Pretreated Oenan the Javanica extract increases anti-inflammatory cytokines, attenuates gliosis, and protects hippocampal neurons following transient global cerebral ischemia in gerbils
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摘要
Recently, we have reported that Oenanthe javanica extract(OJE) displays strong neuroprotective effect against ischemic damage after transient global cerebral ischemia. However, neuroprotective mechanisms of OJE have not been fully identified. Thus, this study investigated the neuroprotection of OJE in the hippocampal CA1 area and its anti-inflammatory activity in gerbils subjected to 5 minutes of transient global cerebral ischemia. We treated the animals by intragastrical injection of OJE(100 and 200 mg/kg)once daily for 1 week prior to transient global cerebral ischemia. Neuroprotection of OJE was observed by immunohistochemistry for neuronal nuclear antigen and histofluorescence staining for Fluoro-Jade B. Im-munohistochemistry of glial fibrillary acidic protein and ionized calcium-binding adapter molecule 1 was done for astrocytosis and microgliosis, respectively. To investigate the neuroprotective mechanisms of OJE,we performed immunohistochemistry of tumor necrosis factor-alpha and interleukin-2 for pro-inflamma-tory function and interleukin-4 and interleukin-13 for anti-inflammatory function. When we treated the animals by intragastrical administration of 200 mg/kg of OJE, hippocampal CA1 pyramidal neurons were protected from transient global cerebral ischemia and cerebral ischemia-induced gliosis was inhibited in the ischemic hippocampal CA1 area. We also found that interleukin-4 and -13 immunoreactivities were significantly increased in pyramidal neurons of the ischemic CA1 area after OJE pretreatment, and the increased immunoreactivities were sustained in the CA1 pyramidal neurons after transient global cere-bral ischemia. However, OJE pretreatment did not increase interleukin-2 and tumor necrosis factor-alpha immunoreactivities in the CA1 pyramidal neurons. Our findings suggest that pretreatment with OJE can protect neurons and attenuate gliosis from transient global cerebral ischemia via increasing expressions of interleukin-4 and -13. The experimental plan of this study was reviewed and approved by the Institutional Animal Care and Use Committee(IACUC) in Kangwon National University(approval No. KW-160802-1)on August 10, 2016.
Recently, we have reported that Oenanthe javanica extract(OJE) displays strong neuroprotective effect against ischemic damage after transient global cerebral ischemia. However, neuroprotective mechanisms of OJE have not been fully identified. Thus, this study investigated the neuroprotection of OJE in the hippocampal CA1 area and its anti-inflammatory activity in gerbils subjected to 5 minutes of transient global cerebral ischemia. We treated the animals by intragastrical injection of OJE(100 and 200 mg/kg)once daily for 1 week prior to transient global cerebral ischemia. Neuroprotection of OJE was observed by immunohistochemistry for neuronal nuclear antigen and histofluorescence staining for Fluoro-Jade B. Im-munohistochemistry of glial fibrillary acidic protein and ionized calcium-binding adapter molecule 1 was done for astrocytosis and microgliosis, respectively. To investigate the neuroprotective mechanisms of OJE,we performed immunohistochemistry of tumor necrosis factor-alpha and interleukin-2 for pro-inflamma-tory function and interleukin-4 and interleukin-13 for anti-inflammatory function. When we treated the animals by intragastrical administration of 200 mg/kg of OJE, hippocampal CA1 pyramidal neurons were protected from transient global cerebral ischemia and cerebral ischemia-induced gliosis was inhibited in the ischemic hippocampal CA1 area. We also found that interleukin-4 and -13 immunoreactivities were significantly increased in pyramidal neurons of the ischemic CA1 area after OJE pretreatment, and the increased immunoreactivities were sustained in the CA1 pyramidal neurons after transient global cere-bral ischemia. However, OJE pretreatment did not increase interleukin-2 and tumor necrosis factor-alpha immunoreactivities in the CA1 pyramidal neurons. Our findings suggest that pretreatment with OJE can protect neurons and attenuate gliosis from transient global cerebral ischemia via increasing expressions of interleukin-4 and -13. The experimental plan of this study was reviewed and approved by the Institutional Animal Care and Use Committee(IACUC) in Kangwon National University(approval No. KW-160802-1)on August 10, 2016.
