlmark K, Smith M-L, Siesjö BK (1994): Delayed treatment with the spin trap a-phenyl-N-tert-butyl nitrone (PBN) reduced infarct size following transient middle cerebral artery occlusion in rats. Acta Physiol Scand 152:349-350.
189. Zini I, Tomasi A, Grimaldi R, Vannini V, Agnati LF (1992): Detection of free radicals during brain ischemia and reperfusion by spin trapping and microdialysis. Neurosci Lett 138:279-282.
190. Zoratti M, Szabo I (1995): The mitochondrial permeability transition. Biochim Biophys Acta 1241:139-176.