Oxidative stress in ischemic brain damage: Mechanisms of cell death and potential molecular targets for neuroprotection

Antioxidants and Redox Signaling

Volumn 14, Issue 8, 2011, Pages 1505-1517

  Chen, Hai ^a   Yoshioka, Hideyuki ^a   Kim, Gab Seok ^a   Jung, Joo Eun ^a   Okami, Nobuya ^a   Sakata, Hiroyuki ^a   Maier, Carolina M ^a   Narasimhan, Purnima ^a   Goeders, Christina E ^a   Chan, Pak H ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; DISUFENTON SODIUM; MANGANESE SUPEROXIDE DISMUTASE; OXIDIZING AGENT; OXYGEN RADICAL; PLACEBO; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

APOPTOSIS; BLOOD BRAIN BARRIER; BRAIN ISCHEMIA; CELL DAMAGE; CELL DEATH; CELL SURVIVAL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; EXCITOTOXICITY; HUMAN; MITOCHONDRIAL DYSFUNCTION; MITOCHONDRIAL TOXICITY; NEUROPROTECTION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; STROKE;

ANIMALS; CELL DEATH; CYTOPROTECTION; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; NADPH OXIDASE; OXIDANTS; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

ANIMALIA;

EID: 79952850719     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3576     Document Type: Review

References (79)