Recently, we have reported that Oenanthe javanica extract(OJE) displays strong neuroprotective effect against ischemic damage after transient global cerebral ischemia. However, neuroprotective mechanisms of OJE have not been fully identified. Thus, this study investigated the neuroprotection of OJE in the hippocampal CA1 area and its anti-inflammatory activity in gerbils subjected to 5 minutes of transient global cerebral ischemia. We treated the animals by intragastrical injection of OJE(100 and 200 mg/kg)once daily for 1 week prior to transient global cerebral ischemia. Neuroprotection of OJE was observed by immunohistochemistry for neuronal nuclear antigen and histofluorescence staining for Fluoro-Jade B. Im-munohistochemistry of glial fibrillary acidic protein and ionized calcium-binding adapter molecule 1 was done for astrocytosis and microgliosis, respectively. To investigate the neuroprotective mechanisms of OJE,we performed immunohistochemistry of tumor necrosis factor-alpha and interleukin-2 for pro-inflamma-tory function and interleukin-4 and interleukin-13 for anti-inflammatory function. When we treated the animals by intragastrical administration of 200 mg/kg of OJE, hippocampal CA1 pyramidal neurons were protected from transient global cerebral ischemia and cerebral ischemia-induced gliosis was inhibited in the ischemic hippocampal CA1 area. We also found that interleukin-4 and -13 immunoreactivities were significantly increased in pyramidal neurons of the ischemic CA1 area after OJE pretreatment, and the increased immunoreactivities were sustained in the CA1 pyramidal neurons after transient global cere-bral ischemia. However, OJE pretreatment did not increase interleukin-2 and tumor necrosis factor-alpha immunoreactivities in the CA1 pyramidal neurons. Our findings suggest that pretreatment with OJE can protect neurons and attenuate gliosis from transient global cerebral ischemia via increasing expressions of interleukin-4 and -13. The experimental plan of this study was reviewed and approved by the Institutional Animal Care and Use Committee(IACUC) in Kangwon National University(approval No. KW-160802-1)on August 10, 2016.
引文
Ai G,Huang ZM,Liu QC,Han YQ,Chen X(2016)The protective effect of total phenolics from Oenanthe Javanica on acute liver failure in-duced by D-galactosamine.J Ethnopharmacol 186:53-60.
Amantea D,Certo M,Russo R,Bagetta G,Corasaniti MT,Tassorelli C(2014)Early reperfusion injury is associated to MMP2 and IL-1beta elevation in cortical neurons of rats subjected to middle cerebral ar-tery occlusion.Neuroscience 277:755-763.
Ashabi G,Khalaj L,Khodagholi F,Goudarzvand M,Sarkaki A(2015)Pre-treatment with metformin activates Nrf2 antioxidant pathways and inhibits inflammatory responses through induction of AMPKafter transient global cerebral ischemia.Metab Brain Dis 30:747-754.
Barone FC,Arvin B,White RF,Miller A,Webb CL,Willette RN,Lysko PG,Feuerstein GZ(1997)Tumor necrosis factor-alpha.A mediator of focal ischemic brain injury.Stroke 28:1233-1244.
Becher B,Spath S,Goverman J(2017)Cytokine networks in neuroin-flammation.Nat Rev Immunol 17:49-59.
Cavaglia M,Dombrowski SM,Drazba J,Vasanji A,Bokesch PM,Jani-gro D(2001)Regional variation in brain capillary density and vascu-lar response to ischemia.Brain Res 910:81-93.
Ceulemans AG,Zgavc T,Kooijman R,Hachimi-Idrissi S,Sarre S,Michotte Y(2010)The dual role of the neuroinflammatory response after ischemic stroke:modulatory effects of hypothermia.J Neuroin-flammation 7:74.
