Effect of ischemic preconditioning on antioxidant status in the gerbil hippocampal CA1 region after transient forebrain ischemia
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摘要
Ischemic preconditioning(IPC) is a condition of sublethal transient global ischemia and exhibits neuroprotective effects against subsequent lethal ischemic insult.We,in this study,examined the neuroprotective effects of IPC and its effects on immunoreactive changes of antioxidant enzymes including superoxide dismutase(SOD) 1 and SOD2,catalase(CAT) and glutathione peroxidase(GPX) in the gerbil hippocampal CA1 region after transient forebrain ischemia.Pyramidal neurons of the stratum pyramidale(SP) in the hippocampal CA1 region of animals died 5 days after lethal transient ischemia without IPC(8.6%(ratio of remanent neurons) of the sham-operated group);however,IPC prevented the pyramidal neurons from subsequent lethal ischemic injury(92.3%(ratio of remanent neurons) of the sham-operated group).SOD1,SOD2,CAT and GPX immunoreactivities in the sham-operated animals were easily detected in pyramidal neurons in the stratum pyramidale(SP) of the hippocampal CA1 region,while all of these immunoreactivities were rarely detected in the stratum pyramidale at 5 days after lethal transient ischemia without IPC.Meanwhile,their immunoreactivities in the sham-operated animals with IPC were similar to(SOD1,SOD2 and CAT) or higher(GPX) than those in the sham-operated animals without IPC.Furthermore,their immunoreactivities in the stratum pyramidale of the ischemia-operated animals with IPC were steadily maintained after lethal ischemia/reperfusion.Results of western blot analysis for SOD1,SOD2,CAT and GPX were similar to immunohistochemical data.In conclusion,IPC maintained or increased the expression of antioxidant enzymes in the stratum pyramidale of the hippocampal CA1 region after subsequent lethal transient forebrain ischemia and IPC exhibited neuroprotective effects in the hippocampal CA1 region against transient forebrain ischemia.
Ischemic preconditioning(IPC) is a condition of sublethal transient global ischemia and exhibits neuroprotective effects against subsequent lethal ischemic insult.We,in this study,examined the neuroprotective effects of IPC and its effects on immunoreactive changes of antioxidant enzymes including superoxide dismutase(SOD) 1 and SOD2,catalase(CAT) and glutathione peroxidase(GPX) in the gerbil hippocampal CA1 region after transient forebrain ischemia.Pyramidal neurons of the stratum pyramidale(SP) in the hippocampal CA1 region of animals died 5 days after lethal transient ischemia without IPC(8.6%(ratio of remanent neurons) of the sham-operated group);however,IPC prevented the pyramidal neurons from subsequent lethal ischemic injury(92.3%(ratio of remanent neurons) of the sham-operated group).SOD1,SOD2,CAT and GPX immunoreactivities in the sham-operated animals were easily detected in pyramidal neurons in the stratum pyramidale(SP) of the hippocampal CA1 region,while all of these immunoreactivities were rarely detected in the stratum pyramidale at 5 days after lethal transient ischemia without IPC.Meanwhile,their immunoreactivities in the sham-operated animals with IPC were similar to(SOD1,SOD2 and CAT) or higher(GPX) than those in the sham-operated animals without IPC.Furthermore,their immunoreactivities in the stratum pyramidale of the ischemia-operated animals with IPC were steadily maintained after lethal ischemia/reperfusion.Results of western blot analysis for SOD1,SOD2,CAT and GPX were similar to immunohistochemical data.In conclusion,IPC maintained or increased the expression of antioxidant enzymes in the stratum pyramidale of the hippocampal CA1 region after subsequent lethal transient forebrain ischemia and IPC exhibited neuroprotective effects in the hippocampal CA1 region against transient forebrain ischemia.