1. Abramov AY, Scorziello A, and Duchen MR. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 27: 1129-1138, 2007. (Pubitemid 46203321)
2. Adibhatla RM, Hatcher JF, and Dempsey RJ. Phospholipase A2, hydroxyl radicals, and lipid peroxidation in transient cerebral ischemia. Antioxid Redox Signal 5: 647-654, 2003. (Pubitemid 37315154)
3. Asahi M, Wang X, Mori T, Sumii T, Jung J-C, Moskowitz MA, FiniME, and Lo EH. Effects of matrix metalloproteinase- 9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21: 7724-7732, 2001. (Pubitemid 32904971)
4. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, White RF, McVey MJ, Legos JJ, Erhardt JA, Nelson AH, Ohlstein EH, Hunter AJ, Ward K, Smith BR, Adams JL, and Parsons AA. SB 239063, a second-generation p38 mitogen-activated protein kinase inhibitor, reduces brain injury and neurological deficits in cerebral focal ischemia. J Pharmacol Exp Ther 296: 312-321, 2001. (Pubitemid 32112455)
5. Beckman JS, Beckman TW, Chen J, Marshall PA, and Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87: 1620-1624, 1990.
6. Bedard K and Krause K-H. The NOX family of ROSgenerating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87: 245-313, 2007. (Pubitemid 46209993)
7. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, Edling Y, Chan PH, and Swanson RA. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 12: 857-863, 2009.
8. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, and Reed JC. Regulation of cell death protease caspase-9 by phosphorylation. Science 282: 1318-1321, 1998. (Pubitemid 28524494)
9. Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 21: 2-14, 2001. (Pubitemid 32036708)
10. Chan PH. Role of oxidants in ischemic brain damage. Stroke 27: 1124-1129, 1996. (Pubitemid 26177617)
11. Chan PH, Kamii H, Yang G, Gafni J, Epstein CJ, Carlson E, and Reola L. Brain infarction is not reduced in SOD-1 transgenic mice after a permanent focal cerebral ischemia. Neuroreport 5: 293-296, 1993. (Pubitemid 24026257)
12. Chan PH, Kawase M, Murakami K, Chen SF, Li Y, Calagui B, Reola L, Carlson E, and Epstein CJ. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci 18: 8292-8299, 1998. (Pubitemid 28465005)
13. Chen H, Song YS, and Chan PH. Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion. J Cereb Blood Flow Metab 29: 1262-1272, 2009.
14. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, and Greenberg ME. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241, 1997. (Pubitemid 27456390)
15. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95, 2002. (Pubitemid 34654215)
16. Endo H, Kamada H, Nito C, Nishi T, and Chan PH. Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats. J Neurosci 26: 7974-7983, 2006. (Pubitemid 44315166)
17. Endo H, Nito C, Kamada H, Nishi T, and Chan PH. Activation of the Akt=GSK3b signaling pathway mediates survival of vulnerable hippocampal neurons after transient global cerebral ischemia in rats. J Cereb Blood Flow Metab 26: 1479-1489, 2006. (Pubitemid 44809077)
18. Epstein CJ, Avraham KB, Lovett M, Smith S, Elroy-Stein O, Rotman G, Bry C, and Groner Y. Transgenic mice with increased Cu=Zn-superoxide dismutase activity: animal model of dosage effects in Down syndrome. Proc Natl Acad Sci USA 84: 8044-8048, 1987.
19. Feigin VL, Lawes CMM, Bennett DA, and Anderson CS. Stroke epidemiology: a review of population-based studies of incidence, prevalence, and case-fatality in the late 20th century. Lancet Neurol 2: 43-53, 2003. (Pubitemid 37443343)
20. Franke TF, Kaplan DR, and Cantley LC. PI3K: downstream AKTion blocks apoptosis. Cell 88: 435-437, 1997. (Pubitemid 27154408)
21. Fujimura M, Morita-Fujimura Y, Kawase M, Copin J-C, Calagui B, Epstein CJ, and Chan PH. Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome c and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19: 3414-3422, 1999. (Pubitemid 29203121)
22. Fujimura M, Morita-Fujimura Y, Noshita N, Sugawara T, Kawase M, and Chan PH. The cytosolic antioxidant copper= zinc-superoxide dismutase prevents the early release of mitochondrial cytochrome c in ischemic brain after transient focal cerebral ischemia in mice. J Neurosci 20: 2817-2824, 2000. (Pubitemid 30220306)
23. Gasche Y, Copin J-C, Sugawara T, Fujimura M, and Chan PH. Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21: 1393-1400, 2001. (Pubitemid 33120943)
24. Green DR and Kroemer G. Cytoplasmic functions of the tumour suppressor p53. Nature 458: 1127-1130, 2009.
25. Gu Z, Cui J, Brown S, Fridman R, Mobashery S, Strongin AY, and Lipton SA. A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 25: 6401-6408, 2005. (Pubitemid 40962536)
26. Gu Z, Kaul M, Yan B, Kridel SJ, Cui J, Strongin A, Smith JW, Liddington RC, and Lipton SA. S-Nitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science 297: 1186-1190, 2002. (Pubitemid 36193354)
27. Hong H, Zeng J-S, Kreulen DL, Kaufman DI, and Chen AF. Atorvastatin protects against cerebral infarction via inhibition of NADPH oxidase-derived superoxide in ischemic stroke. Am J Physiol Heart Circ Physiol 291: H2210-H2215, 2006.
28. Infanger DW, Sharma RV, and Davisson RL. NADPH oxidases of the brain: distribution, regulation, and function. Antioxid Redox Signal 8: 1583-1596, 2006. (Pubitemid 44726333)