Chen X,Zhang X,Wang Y,Lei H,Su H,Zeng J,Pei Z,Huang R(2015)Inhibition of immunoproteasome reduces infarction volume and attenuates inflammatory reaction in a rat model of ischemic stroke.Cell Death Dis 6:e1626.
Dekanski D,Selakovic V,Piperski V,Radulovic Z,Korenic A,Rade-novic L(2011)Protective effect of olive leaf extract on hippocampal injury induced by transient global cerebral ischemia and reperfusion in Mongolian gerbils.Phytomedicine 18:1137-1143.
Globus MY,Busto R,Martinez E,Valdes I,Dietrich WD,Ginsberg MD(1991)Comparative effect of transient global ischemia on extracel-lular levels of glutamate,glycine,and gamma-aminobutyric acid in vulnerable and nonvulnerable brain regions in the rat.J Neurochem57:470-478.
Huttner HB,Bergmann O,Salehpour M,Rácz A,Tatarishvili J,Lind-gren E,Csonka T,Csiba L,Hortobágyi T,Méhes G,Englund E,Solnestam BW,Zdunek S,Scharenberg C,Str?m L,St?hl P,Sigur-geirsson B,Dahl A,Schwab S,Possnert G,et al.(2014)The age and genomic integrity of neurons after cortical stroke in humans.Nat Neurosci 17:801-803.
Hwang IK,Yoo KY,Kim DW,Lee HJ,Kang HY,Lee HY,Kang TC,Choi SY,Kim YS,Won MH(2006)Transient ischemia-induced changes of interleukin-2 and its receptor beta immunoreactivity and levels in the gerbil hippocampal CA1 region.Brain Res 1106:197-204.
Ji G,Yao X,Zang Z,Huang Z(1990)Antiarrhythmic effect of Oenanthe javanica(Bl.)DC.injection.Zhongguo Zhong Yao Za Zhi 15:429-431,448.
Jiang Q,Wang F,Tan HW,Li MY,Xu ZS,Tan GF,Xiong AS(2015)De novo transcriptome assembly,gene annotation,marker development,and miRNA potential target genes validation under abiotic stresses in Oenanthe javanica.Mol Genet Genomics 290:671-683.
Kaundal RK,Iyer S,Kumar A,Sharma SS(2009)Protective effects of pioglitazone against global cerebral ischemic-reperfusion injury in gerbils.J Pharmacol Sci 109:361-367.
Kim JY,Park J,Chang JY,Kim SH,Lee JE(2016)Inflammation after ischemic stroke:the role of leukocytes and glial cells.Exp Neurobiol25:241-251.
Kirino T(1982)Delayed neuronal death in the gerbil hippocampus fol-lowing ischemia.Brain Res 239:57-69.
Kuang X,Wang LF,Yu L,Li YJ,Wang YN,He Q,Chen C,Du JR(2014)Ligustilide ameliorates neuroinflammation and brain injury in fo-cal cerebral ischemia/reperfusion rats:involvement of inhibition of TLR4/peroxiredoxin 6 signaling.Free Radic Biol Med 71:165-175.
Ledeboer A,Breve JJ,Poole S,Tilders FJ,Van Dam AM(2000)Interleu-kin-10,interleukin-4,and transforming growth factor-beta differen-tially regulate lipopolysaccharide-induced production of pro-inflam-matory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells.Glia 30:134-142.
Lee JC,Park JH,Kim IH,Cho GS,Ahn JH,Tae HJ,Choi SY,Cho JH,Kim DW,Kwon YG,Kang IJ,Won MH,Kim YM(2017)Neuropro-tection of ischemic preconditioning is mediated by thioredoxin 2 in the hippocampal CA1 region following a subsequent transient cere-bral ischemia.Brain Pathol 27:276-291.
