Oxidative Stress in Brain Ischemia

Brain Pathology - Tập 9 Số 1 - Trang 119-131 - 1999
Seth Love1
1Department of Neuropathology, Frenchay Hospital, Bristol BS16 1LE, UK

Tóm tắt

Brain ischemia initiates a complex cascade of metabolic events, several of which involve the generation of nitrogen and oxygen free radicals. These free radicals and related reactive chemical species mediate much of damage that occurs after transient brain ischemia, and in the penumbral region of infarcts caused by permanent ischemia. Nitric oxide, a water‐ and lipid‐soluble free radical, is generated by the action of nitric oxide synthases. Ischemia causes a surge in nitric oxide synthase 1 (NOS 1) activity in neurons and, possibly, glia, increased NOS 3 activity in vascular endothelium, and later an increase in NOS 2 activity in a range of cells including infiltrating neutrophils and macrophages, activated microglia and astrocytes. The effects of ischemia on the activity of NOS 1, a Ca2+‐dependent enzyme, are thought to be secondary to reversal of glutamate reuptake at synapses, activation of NMDA receptors, and resulting elevation of intracellular Ca2+. The up‐regulation of NOS 2 activity is mediated by transcriptional inducers. In the context of brain ischemia, the activity of NOS 1 and NOS 2 is broadly deleterious, and their inhibition or inactivation is neuroprotective. However, the production of nitric oxide in blood vessels by NOS 3, which, like NOS 1, is Ca2+‐dependent, causes vasodilatation and improves blood flow in the penumbral region of brain infarcts. In addition to causing the synthesis of nitric oxide, brain ischemia leads to the generation of superoxide, through the action of nitric oxide synthases, xanthine oxidase, leakage from the mito‐chondrial electron transport chain, and other mechanisms. Nitric oxide and superoxide are themselves highly reactive but can also combine to form a highly toxic an ion, peroxynitrite. The toxicity of the free radicals and peroxynitrite results from their modification of macromolecules, especially DNA, and from the resulting induction of apoptotic and necrotic pathways. The mode of cell death that prevails probably depends on the severity and precise nature of the ischemie injury. Recent studies have emphasized the role of peroxynitrite in causing singlestand breaks in DNA, which activate the DNA repair protein poly(ADP‐ribose) polymerase (PARP). This catalyzes the cleavage and thereby the consumption of NAD+, the source of energy for many vital cellular processes. Over‐activation of PARP, with resulting depletion of NAD+, has been shown to make a major contribution to brain damage after transient focal ischemia in experimental animals. Neuronal accumulation of poly(ADP‐ribose), the end‐product of PARP activity has been demonstrated after brain ischemia in man. Several therapeutic strategies have been used to try to prevent oxidative damage and its consequences after brain ischemia in man. Although some of the drugs used in early studies were ineffective or had unacceptable side effects, other trials with antioxidant drugs have proven highly encouraging. The findings in recent animal studies are likely to lead to a range of further pharmacological strategies to limit brain injury in stroke patients.

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Tài liệu tham khảo

10.1113/jphysiol.1994.sp020302

10.1074/jbc.271.25.15069

10.1161/01.CIR.92.10.2855

10.1038/335433a0

10.1097/00004647-199801000-00009

10.1152/ajpcell.1996.271.5.C1424

10.1016/S0006-8993(97)01407-8

10.1006/geno.1995.1086

10.1073/pnas.92.16.7162

10.1023/A:1006800322719

10.1097/00004647-199801000-00008

10.1046/j.1471-4159.1997.69010232.x

10.1523/JNEUROSCI.18-13-04914.1998

Chopp M, 1996, Apoptosis in focal cerebral ischemia, Ada Neurochir, 66, 21

10.1006/excr.1995.1397

10.1007/978-1-4757-9480-9_21

Dalkara T, 1994, The complex role of nitric oxide in the pathophysiology of focal cerebral ischemia, Brain Pathol, 1994, 49, 10.1111/j.1750-3639.1994.tb00810.x