Ischemic preconditioning(IPC) is a condition of sublethal transient global ischemia and exhibits neuroprotective effects against subsequent lethal ischemic insult.We,in this study,examined the neuroprotective effects of IPC and its effects on immunoreactive changes of antioxidant enzymes including superoxide dismutase(SOD) 1 and SOD2,catalase(CAT) and glutathione peroxidase(GPX) in the gerbil hippocampal CA1 region after transient forebrain ischemia.Pyramidal neurons of the stratum pyramidale(SP) in the hippocampal CA1 region of animals died 5 days after lethal transient ischemia without IPC(8.6%(ratio of remanent neurons) of the sham-operated group);however,IPC prevented the pyramidal neurons from subsequent lethal ischemic injury(92.3%(ratio of remanent neurons) of the sham-operated group).SOD1,SOD2,CAT and GPX immunoreactivities in the sham-operated animals were easily detected in pyramidal neurons in the stratum pyramidale(SP) of the hippocampal CA1 region,while all of these immunoreactivities were rarely detected in the stratum pyramidale at 5 days after lethal transient ischemia without IPC.Meanwhile,their immunoreactivities in the sham-operated animals with IPC were similar to(SOD1,SOD2 and CAT) or higher(GPX) than those in the sham-operated animals without IPC.Furthermore,their immunoreactivities in the stratum pyramidale of the ischemia-operated animals with IPC were steadily maintained after lethal ischemia/reperfusion.Results of western blot analysis for SOD1,SOD2,CAT and GPX were similar to immunohistochemical data.In conclusion,IPC maintained or increased the expression of antioxidant enzymes in the stratum pyramidale of the hippocampal CA1 region after subsequent lethal transient forebrain ischemia and IPC exhibited neuroprotective effects in the hippocampal CA1 region against transient forebrain ischemia.
引文
Ali SF,LeBel CP,Bondy SC(1992)Reactive oxygen species formation as a biomarker of methylmercury and trimethyltin neurotoxicity.Neurotoxicology 13:637-648.
Alkan T,Goren B,Vatansever E,Sarandol E(2008)Effects of hypoxic preconditioning in antioxidant enzyme activities in hypoxic-ischemic brain damage in immature rats.Turk Neurosurg 18:165-171.
Allen CL,Bayraktutan U(2009)Oxidative stress and its role in the pathogenesis of ischaemic stroke.Int J Stroke 4:461-470.
Armogida M,Spalloni A,Amantea D,Nutini M,Petrelli F,Longone P,Bagetta G,Nistico R,Mercuri NB(2011)The protective role of catalase against cerebral ischemia in vitro and in vivo.Int J Immunopathol Pharmacol 24:735-747.
Block F(1999)Global ischemia and behavioural deficits.Prog Neurobiol 58:279-295.
Blomgren K,Hagberg H(2006)Free radicals,mitochondria,and hypoxia-ischemia in the developing brain.Free Radic Biol Med 40:388-397.
Candelario-Jalil E,Alvarez D,Merino N,Leon OS(2003)Delayed treatment with nimesulide reduces measures of oxidative stress following global ischemic brain injury in gerbils.Neurosci Res 47:245-253.
Chan PH(1994)Oxygen radicals in focal cerebral ischemia.Brain Pathol 4:59-65.
Chan PH(2001)Reactive oxygen radicals in signaling and damage in the ischemic brain.J Cereb Blood Flow Metab 21:2-14.
Chan PH,Kawase M,Murakami K,Chen SF,Li Y,Calagui B,Reola L,Carlson E,Epstein CJ(1998)Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion.J Neurosci 18:8292-8299.
Choi YS,Cho KO,Kim EJ,Sung KW,Kim SY(2007)Ischemic preconditioning in the rat hippocampus increases antioxidant activities but does not affect the level of hydroxyl radicals during subsequent severe ischemia.Exp Mol Med 39:556-563.
Christophe M,Nicolas S(2006)Mitochondria:a target for neuroprotective interventions in cerebral ischemia-reperfusion.Curr Pharm Des 12:739-757.