Liu RL,Xiong QJ,Shu Q,Wu WN,Cheng J,Fu H,Wang F,Chen JG,Hu ZL(2012)Hyperoside protects cortical neurons from oxy-gen-glucose deprivation-reperfusion induced injury via nitric oxide signal pathway.Brain Res 1469:164-173.
Ma CJ,Lee KY,Jeong EJ,Kim SH,Park J,Choi YH,Kim YC,Sung SH(2010)Persicarin from water dropwort(Oenanthe javanica)protects primary cultured rat cortical cells from glutamate-induced neurotox-icity.Phytother Res 24:913-918.
Murakami Y,Saito K,Hara A,Zhu Y,Sudo K,Niwa M,Fujii H,Wada H,Ishiguro H,Mori H,Seishima M(2005)Increases in tumor necro-sis factor-alpha following transient global cerebral ischemia do not contribute to neuron death in mouse hippocampus.J Neurochem93:1616-1622.
Niizuma K,Endo H,Nito C,Myer DJ,Chan PH(2009)Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia.Stroke 40:618-625.
Park JH,Long A,Owens K,Kristian T(2016)Nicotinamide mononu-cleotide inhibits post-ischemic NAD(+)degradation and dramati-cally ameliorates brain damage following global cerebral ischemia.Neurobiol Dis 95:102-110.
Park JH,Kim YH,Ahn JH,Choi SY,Hong S,Kim SK,Kang IJ,Kim YM,Lee TK,Won MH,Lee CH(2017a)Atomoxetine protects against NMDA receptor-mediated hippocampal neuronal death following transient global cerebral ischemia.Curr Neurovasc Res14:158-168.
Park JH,Cho JH,Kim IH,Ahn JH,Lee JC,Chen BH,Shin BN,Tae HJ,Yoo KY,Hong S,Kang IJ,Won MH,Kim JD(2015)Oenanthe Javani-ca extract protects against experimentally induced ischemic neuronal damage via its antioxidant effects.Chin Med J(Engl)128:2932-2937.
Park JH,Lee TK,Yan BC,Shin BN,Ahn JH,Kim IH,Cho JH,Lee JC,Hwang IK,Kim JD,Hong S,Lee YJ,Won MH,Kang IJ(2017b)Pre-treated Glehnia littoralis extract prevents neuronal death following transient global cerebral ischemia through increases of superoxide dismutase 1 and brain-derived neurotrophic factor expressions in the gerbil hippocampal cornu ammonis 1 area.Chin Med J(Engl)130:1796-1803.
Park JH,Park O,Cho JH,Chen BH,Kim IH,Ahn JH,Lee JC,Yan BC,Yoo KY,Lee CH,Hwang IK,Kwon SH,Lee YL,Won MH,Choi JH(2014)Anti-inflammatory effect of tanshinone I in neuroprotection against cerebral ischemia-reperfusion injury in the gerbil hippocam-pus.Neurochem Res 39:1300-1312.
Park JH,Park CW,Ahn JH,Choi SY,Shin MC,Cho JH,Lee TK,Kim IH,Cho JH,Lee JC,Kim YH,Kim YM,Kim JD,Tae HJ,Shin BN,Bae EJ,Chen BH,Won MH,Kang IJ(2017c)Neuroprotection and reduced gliosis by pre-and post-treatments of hydroquinone in a gerbil model of transient cerebral ischemia.Chem Biol Interact278:230-238.
Raghavan A,Shah ZA(2015)Withania somnifera improves ischemic stroke outcomes by attenuating PARP1-AIF-mediated caspase-inde-pendent apoptosis.Mol Neurobiol 52:1093-1105.
Sasaki T,Li W,Ohmoto T,Koike K(2016)Evaluation of canthinone al-kaloids as cerebral protective agents.Bioorg Med Chem Lett 26:4992-4995.
Somera-Molina KC,Nair S,Van Eldik LJ,Watterson DM,Wainwright MS(2009)Enhanced microglial activation and proinflammatory cytokine upregulation are linked to increased susceptibility to sei-zures and neurologic injury in a‘two-hit’seizure model.Brain Res1282:162-172.