29. Irving EA and Bamford M. Role of mitogen- and stress-activated kinases in ischemic injury. J Cereb Blood Flow Metab 22: 631-647, 2002. (Pubitemid 34596455)
30. Jian Liu K and Rosenberg GA. Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med 39: 71-80, 2005. (Pubitemid 40733117)
31. Johnson JL, Park J-W, El Benna J, Faust LP, Inanami O, and Babior BM. Activation of p47PHOX, a cytosolic subunit of the leukocyte NADPH oxidase. Phosphorylation of Ser-359 or Ser-370 precedes phosphorylation at other sites and is required for activity. J Biol Chem 273: 35147-35152, 1998. (Pubitemid 29028218)
32. Jung JE, Kim GS, Narasimhan P, Song YS, and Chan PH. Regulation of Mn-superoxide dismutase activity and neuroprotection by STAT3 in mice after cerebral ischemia. J Neurosci 29: 7003-7014, 2009.
33. Kahles T, Luedike P, Endres M, Galla H-J, Steinmetz H, Busse R, Neumann-Haefelin T, and Brandes RP. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 38: 3000-3006, 2007. (Pubitemid 350035696)
34. Kamada H, Yu F, Nito C, and Chan PH. Influence of hyperglycemia on oxidative stress and matrix metalloproteinase- 9 activation after focal cerebral ischemia=reperfusion in rats. Relation to blood-brain barrier dysfunction. Stroke 38: 1044-1049, 2007. (Pubitemid 46568472)
35. Kapahi P, Takahashi T, Natoli G, Adams SR, Chen Y, Tsien RY, and Karin M. Inhibition of NF-kB activation by arsenite through reaction with a critical cysteine in the activation loop of IkB kinase. J Biol Chem 275: 36062-36066, 2000.
36. Kawase M, Murakami K, Fujimura M, Morita-Fujimura Y, Gasche Y, Kondo T, Scott RW, and Chan PH. Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke 30: 1962-1968, 1999. (Pubitemid 29411842)
37. Keller JN, Kindy MS, Holtsberg FW, St. Clair DK, Yen H-C, Germeyer A, Steiner SM, Bruce-Keller AJ, Hutchins JB, and Mattson MP. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci 18: 687-697, 1998. (Pubitemid 28041905)
38. Kim GS, Jung JE, Niizuma K, and Chan PH. CK2 is a novel negative regulator of NADPH oxidase and a neuroprotectant in mice after cerebral ischemia. J Neurosci 29: 14779-14789, 2009.
39. Kondo T, Reaume AG, Huang T-T, Carlson E, Murakami K, Chen SF, Hoffman EK, Scott RW, Epstein CJ, and Chan PH. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17: 4180-4189, 1997. (Pubitemid 27220609)
40. Lee BI, Chan PH, and Kim GW. Metalloporphyrin-based superoxide dismutase mimic attenuates the nuclear translocation of apoptosis-inducing factor and the subsequent DNA fragmentation after permanent focal cerebral ischemia in mice [Erratum: Stroke 37:576, 2006]. Stroke 36: 2712-2717, 2005.
41. Leker RR, Aharonowiz M, Greig NH, and Ovadia H. The role of p53-induced apoptosis in cerebral ischemia: effects of the p53 inhibitor pifithrin a. Exp Neurol 187: 478-486, 2004. (Pubitemid 38610294)
42. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 79: 1431-1568, 1999. (Pubitemid 29473320)
43. Lo EH, Dalkara T, and Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci 4: 399-415, 2003. (Pubitemid 37280178)
44. Luo Y, Kuo C-C, Shen H, Chou J, Greig NH, Hoffer BJ, and Wang Y. Delayed treatment with a p53 inhibitor enhances recovery in stroke brain. Ann Neurol 65: 520-530, 2009.
45. Maier CM, Hsieh L, Crandall T, Narasimhan P, and Chan PH. Evaluating therapeutic targets for reperfusion-related brain hemorrhage. Ann Neurol 59: 929-938, 2006. (Pubitemid 43830925)
46. Maier CM, Hsieh L, Yu F, Bracci P, and Chan PH. Matrix metalloproteinase-9 and myeloperoxidase expression. Quantitative analysis by antigen immunohistochemistry in a model of transient focal cerebral ischemia. Stroke 35: 1169-1174, 2004. (Pubitemid 38543538)
47. Momand J, Zambetti GP, Olson DC, George D, and Levine AJ. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 69: 1237-1245, 1992.
48. Murakami K, Kondo T, Epstein CJ, and Chan PH. Overexpression of CuZn-superoxide dismutase reduces hippocampal injury after global ischemia in transgenic mice [Erratum: Stroke 28:2573, 1997]. Stroke 28: 1797-1804, 1997. (Pubitemid 27391452)
49. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, and Chan PH. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18: 205-213, 1998. (Pubitemid 28046782)
50. Narasimhan P, Liu J, Song YS, Massengale JL, and Chan PH. VEGF stimulates the ERK 1=2 signaling pathway and apoptosis in cerebral endothelial cells after ischemic conditions. Stroke 40: 1467-1473, 2009.
51. Niizuma K, Endo H, Nito C, Myer DJ, and Chan PH. Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia. Stroke 40: 618-625, 2009.
52. Niizuma K, Endo H, Nito C, Myer DJ, Kim GS, and Chan PH. The PIDDosome mediates delayed death of hippocampal CA1 neurons after transient global cerebral ischemia in rats. Proc Natl Acad Sci USA 105: 16369-16374, 2008.
53. Niizuma K, Yoshioka H, Chen H, Kim GS, Jung JE, Katsu M, Okami N, and Chan PH. Mitochondrial and apoptotic neuronal death signaling pathways in cerebral ischemia. Biochim Biophys Acta 1802: 92-99, 2010.
54. Nishi T, Maier CM, Hayashi T, Saito A, and Chan PH. Superoxide dismutase 1 overexpression reduces MCP-1 and MIP-1a expression after transient focal cerebral ischemia. J Cereb Blood Flow Metab 25: 1312-1324, 2005. (Pubitemid 41348733)