Crack PJ,Taylor JM,de Haan JB,Kola I,Hertzog P,Iannello RC(2003)Glutathione peroxidase-1 contributes to the neuroprotection seen in the superoxide dismutase-1 transgenic mouse in response to ischemia/reperfusion injury.J Cereb Blood Flow Metab 23:19-22.
de Haan JB,Bladier C,Griffiths P,Kelner M,O'Shea RD,Cheung NS,Bronson RT,Silvestro MJ,Wild S,Zheng SS,Beart PM,Hertzog PJ,Kola I(1998)Mice with a homozygous null mutation for the most abundant glutathione peroxidase,Gpx1,show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide.J Biol Chem 273:22528-22536.
Delanty N,Dichter MA(2000)Antioxidant therapy in neurologic disease.Arch Neurol 57:1265-1270.
Durukan A,Tatlisumak T(2010)Preconditioning-induced ischemic tolerance:a window into endogenous gearing for cerebroprotection.Exp Transl Stroke Med 2:2.
Duszczyk M,Ziembowicz A,Gadamski R,Wieronska JM,Smialowska M,Lazarewicz JW(2009)Changes in the NPY immunoreactivity in gerbil hippocampus after hypoxic and ischemic preconditioning.Neuropeptides 43:31-39.
Floyd RA(1999)Antioxidants,oxidative stress,and degenerative neurological disorders.Proc Soc Exp Biol Med 222:236-245.
Fujimura M,Tominaga T,Chan PH(2005)Neuroprotective effect of an antioxidant in ischemic brain injury:involvement of neuronal apoptosis.Neurocrit Care 2:59-66.
Gidday JM(2006)Cerebral preconditioning and ischaemic tolerance.Nat Rev Neurosci 7:437-448.
Jenner P(2003)Oxidative stress in Parkinson's disease.Ann Neurol 53Suppl 3:S26-36;discussion S36-28.
Kehrer JP(2000)The Haber-Weiss reaction and mechanisms of toxicity.Toxicology 149:43-50.
Kim DW,Lee JC,Cho JH,Park JH,Ahn JH,Chen BH,Shin BN,Tae HJ,Seo JY,Kang IJ,Hong S,Kim YM,Won MH,Kim IH(2015)Neuroprotection of ischemic preconditioning is mediated by anti-inflammatory,not pro-inflammatory,cytokines in the gerbil hippocampus induced by a subsequent lethal transient cerebral ischemia.Neurochem Res 40:1984-1995.
Kim GW,Lewen A,Copin J,Watson BD,Chan PH(2001)The cytosolic antioxidant,copper/zinc superoxide dismutase,attenuates blood-brain barrier disruption and oxidative cellular injury after photothrombotic cortical ischemia in mice.Neuroscience 105:1007-1018.
Kim IH,Yan BC,Park JH,Yeun GH,Yim Y,Ahn JH,Lee JC,Hwang IK,Cho JH,Kim YM,Lee YL,Won MH(2013)Neuroprotection of a novel synthetic caffeic acid-syringic acid hybrid compound against experimentally induced transient cerebral ischemic damage.Planta Med 79:313-321.
Kim IH,Yoo KY,Park JH,Yan BC,Ahn JH,Lee JC,Kwon HM,Kim JD,Kim YM,You SG,Kang IJ,Won MH(2014)Comparison of neuroprotective effects of extract and fractions from Agarum clathratum against experimentally induced transient cerebral ischemic damage.PharmBiol 52:335-343.
Kirino T(1982)Delayed neuronal death in the gerbil hippocampus following ischemia.Brain Res 239:57-69.
Kirino T,Sano K(1984)Selective vulnerability in the gerbil hippocampus following transient ischemia.Acta Neuropathol 62:201-208.
Kirino T,Nakagomi T,Kanemitsu H,Tamura A(1996)Ischemic tolerance.Adv Neurol 71:505-511.
Lee JC,Kim IH,Cho GS,Park JH,Ahn JH,Yan BC,Kwon HM,Kim YM,Cheon SH,Cho JH,Lee HY,Won MH,Seo JY(2014)Ischemic preconditioning-induced neuroprotection against transient cerebral ischemic damage via attenuating ubiquitin aggregation.J Neurol Sci336:74-82.