10.1016/S0074-7742(08)60726-6

10.1177/107385849500100103

10.1523/JNEUROSCI.14-09-05147.1994

10.1073/pnas.94.14.7303

10.1016/S0027-5107(97)00009-2

10.1016/0167-4838(91)99007-F

10.1073/pnas.91.10.4214

10.1016/S0306-4522(96)00297-7

10.1097/00004647-199603000-00003

10.1523/JNEUROSCI.15-10-06377.1995

10.1139/o97-043

10.1074/jbc.271.32.19199

10.1038/34923

10.1016/0014-5793(94)01280-6

10.1073/pnas.94.7.3396

10.1038/nm1097-1089

10.1515/JPEM.1996.9.5.501

10.1042/bj2620575

Endres M, 1997, Ischemie brain injury is mediated by the activation of poly(ADP‐ribose)polymerase, J Cereb Blood Flow Metab, 17, 1143, 10.1097/00004647-199711000-00002

10.1097/00004647-199803000-00002

10.1093/nar/24.9.1625

10.1093/nar/24.21.4105

10.1016/0378-4274(93)90046-Z

10.1097/00004647-199803000-00006

10.1016/S0021-9258(18)47344-9

10.1016/S0190-9622(97)70260-3

Gale EA, 1996, Molecular mechanisms of β‐cell destruction in IDDM: the role of nicotinamide, Hormone Res, 1, 39

10.1146/annurev.ph.57.030195.003343

10.1146/annurev.ph.57.030195.003513

10.3171/jns.1997.86.3.0467

10.1097/00004647-199607000-00010

10.1073/pnas.94.5.2007

10.1042/bj2460325

Hibbs JB, 1987, L‐arginine is required for expression of the activated macrophage effector mechanism causing selective inhibition in target cells, J Immunol, 138, 550, 10.4049/jimmunol.138.2.550

10.1016/0005-2728(94)90220-8

10.1016/S0190-9622(97)70336-0

10.1111/j.1750-3639.1994.tb00808.x

10.1007/BF00217517

10.1038/377239a0

10.1097/00004647-199609000-00023

10.1126/science.7522345

10.1016/S0166-2236(96)10074-6

Ladecola C, 1997, Delayed reduction of ischemie brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene, J Neurosci, 17, 9157, 10.1523/JNEUROSCI.17-23-09157.1997

Ladecola C, 1995, Inhibition of inducible nitric oxide synthase ameliorates cerebral ischemie damage, Am J Physiol, 268, R286

10.1016/0014-5793(95)00873-8

10.1016/0304-3940(96)12669-0

10.1016/S0960-9822(98)70032-6

10.1007/BF02252945

10.3171/jns.1996.84.2.0221

10.1016/0304-3940(96)12446-0

10.1042/bj2980249

10.1002/(SICI)1098-1136(199602)16:2<165::AID-GLIA8>3.0.CO;2-2

10.1016/0098-2997(94)90023-X

10.1006/bbrc.1996.0263

Lam TT, 1997, The effect of 3‐aminobenzamide, an inhibitor of poly‐ADP‐ribose polymerase, on ischemia/reperfusion damage in rat retina. Res, Comm Molec Pathol Pharmacol, 95, 241

10.1007/BF01076101

10.1139/o90-085

10.1038/371346a0

10.1212/WNL.49.5_Suppl_4.S66

10.1006/bbrc.1997.6491

Leist M, 1997, Caspase‐mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide, Molec Wed, 3, 750

10.1038/jcbfm.1995.49

10.1161/01.STR.26.7.1252

Liu PK, 1996, Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia‐reperfusion, J Neurosci, 16, 6795, 10.1523/JNEUROSCI.16-21-06795.1996

10.1016/0165-1110(95)90004-7

10.1161/01.STR.29.4.830

10.1161/01.STR.27.8.1381

Love S, 1998, DNA fragmentation and repair in ischaemic brain injury in man, Neuropathol Appl Neurobiol, 24, 134

LoveS BarberR WilcockGK(1998)Apoptosis and expression of DNA repair proteins in ischaemic brain injury in man.NeuroReportQ:955–959.