Uno H,Matsuyama T,Akita H,Nishimura H,Sugita M(1997)In-duction of tumor necrosis factor-alpha in the mouse hippocampus following transient forebrain ischemia.J Cereb Blood Flow Metab17:491-499.
Vila N,Castillo J,Davalos A,Chamorro A(2000)Proinflammatory cy-tokines and early neurological worsening in ischemic stroke.Stroke31:2325-2329.
Wang J,Tsirka SE(2005)Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage.Brain 128:1622-1633.
Xiong X,Barreto GE,Xu L,Ouyang YB,Xie X,Giffard RG(2011)In-creased brain injury and worsened neurological outcome in interleu-kin-4 knockout mice after transient focal cerebral ischemia.Stroke42:2026-2032.
Yang MS,Park EJ,Sohn S,Kwon HJ,Shin WH,Pyo HK,Jin B,Choi KS,Jou I,Joe EH(2002)Interleukin-13 and-4 induce death of activated microglia.Glia 38:273-280.
Yang SA,Jung YS,Lee SJ,Park SC,Kim MJ,Lee EJ,Byun HJ,Jhee KH,Lee SP(2014)Hepatoprotective effects of fermented field wa-ter-dropwort(Oenanthe javanica)extract and its major constituents.Food Chem Toxicol 67:154-160.
Yang XB,Huang ZM,Cao WB,Zheng M,Chen HY,Zhang JZ(2000)Antidiabetic effect of Oenanthe javanica flavone.Acta Pharmacol Sin21:239-242.
Yin L,Ohtaki H,Nakamachi T,Dohi K,Iwai Y,Funahashi H,Makino R,Shioda S(2003)Expression of tumor necrosis factor alpha(TN-Falpha)following transient cerebral ischemia.Acta Neurochir Suppl86:93-96.
Yoo KY,Kim IH,Cho JH,Ahn JH,Park JH,Lee JC,Tae HJ,Kim DW,Kim JD,Hong S,Won MH,Kang IJ(2016)Neuroprotection of Chry-santhemum indicum Linne against cerebral ischemia/reperfusion in-jury by anti-inflammatory effect in gerbils.Neural Regen Res 11:270-277.
Zhang H,Park JH,Maharjan S,Park JA,Choi KS,Park H,Jeong Y,Ahn JH,Kim IH,Lee JC,Cho JH,Lee IK,Lee CH,Hwang IK,Kim YM,Suh YG,Won MH,Kwon YG(2017)Sac-1004,a vascular leakage blocker,reduces cerebral ischemia-reperfusion injury by suppressing blood-brain barrier disruption and inflammation.J Neuroinflamma-tion 14:122.
Zhao JJ,Song JQ,Pan SY,Wang K(2016)Treatment with isorhamnetin protects the brain against ischemic injury in mice.Neurochem Res41:1939-1948.
Zhu Y,Gao Y,Zheng D,Shui M,Yu K,Liu X,Lin Y,Su L,Yang W,Wang Y(2017)Design and evaluation of EphrinA1 mutants with cerebral protective effect.Sci Rep 7:1881.
Amantea D,Certo M,Russo R,Bagetta G,Corasaniti MT,Tassorelli C(2014)Early reperfusion injury is associated to MMP2 and IL-1beta elevation in cortical neurons of rats subjected to middle cerebral ar-tery occlusion.Neuroscience 277:755-763.
Ashabi G,Khalaj L,Khodagholi F,Goudarzvand M,Sarkaki A(2015)Pre-treatment with metformin activates Nrf2 antioxidant pathways and inhibits inflammatory responses through induction of AMPKafter transient global cerebral ischemia.Metab Brain Dis 30:747-754.
Barone FC,Arvin B,White RF,Miller A,Webb CL,Willette RN,Lysko PG,Feuerstein GZ(1997)Tumor necrosis factor-alpha.A mediator of focal ischemic brain injury.Stroke 28:1233-1244.