Lee JC,Kim IH,Park JH,Ahn JH,Cho JH,Cho GS,Tae HJ,Chen BH,Yan BC,Yoo KY,Choi JH,Lee CH,Hwang IK,Kwon YG,Kim YM,Won MH(2015)Ischemic preconditioning protects hippocampal pyramidal neurons from transient ischemic injury via the attenuation of oxidative damage through upregulating heme oxygenase-1.Free Radic Biol Med 79:78-90.
Lehotsky J,Burda J,Danielisova V,Gottlieb M,Kaplan P,Saniova B(2009)Ischemic tolerance:the mechanisms of neuroprotective strategy.Anat Rec(Hoboken)292:2002-2012.
Lipton P(1999)Ischemic cell death in brain neurons.Physiol Rev79:1431-1568.
Liu Y,Nakamura T,Toyoshima T,Shinomiya A,Tamiya T,Tokuda M,Keep RF,Itano T(2014a)The effects of D-allose on transient ischemic neuronal death and analysis of its mechanism.Brain Res Bull109:127-131.
Liu YR,Li PW,Suo JJ,Sun Y,Zhang BA,Lu H,Zhu HC,Zhang GB(2014b)Catalpol provides protective effects against cerebral ischaemia/reperfusion injury in gerbils.J Pharm Pharmacol 66:1265-1270.
Makarewicz D,Sulejczak D,Duszczyk M,Malek M,Slomka M,Lazarewicz JW(2014)Delayed preconditioning with NMDA receptor antagonists in a rat model of perinatal asphyxia.Folia Neuropathol52:270-284.
Mohsenzadegan M,Mirshafiey A(2012)The immunopathogenic role of reactive oxygen species in Alzheimer disease.Iran J Allergy Asthma Immunol 11:203-216.
Moraru L,Tong S,Malhotra A,Geocadin R,Thakor N,Bezerianos A(2005)Investigation of the effects of ischemic preconditioning on the HRV response to transient global ischemia using linear and nonlinear methods.Med Eng Phys 27:465-473.
Moro MA,Almeida A,Bolanos JP,Lizasoain I(2005)Mitochondrial respiratory chain and free radical generation in stroke.Free Radic Biol Med 39:1291-1304.
Murakami K,Kondo T,Kawase M,Li Y,Sato S,Chen SF,Chan PH(1998)Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency.J Neurosci18:205-213.
Nakamura H,Katsumata T,Nishiyama Y,Otori T,Katsura K,Katayama Y(2006)Effect of ischemic preconditioning on cerebral blood flow after subsequent lethal ischemia in gerbils.Life Sci 78:1713-1719.
Noshita N,Sugawara T,Fujimura M,Morita-Fujimura Y,Chan PH(2001)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.
Numagami Y,Sato S,Ohnishi ST(1996)Attenuation of rat ischemic brain damage by aged garlic extracts:a possible protecting mechanism as antioxidants.Neurochem Int 29:135-143.
Pires VL,Souza JR,Guimaraes SB,Silva Filho AR,Garcia JH,Vasconcelos PR(2011)Preconditioning with L-alanyl-L-glutamine in a Mongolian gerbil model of acute cerebral ischemia/reperfusion injury.Acta Cir Bras 26 Suppl 1:14-20.
Radi R,Sims S,Cassina A,Turrens JF(1993)Roles of catalase and cytochrome c in hydroperoxide-dependent lipid peroxidation and chemiluminescence in rat heart and kidney mitochondria.Free Radic Biol Med 15:653-659.
Rodrigo R,Fernandez-Gajardo R,Gutierrez R,Matamala JM,Carrasco R,Miranda-Merchak A,Feuerhake W(2013)Oxidative stress and pathophysiology of ischemic stroke:novel therapeutic opportunities.CNS Neurol Disord Drug Targets 12:698-714.
Schmidt-Kastner R,Freund TF(1991)Selective vulnerability of the hippocampus in brain ischemia.Neuroscience 40:599-636.