LoveS BarberR WilcockGK(In press) Neuronal accumulation of poly(ADP‐ribose) after brain ischaemia.Neuropathol Appl Neurobiol.

10.1016/0014-5793(92)80697-F

10.1002/(SICI)1097-4547(19970515)48:4<372::AID-JNR9>3.0.CO;2-8

Moncada S, 1991, Nitric oxide: physiology, pathophysiology and pharmacology, Pharmacol Rev, 43, 109

10.1111/j.1750-3639.1994.tb00809.x

10.1161/01.STR.26.3.503

10.1073/pnas.85.22.8737

10.1097/00001756-199507310-00019

10.1007/BF01209751

10.1126/science.1329206

10.1523/JNEUROSCI.18-10-03659.1998

10.1016/S0021-9258(17)36703-0

10.1073/pnas.89.7.3030

10.1097/00004647-199803000-00003

10.1038/376037a0

Nicotera P, 1997, Neuronal necrosis and apoptosis: two distinct events induced by exposure to glutamate or oxidative stress, Adv Neurol, 72, 95

10.1007/978-1-4899-2638-8_74

10.1006/excr.1994.1156

Obrenovitch TP, 1995, Extracellular neurotransmitter changes in cerebral ischaemia, Cerebrovasc Brain Metab Rev, 7, 1

10.1021/bi9727390

10.1038/327524a0

10.1161/01.STR.27.2.327

10.1111/j.1365-2230.1995.tb01317.x

10.1203/00006450-199309000-00025

10.2337/diacare.19.12.1357

10.1530/eje.0.1370234

10.1007/s001250050362

10.1006/abbi.1994.1013

10.1073/pnas.87.13.5193

10.1006/geno.1994.1068

10.1006/excr.1997.3536

10.1080/095530098142428

10.1097/00006123-199802000-00038

10.1006/abbi.1995.1493

10.1006/bbrc.1995.1759

10.1161/01.STR.28.6.1283

10.1038/356356a0

10.1016/0092-8674(94)90267-4

10.1016/0165-6147(93)90107-U

10.1016/0300-9084(96)88140-5

10.1085/jgp.95.5.837

10.1038/jcbfm.1992.107

10.1021/bi953010z

10.1016/1357-2725(95)00026-L

10.1016/0014-5793(95)01117-W

SpencerJP WongJ JennerA AruomaOI CrossCE HalliwellB(1996)Base modification and strand breakage in isolated calf thymus DNA and in DNA from human skin epidermal keratinocytes exposed to peroxynitrite or 3‐morpholinosydnonimine.Chem Res ToxicolQ:1152–1158.

10.1006/niox.1997.0143

Szabó C, 1996, DNA strand breakage, activation of poly (ADP‐ribose) synthetase, and cellular energy depletion are involved in the cytotoxicity of macrophages and smooth muscle cells exposed to peroxynitrite, Proc Natl Acad Sci USA, 93, 1753, 10.1073/pnas.93.5.1753

10.1016/0166-2236(94)90040-X

10.1242/jeb.200.2.401

10.1097/00004647-199711000-00001

Tanaka Y, 1995, Inhibition and down‐regulation of poly(ADP‐ribose) polymerase results in a marked resistance of HL‐60 cells to various apoptosis‐inducers, Cell Molec, 41, 771

10.1074/jbc.272.12.7617

10.1161/01.STR.28.11.2252

10.1101/gad.9.5.509

10.1101/gad.11.18.2347

10.2307/3579534

10.1126/science.1948068

WisdenW SeeburgP.(1993).Mammalian ionotropic glutamate receptors.Current Opinion NeurobiolZ:291–298.

10.1159/000133562

10.1161/01.STR.29.1.12

10.1074/jbc.271.15.9129

10.1038/jcbfm.1994.123

10.1002/mrm.1910370204

10.1161/01.STR.27.2.317

10.1016/0006-8993(94)91574-1

10.1161/01.STR.24.12.2016