Becher B,Spath S,Goverman J(2017)Cytokine networks in neuroin-flammation.Nat Rev Immunol 17:49-59.
Cavaglia M,Dombrowski SM,Drazba J,Vasanji A,Bokesch PM,Jani-gro D(2001)Regional variation in brain capillary density and vascu-lar response to ischemia.Brain Res 910:81-93.
Ceulemans AG,Zgavc T,Kooijman R,Hachimi-Idrissi S,Sarre S,Michotte Y(2010)The dual role of the neuroinflammatory response after ischemic stroke:modulatory effects of hypothermia.J Neuroin-flammation 7:74.
Chen X,Zhang X,Wang Y,Lei H,Su H,Zeng J,Pei Z,Huang R(2015)Inhibition of immunoproteasome reduces infarction volume and attenuates inflammatory reaction in a rat model of ischemic stroke.Cell Death Dis 6:e1626.
Dekanski D,Selakovic V,Piperski V,Radulovic Z,Korenic A,Rade-novic L(2011)Protective effect of olive leaf extract on hippocampal injury induced by transient global cerebral ischemia and reperfusion in Mongolian gerbils.Phytomedicine 18:1137-1143.
Globus MY,Busto R,Martinez E,Valdes I,Dietrich WD,Ginsberg MD(1991)Comparative effect of transient global ischemia on extracel-lular levels of glutamate,glycine,and gamma-aminobutyric acid in vulnerable and nonvulnerable brain regions in the rat.J Neurochem57:470-478.
Huttner HB,Bergmann O,Salehpour M,Rácz A,Tatarishvili J,Lind-gren E,Csonka T,Csiba L,Hortobágyi T,Méhes G,Englund E,Solnestam BW,Zdunek S,Scharenberg C,Str?m L,St?hl P,Sigur-geirsson B,Dahl A,Schwab S,Possnert G,et al.(2014)The age and genomic integrity of neurons after cortical stroke in humans.Nat Neurosci 17:801-803.
Hwang IK,Yoo KY,Kim DW,Lee HJ,Kang HY,Lee HY,Kang TC,Choi SY,Kim YS,Won MH(2006)Transient ischemia-induced changes of interleukin-2 and its receptor beta immunoreactivity and levels in the gerbil hippocampal CA1 region.Brain Res 1106:197-204.
Ji G,Yao X,Zang Z,Huang Z(1990)Antiarrhythmic effect of Oenanthe javanica(Bl.)DC.injection.Zhongguo Zhong Yao Za Zhi 15:429-431,448.
Jiang Q,Wang F,Tan HW,Li MY,Xu ZS,Tan GF,Xiong AS(2015)De novo transcriptome assembly,gene annotation,marker development,and miRNA potential target genes validation under abiotic stresses in Oenanthe javanica.Mol Genet Genomics 290:671-683.
Kaundal RK,Iyer S,Kumar A,Sharma SS(2009)Protective effects of pioglitazone against global cerebral ischemic-reperfusion injury in gerbils.J Pharmacol Sci 109:361-367.
Kim JY,Park J,Chang JY,Kim SH,Lee JE(2016)Inflammation after ischemic stroke:the role of leukocytes and glial cells.Exp Neurobiol25:241-251.
Kirino T(1982)Delayed neuronal death in the gerbil hippocampus fol-lowing ischemia.Brain Res 239:57-69.
Kuang X,Wang LF,Yu L,Li YJ,Wang YN,He Q,Chen C,Du JR(2014)Ligustilide ameliorates neuroinflammation and brain injury in fo-cal cerebral ischemia/reperfusion rats:involvement of inhibition of TLR4/peroxiredoxin 6 signaling.Free Radic Biol Med 71:165-175.