Sharma SS,Gupta S(2007)Neuroprotective effect of MnTMPyP,a superoxide dismutase/catalase mimetic in global cerebral ischemia is mediated through reduction of oxidative stress and DNA fragmentation.Eur J Pharmacol 561:72-79.
Shen Y,Wang Z,Li F,Sun L(2016)Morphological characteristics of eosinophilic neuronal death after transient unilateral forebrain ischemia in Mongolian gerbils.Neuropathology 36:227-236.
Slemmer JE,Shacka JJ,Sweeney MI,Weber JT(2008)Antioxidants and free radical scavengers for the treatment of stroke,traumatic brain injury and aging.Curr Med Chem 15:404-414.
Stroev SA,Gluschenko TS,Tjulkova EI,Rybnikova EA,Samoilov MO,Pelto-Huikko M(2005)The effect of preconditioning on the Cu,Zn superoxide dismutase expression and enzyme activity in rat brain at the early period after severe hypobaric hypoxia.Neurosci Res 53:39-47.
Sugawara T,Noshita N,Lewen A,Gasche Y,Ferrand-Drake M,Fujimura M,Morita-Fujimura Y,Chan PH(2002)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.
Sugawara T,Fujimura M,Noshita N,Kim GW,Saito A,Hayashi T,Narasimhan P,Maier CM,Chan PH(2004)Neuronal death/survival signaling pathways in cerebral ischemia.NeuroRx 1:17-25.
Valko M,Leibfritz D,Moncol J,Cronin MT,Mazur M,Telser J(2007)Free radicals and antioxidants in normal physiological functions and human disease.Int J Biochem Cell Biol 39:44-84.
Weisbrot-Lefkowitz M,Reuhl K,Perry B,Chan PH,Inouye M,Mirochnitchenko O(1998)Overexpression of human glutathione peroxidase protects transgenic mice against focal cerebral ischemia/reperfusion damage.Brain Res Mol Brain Res 53:333-338.
White BC,Grossman LI,Krause GS(1993)Brain injury by global ischemia and reperfusion:a theoretical perspective on membrane damage and repair.Neurology 43:1656-1665.
White BC,Sullivan JM,DeGracia DJ,O'Neil BJ,Neumar RW,Grossman LI,Rafols JA,Krause GS(2000)Brain ischemia and reperfusion:molecular mechanisms of neuronal injury.J Neurol Sci 179:1-33.
Zhang Y,Marcillat O,Giulivi C,Ernster L,Davies KJ(1990)The oxidative inactivation of mitochondrial electron transport chain components and ATPase.J Biol Chem 265:16330-16336.
Zhang Y,Du Y,Le W,Wang K,Kieffer N,Zhang J(2011)Redox control of the survival of healthy and diseased cells.Antioxid Redox Signal15:2867-2908.
Alkan T,Goren B,Vatansever E,Sarandol E(2008)Effects of hypoxic preconditioning in antioxidant enzyme activities in hypoxic-ischemic brain damage in immature rats.Turk Neurosurg 18:165-171.
Allen CL,Bayraktutan U(2009)Oxidative stress and its role in the pathogenesis of ischaemic stroke.Int J Stroke 4:461-470.
Armogida M,Spalloni A,Amantea D,Nutini M,Petrelli F,Longone P,Bagetta G,Nistico R,Mercuri NB(2011)The protective role of catalase against cerebral ischemia in vitro and in vivo.Int J Immunopathol Pharmacol 24:735-747.
Block F(1999)Global ischemia and behavioural deficits.Prog Neurobiol 58:279-295.
Blomgren K,Hagberg H(2006)Free radicals,mitochondria,and hypoxia-ischemia in the developing brain.Free Radic Biol Med 40:388-397.
Candelario-Jalil E,Alvarez D,Merino N,Leon OS(2003)Delayed treatment with nimesulide reduces measures of oxidative stress following global ischemic brain injury in gerbils.Neurosci Res 47:245-253.