55. Nito C, Kamada H, Endo H, Niizuma K, Myer DJ, and Chan PH. Role of the p38 mitogen-activated protein kinase= cytosolic phospholipase A2 signaling pathway in bloodbrain barrier disruption after focal cerebral ischemia and reperfusion. J Cereb Blood Flow Metab 28: 1686-1696, 2008.
56. Noshita N, Sugawara T, Fujimura M, Morita-Fujimura Y, and Chan PH. Manganese superoxide dismutase affects cytochrome c release and caspase-9 activation after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 21: 557-567, 2001. (Pubitemid 32422876)
57. Noshita N, Sugawara T, Lewén A, Hayashi T, and Chan PH. Copper-zinc superoxide dismutase affects Akt activation after transient focal cerebral ischemia in mice. Stroke 34: 1513-1518, 2003. (Pubitemid 36693527)
58. Nozaki K, Nishimura M, and Hashimoto N. Mitogenactivated protein kinases and cerebral ischemia. Mol Neurobiol 23: 1-19, 2001. (Pubitemid 32948270)
59. Ridder DA and Schwaninger M. NF-kB signaling in cerebral ischemia. Neuroscience 158: 995-1006, 2009.
60. Saito A, Hayashi T, Okuno S, Ferrand-Drake M, and Chan PH. Overexpression of copper=zinc superoxide dismutase in transgenic mice protects against neuronal cell death after transient focal ischemia by blocking activation of the Bad cell death signaling pathway. J Neurosci 23: 1710-1718, 2003. (Pubitemid 36314726)
61. Saito A, Hayashi T, Okuno S, Nishi T, and Chan PH. Modulation of p53 degradation via MDM2-mediated ubiquitylation and the ubiquitin-proteasome system during reperfusion after stroke: role of oxidative stress. J Cereb Blood Flow Metab 25: 267-280, 2005. (Pubitemid 40171208)
62. Saito A, Hayashi T, Okuno S, Nishi T, and Chan PH. Modulation of proline-rich Akt substrate survival signaling pathways by oxidative stress in mouse brains after transient focal cerebral ischemia. Stroke 37: 513-517, 2006. (Pubitemid 43732016)
63. Saito A, Narasimhan P, Hayashi T, Okuno S, Ferrand-Drake M, and Chan PH. Neuroprotective role of a proline-rich Akt substrate in apoptotic neuronal cell death after stroke: relationships with nerve growth factor. J Neurosci 24: 1584-1593, 2004. (Pubitemid 38240953)
64. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, Diener H-C, Ashwood T, Wasiewski WW, Emeribe U, and Investigators SIT. NXY-059 for the treatment of acute ischemic stroke. N Engl J Med 357: 562-571, 2007. (Pubitemid 47236281)
65. Song YS, Lee Y-S, and Chan PH. Oxidative stress transiently decreases the IKK complex (IKKa, b, and g), an upstream component of NF-kB signaling, after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 25: 1301-1311, 2005. (Pubitemid 41348732)
66. Song YS, Lee Y-S, Narasimhan P, and Chan PH. Reduced oxidative stress promotes NF-kB-mediated neuroprotective gene expression after transient focal cerebral ischemia: lymphocytotrophic cytokines and antiapoptotic factors. J Cereb Blood Flow Metab 27: 764-775, 2007. (Pubitemid 46474611)
67. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, and Chan PH. Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci 19:RC39: 1-6, 1999.
68. Sugawara T, Noshita N, Lewén A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y, and Chan PH. Overexpression of copper=zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22: 209-217, 2002. (Pubitemid 34036536)
69. Suh SW, Gum ET, Hamby AM, Chan PH, and Swanson RA. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest 117: 910-918, 2007. (Pubitemid 46556747)
70. Suh SW, Shin BS, Ma H, Van Hoecke M, Brennan AM, Yenari MA, and Swanson RA. Glucose and NADPH oxidase drive neuronal superoxide formation in stroke. Ann Neurol 64: 654-663, 2008.
71. Tang XN, Cairns B, Cairns N, and Yenari MA. Apocynin improves outcome in experimental stroke with a narrow dose range. Neuroscience 154: 556-562, 2008.
72. Walder CE, Green SP, Darbonne WC, Mathias J, Rae J, Dinauer MC, Curnutte JT, and Thomas GR. Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke 28: 2252-2258, 1997. (Pubitemid 27497931)
73. Wang Q, Tompkins KD, Simonyi A, Korthuis RJ, Sun AY, and Sun GY. Apocynin protects against global cerebral ischemia- reperfusion-induced oxidative stress and injury in the gerbil hippocampus. Brain Res 1090: 182-189, 2006. (Pubitemid 43817927)
74. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev 15: 2922-2933, 2001. (Pubitemid 33078942)
75. Yang G, Chan PH, Chen J, Carlson E, Chen SF, Weinstein P, Epstein CJ, and Kamii H. Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25: 165-170, 1994.
76. Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, and Mak TW. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94: 739-750, 1998. (Pubitemid 28436006)
77. Yoshioka H, Niizuma K, Katsu M, Okami N, Sakata H, Kim GS, Narasimhan P, and Chan PH. NADPH oxidase mediates striatal neuronal injury after transient global cerebral ischemia. J Cereb Blood Flow Metab 2010 [Epub ahead of print].
78. Yu J and Zhang L. PUMA, a potent killer with or without p53. Oncogene 27: S71-S83, 2009.
79. Zha J, Harada H, Yang E, Jockel J, and Korsmeyer SJ. Serine phosphorylation of death agonist BAD in response to survival factor results in binding to 14-3-3 not BCL-XL. Cell 87: 619-628, 1996. (Pubitemid 26386936)