Ledeboer A,Breve JJ,Poole S,Tilders FJ,Van Dam AM(2000)Interleu-kin-10,interleukin-4,and transforming growth factor-beta differen-tially regulate lipopolysaccharide-induced production of pro-inflam-matory cytokines and nitric oxide in co-cultures of rat astroglial and microglial cells.Glia 30:134-142.
Lee JC,Park JH,Kim IH,Cho GS,Ahn JH,Tae HJ,Choi SY,Cho JH,Kim DW,Kwon YG,Kang IJ,Won MH,Kim YM(2017)Neuropro-tection of ischemic preconditioning is mediated by thioredoxin 2 in the hippocampal CA1 region following a subsequent transient cere-bral ischemia.Brain Pathol 27:276-291.
Liu RL,Xiong QJ,Shu Q,Wu WN,Cheng J,Fu H,Wang F,Chen JG,Hu ZL(2012)Hyperoside protects cortical neurons from oxy-gen-glucose deprivation-reperfusion induced injury via nitric oxide signal pathway.Brain Res 1469:164-173.
Ma CJ,Lee KY,Jeong EJ,Kim SH,Park J,Choi YH,Kim YC,Sung SH(2010)Persicarin from water dropwort(Oenanthe javanica)protects primary cultured rat cortical cells from glutamate-induced neurotox-icity.Phytother Res 24:913-918.
Murakami Y,Saito K,Hara A,Zhu Y,Sudo K,Niwa M,Fujii H,Wada H,Ishiguro H,Mori H,Seishima M(2005)Increases in tumor necro-sis factor-alpha following transient global cerebral ischemia do not contribute to neuron death in mouse hippocampus.J Neurochem93:1616-1622.
Niizuma K,Endo H,Nito C,Myer DJ,Chan PH(2009)Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia.Stroke 40:618-625.
Park JH,Long A,Owens K,Kristian T(2016)Nicotinamide mononu-cleotide inhibits post-ischemic NAD(+)degradation and dramati-cally ameliorates brain damage following global cerebral ischemia.Neurobiol Dis 95:102-110.
Park JH,Kim YH,Ahn JH,Choi SY,Hong S,Kim SK,Kang IJ,Kim YM,Lee TK,Won MH,Lee CH(2017a)Atomoxetine protects against NMDA receptor-mediated hippocampal neuronal death following transient global cerebral ischemia.Curr Neurovasc Res14:158-168.
Park JH,Cho JH,Kim IH,Ahn JH,Lee JC,Chen BH,Shin BN,Tae HJ,Yoo KY,Hong S,Kang IJ,Won MH,Kim JD(2015)Oenanthe Javani-ca extract protects against experimentally induced ischemic neuronal damage via its antioxidant effects.Chin Med J(Engl)128:2932-2937.
Park JH,Lee TK,Yan BC,Shin BN,Ahn JH,Kim IH,Cho JH,Lee JC,Hwang IK,Kim JD,Hong S,Lee YJ,Won MH,Kang IJ(2017b)Pre-treated Glehnia littoralis extract prevents neuronal death following transient global cerebral ischemia through increases of superoxide dismutase 1 and brain-derived neurotrophic factor expressions in the gerbil hippocampal cornu ammonis 1 area.Chin Med J(Engl)130:1796-1803.
Park JH,Park O,Cho JH,Chen BH,Kim IH,Ahn JH,Lee JC,Yan BC,Yoo KY,Lee CH,Hwang IK,Kwon SH,Lee YL,Won MH,Choi JH(2014)Anti-inflammatory effect of tanshinone I in neuroprotection against cerebral ischemia-reperfusion injury in the gerbil hippocam-pus.Neurochem Res 39:1300-1312.
Park JH,Park CW,Ahn JH,Choi SY,Shin MC,Cho JH,Lee TK,Kim IH,Cho JH,Lee JC,Kim YH,Kim YM,Kim JD,Tae HJ,Shin BN,Bae EJ,Chen BH,Won MH,Kang IJ(2017c)Neuroprotection and reduced gliosis by pre-and post-treatments of hydroquinone in a gerbil model of transient cerebral ischemia.Chem Biol Interact278:230-238.