Chan PH(1994)Oxygen radicals in focal cerebral ischemia.Brain Pathol 4:59-65.
Chan PH(2001)Reactive oxygen radicals in signaling and damage in the ischemic brain.J Cereb Blood Flow Metab 21:2-14.
Chan PH,Kawase M,Murakami K,Chen SF,Li Y,Calagui B,Reola L,Carlson E,Epstein CJ(1998)Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion.J Neurosci 18:8292-8299.
Choi YS,Cho KO,Kim EJ,Sung KW,Kim SY(2007)Ischemic preconditioning in the rat hippocampus increases antioxidant activities but does not affect the level of hydroxyl radicals during subsequent severe ischemia.Exp Mol Med 39:556-563.
Christophe M,Nicolas S(2006)Mitochondria:a target for neuroprotective interventions in cerebral ischemia-reperfusion.Curr Pharm Des 12:739-757.
Crack PJ,Taylor JM,de Haan JB,Kola I,Hertzog P,Iannello RC(2003)Glutathione peroxidase-1 contributes to the neuroprotection seen in the superoxide dismutase-1 transgenic mouse in response to ischemia/reperfusion injury.J Cereb Blood Flow Metab 23:19-22.
de Haan JB,Bladier C,Griffiths P,Kelner M,O'Shea RD,Cheung NS,Bronson RT,Silvestro MJ,Wild S,Zheng SS,Beart PM,Hertzog PJ,Kola I(1998)Mice with a homozygous null mutation for the most abundant glutathione peroxidase,Gpx1,show increased susceptibility to the oxidative stress-inducing agents paraquat and hydrogen peroxide.J Biol Chem 273:22528-22536.
Delanty N,Dichter MA(2000)Antioxidant therapy in neurologic disease.Arch Neurol 57:1265-1270.
Durukan A,Tatlisumak T(2010)Preconditioning-induced ischemic tolerance:a window into endogenous gearing for cerebroprotection.Exp Transl Stroke Med 2:2.
Duszczyk M,Ziembowicz A,Gadamski R,Wieronska JM,Smialowska M,Lazarewicz JW(2009)Changes in the NPY immunoreactivity in gerbil hippocampus after hypoxic and ischemic preconditioning.Neuropeptides 43:31-39.
Floyd RA(1999)Antioxidants,oxidative stress,and degenerative neurological disorders.Proc Soc Exp Biol Med 222:236-245.
Fujimura M,Tominaga T,Chan PH(2005)Neuroprotective effect of an antioxidant in ischemic brain injury:involvement of neuronal apoptosis.Neurocrit Care 2:59-66.
Gidday JM(2006)Cerebral preconditioning and ischaemic tolerance.Nat Rev Neurosci 7:437-448.
Jenner P(2003)Oxidative stress in Parkinson's disease.Ann Neurol 53Suppl 3:S26-36;discussion S36-28.
Kehrer JP(2000)The Haber-Weiss reaction and mechanisms of toxicity.Toxicology 149:43-50.
Kim DW,Lee JC,Cho JH,Park JH,Ahn JH,Chen BH,Shin BN,Tae HJ,Seo JY,Kang IJ,Hong S,Kim YM,Won MH,Kim IH(2015)Neuroprotection of ischemic preconditioning is mediated by anti-inflammatory,not pro-inflammatory,cytokines in the gerbil hippocampus induced by a subsequent lethal transient cerebral ischemia.Neurochem Res 40:1984-1995.
Kim GW,Lewen A,Copin J,Watson BD,Chan PH(2001)The cytosolic antioxidant,copper/zinc superoxide dismutase,attenuates blood-brain barrier disruption and oxidative cellular injury after photothrombotic cortical ischemia in mice.Neuroscience 105:1007-1018.
Kim IH,Yan BC,Park JH,Yeun GH,Yim Y,Ahn JH,Lee JC,Hwang IK,Cho JH,Kim YM,Lee YL,Won MH(2013)Neuroprotection of a novel synthetic caffeic acid-syringic acid hybrid compound against experimentally induced transient cerebral ischemic damage.Planta Med 79:313-321.
Kim IH,Yoo KY,Park JH,Yan BC,Ahn JH,Lee JC,Kwon HM,Kim JD,Kim YM,You SG,Kang IJ,Won MH(2014)Comparison of neuroprotective effects of extract and fractions from Agarum clathratum against experimentally induced transient cerebral ischemic damage.PharmBiol 52:335-343.
Kirino T(1982)Delayed neuronal death in the gerbil hippocampus following ischemia.Brain Res 239:57-69.
Kirino T,Sano K(1984)Selective vulnerability in the gerbil hippocampus following transient ischemia.Acta Neuropathol 62:201-208.
Kirino T,Nakagomi T,Kanemitsu H,Tamura A(1996)Ischemic tolerance.Adv Neurol 71:505-511.
Lee JC,Kim IH,Cho GS,Park JH,Ahn JH,Yan BC,Kwon HM,Kim YM,Cheon SH,Cho JH,Lee HY,Won MH,Seo JY(2014)Ischemic preconditioning-induced neuroprotection against transient cerebral ischemic damage via attenuating ubiquitin aggregation.J Neurol Sci336:74-82.
Lee JC,Kim IH,Park JH,Ahn JH,Cho JH,Cho GS,Tae HJ,Chen BH,Yan BC,Yoo KY,Choi JH,Lee CH,Hwang IK,Kwon YG,Kim YM,Won MH(2015)Ischemic preconditioning protects hippocampal pyramidal neurons from transient ischemic injury via the attenuation of oxidative damage through upregulating heme oxygenase-1.Free Radic Biol Med 79:78-90.
Lehotsky J,Burda J,Danielisova V,Gottlieb M,Kaplan P,Saniova B(2009)Ischemic tolerance:the mechanisms of neuroprotective strategy.Anat Rec(Hoboken)292:2002-2012.
Lipton P(1999)Ischemic cell death in brain neurons.Physiol Rev79:1431-1568.
Liu Y,Nakamura T,Toyoshima T,Shinomiya A,Tamiya T,Tokuda M,Keep RF,Itano T(2014a)The effects of D-allose on transient ischemic neuronal death and analysis of its mechanism.Brain Res Bull109:127-131.
Liu YR,Li PW,Suo JJ,Sun Y,Zhang BA,Lu H,Zhu HC,Zhang GB(2014b)Catalpol provides protective effects against cerebral ischaemia/reperfusion injury in gerbils.J Pharm Pharmacol 66:1265-1270.
Makarewicz D,Sulejczak D,Duszczyk M,Malek M,Slomka M,Lazarewicz JW(2014)Delayed preconditioning with NMDA receptor antagonists in a rat model of perinatal asphyxia.Folia Neuropathol52:270-284.
Mohsenzadegan M,Mirshafiey A(2012)The immunopathogenic role of reactive oxygen species in Alzheimer disease.Iran J Allergy Asthma Immunol 11:203-216.
Moraru L,Tong S,Malhotra A,Geocadin R,Thakor N,Bezerianos A(2005)Investigation of the effects of ischemic preconditioning on the HRV response to transient global ischemia using linear and nonlinear methods.Med Eng Phys 27:465-473.
Moro MA,Almeida A,Bolanos JP,Lizasoain I(2005)Mitochondrial respiratory chain and free radical generation in stroke.Free Radic Biol Med 39:1291-1304.
Murakami K,Kondo T,Kawase M,Li Y,Sato S,Chen SF,Chan PH(1998)Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency.J Neurosci18:205-213.
Nakamura H,Katsumata T,Nishiyama Y,Otori T,Katsura K,Katayama Y(2006)Effect of ischemic preconditioning on cerebral blood flow after subsequent lethal ischemia in gerbils.Life Sci 78:1713-1719.
Noshita N,Sugawara T,Fujimura M,Morita-Fujimura Y,Chan PH(2001)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.