Raghavan A,Shah ZA(2015)Withania somnifera improves ischemic stroke outcomes by attenuating PARP1-AIF-mediated caspase-inde-pendent apoptosis.Mol Neurobiol 52:1093-1105.
Sasaki T,Li W,Ohmoto T,Koike K(2016)Evaluation of canthinone al-kaloids as cerebral protective agents.Bioorg Med Chem Lett 26:4992-4995.
Somera-Molina KC,Nair S,Van Eldik LJ,Watterson DM,Wainwright MS(2009)Enhanced microglial activation and proinflammatory cytokine upregulation are linked to increased susceptibility to sei-zures and neurologic injury in a‘two-hit’seizure model.Brain Res1282:162-172.
Uno H,Matsuyama T,Akita H,Nishimura H,Sugita M(1997)In-duction of tumor necrosis factor-alpha in the mouse hippocampus following transient forebrain ischemia.J Cereb Blood Flow Metab17:491-499.
Vila N,Castillo J,Davalos A,Chamorro A(2000)Proinflammatory cy-tokines and early neurological worsening in ischemic stroke.Stroke31:2325-2329.
Wang J,Tsirka SE(2005)Neuroprotection by inhibition of matrix metalloproteinases in a mouse model of intracerebral haemorrhage.Brain 128:1622-1633.
Xiong X,Barreto GE,Xu L,Ouyang YB,Xie X,Giffard RG(2011)In-creased brain injury and worsened neurological outcome in interleu-kin-4 knockout mice after transient focal cerebral ischemia.Stroke42:2026-2032.
Yang MS,Park EJ,Sohn S,Kwon HJ,Shin WH,Pyo HK,Jin B,Choi KS,Jou I,Joe EH(2002)Interleukin-13 and-4 induce death of activated microglia.Glia 38:273-280.
Yang SA,Jung YS,Lee SJ,Park SC,Kim MJ,Lee EJ,Byun HJ,Jhee KH,Lee SP(2014)Hepatoprotective effects of fermented field wa-ter-dropwort(Oenanthe javanica)extract and its major constituents.Food Chem Toxicol 67:154-160.
Yang XB,Huang ZM,Cao WB,Zheng M,Chen HY,Zhang JZ(2000)Antidiabetic effect of Oenanthe javanica flavone.Acta Pharmacol Sin21:239-242.
Yin L,Ohtaki H,Nakamachi T,Dohi K,Iwai Y,Funahashi H,Makino R,Shioda S(2003)Expression of tumor necrosis factor alpha(TN-Falpha)following transient cerebral ischemia.Acta Neurochir Suppl86:93-96.
Yoo KY,Kim IH,Cho JH,Ahn JH,Park JH,Lee JC,Tae HJ,Kim DW,Kim JD,Hong S,Won MH,Kang IJ(2016)Neuroprotection of Chry-santhemum indicum Linne against cerebral ischemia/reperfusion in-jury by anti-inflammatory effect in gerbils.Neural Regen Res 11:270-277.
Zhang H,Park JH,Maharjan S,Park JA,Choi KS,Park H,Jeong Y,Ahn JH,Kim IH,Lee JC,Cho JH,Lee IK,Lee CH,Hwang IK,Kim YM,Suh YG,Won MH,Kwon YG(2017)Sac-1004,a vascular leakage blocker,reduces cerebral ischemia-reperfusion injury by suppressing blood-brain barrier disruption and inflammation.J Neuroinflamma-tion 14:122.
Zhao JJ,Song JQ,Pan SY,Wang K(2016)Treatment with isorhamnetin protects the brain against ischemic injury in mice.Neurochem Res41:1939-1948.
Zhu Y,Gao Y,Zheng D,Shui M,Yu K,Liu X,Lin Y,Su L,Yang W,Wang Y(2017)Design and evaluation of EphrinA1 mutants with cerebral protective effect.Sci Rep 7:1881.
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