Numagami Y,Sato S,Ohnishi ST(1996)Attenuation of rat ischemic brain damage by aged garlic extracts:a possible protecting mechanism as antioxidants.Neurochem Int 29:135-143.
Pires VL,Souza JR,Guimaraes SB,Silva Filho AR,Garcia JH,Vasconcelos PR(2011)Preconditioning with L-alanyl-L-glutamine in a Mongolian gerbil model of acute cerebral ischemia/reperfusion injury.Acta Cir Bras 26 Suppl 1:14-20.
Radi R,Sims S,Cassina A,Turrens JF(1993)Roles of catalase and cytochrome c in hydroperoxide-dependent lipid peroxidation and chemiluminescence in rat heart and kidney mitochondria.Free Radic Biol Med 15:653-659.
Rodrigo R,Fernandez-Gajardo R,Gutierrez R,Matamala JM,Carrasco R,Miranda-Merchak A,Feuerhake W(2013)Oxidative stress and pathophysiology of ischemic stroke:novel therapeutic opportunities.CNS Neurol Disord Drug Targets 12:698-714.
Schmidt-Kastner R,Freund TF(1991)Selective vulnerability of the hippocampus in brain ischemia.Neuroscience 40:599-636.
Sharma SS,Gupta S(2007)Neuroprotective effect of MnTMPyP,a superoxide dismutase/catalase mimetic in global cerebral ischemia is mediated through reduction of oxidative stress and DNA fragmentation.Eur J Pharmacol 561:72-79.
Shen Y,Wang Z,Li F,Sun L(2016)Morphological characteristics of eosinophilic neuronal death after transient unilateral forebrain ischemia in Mongolian gerbils.Neuropathology 36:227-236.
Slemmer JE,Shacka JJ,Sweeney MI,Weber JT(2008)Antioxidants and free radical scavengers for the treatment of stroke,traumatic brain injury and aging.Curr Med Chem 15:404-414.
Stroev SA,Gluschenko TS,Tjulkova EI,Rybnikova EA,Samoilov MO,Pelto-Huikko M(2005)The effect of preconditioning on the Cu,Zn superoxide dismutase expression and enzyme activity in rat brain at the early period after severe hypobaric hypoxia.Neurosci Res 53:39-47.
Sugawara T,Noshita N,Lewen A,Gasche Y,Ferrand-Drake M,Fujimura M,Morita-Fujimura Y,Chan PH(2002)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.
Sugawara T,Fujimura M,Noshita N,Kim GW,Saito A,Hayashi T,Narasimhan P,Maier CM,Chan PH(2004)Neuronal death/survival signaling pathways in cerebral ischemia.NeuroRx 1:17-25.
Valko M,Leibfritz D,Moncol J,Cronin MT,Mazur M,Telser J(2007)Free radicals and antioxidants in normal physiological functions and human disease.Int J Biochem Cell Biol 39:44-84.
Weisbrot-Lefkowitz M,Reuhl K,Perry B,Chan PH,Inouye M,Mirochnitchenko O(1998)Overexpression of human glutathione peroxidase protects transgenic mice against focal cerebral ischemia/reperfusion damage.Brain Res Mol Brain Res 53:333-338.
White BC,Grossman LI,Krause GS(1993)Brain injury by global ischemia and reperfusion:a theoretical perspective on membrane damage and repair.Neurology 43:1656-1665.
White BC,Sullivan JM,DeGracia DJ,O'Neil BJ,Neumar RW,Grossman LI,Rafols JA,Krause GS(2000)Brain ischemia and reperfusion:molecular mechanisms of neuronal injury.J Neurol Sci 179:1-33.
Zhang Y,Marcillat O,Giulivi C,Ernster L,Davies KJ(1990)The oxidative inactivation of mitochondrial electron transport chain components and ATPase.J Biol Chem 265:16330-16336.
Zhang Y,Du Y,Le W,Wang K,Kieffer N,Zhang J(2011)Redox control of the survival of healthy and diseased cells.Antioxid Redox Signal15:2867-2908.