ESE1 expression correlates with neuronal apoptosis in the hippocampus after cerebral ischemia/reperfusion injury
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摘要
Epithelial-specific ETS-1(ESE1), a member of the ETS transcription factor family, is widely expressed in multiple tissues and performs various functions in inflammation. During neuroinflammation, ESE1 promotes neuronal apoptosis; however, the expression and biological functions of ESE1 remain unclear after cerebral ischemia/reperfusion. We performed in vivo and in vitro experiments to explore the role of ESE1 in cerebral ischemic injury. A modified four vessel occlusion method was used in adult Sprague-Dawley rats. At 6, 12, 24, 48, and 72 hours after model induction, the hippocampus was collected for analysis. Western blot assays and immunohistochemistry showed that the expression of ESE1, phosphorylated p65 and active caspase-3 was significantly up-regulated after ischemia. Double immunofluorescence staining indicated that ESE1 and NeuN were mostly co-located in the hippocampus after ischemia. Furthermore, ESE1 was also co-expressed with active caspase-3. PC12 cells were stimulated with cobalt chloride(CoCl_2) to establish a chemical hypoxia model. After ESE1 knockdown by siRNA for 6 hours, cell viability was detected by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-H-tetrazolium bromide assays. The levels of ESE1, phosphorylated p65 and active caspase-3 were also remarkably increased in PC12 cells after CoCl_2 stimulation. After ESE1 knockdown, PC12 cell viability was increased after hypoxia. siRNA knockdown of ESE1 decreased the level of p-p65 and active caspase-3 after CoCl_2 stimulation. These data reveal that ESE1 levels are elevated in the hippocampus after cerebral ischemia/reperfusion injury. This may play a role in neuronal apoptosis via activation of the nuclear factor-κB pathway.
Epithelial-specific ETS-1(ESE1), a member of the ETS transcription factor family, is widely expressed in multiple tissues and performs various functions in inflammation. During neuroinflammation, ESE1 promotes neuronal apoptosis; however, the expression and biological functions of ESE1 remain unclear after cerebral ischemia/reperfusion. We performed in vivo and in vitro experiments to explore the role of ESE1 in cerebral ischemic injury. A modified four vessel occlusion method was used in adult Sprague-Dawley rats. At 6, 12, 24, 48, and 72 hours after model induction, the hippocampus was collected for analysis. Western blot assays and immunohistochemistry showed that the expression of ESE1, phosphorylated p65 and active caspase-3 was significantly up-regulated after ischemia. Double immunofluorescence staining indicated that ESE1 and NeuN were mostly co-located in the hippocampus after ischemia. Furthermore, ESE1 was also co-expressed with active caspase-3. PC12 cells were stimulated with cobalt chloride(CoCl_2) to establish a chemical hypoxia model. After ESE1 knockdown by siRNA for 6 hours, cell viability was detected by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-H-tetrazolium bromide assays. The levels of ESE1, phosphorylated p65 and active caspase-3 were also remarkably increased in PC12 cells after CoCl_2 stimulation. After ESE1 knockdown, PC12 cell viability was increased after hypoxia. siRNA knockdown of ESE1 decreased the level of p-p65 and active caspase-3 after CoCl_2 stimulation. These data reveal that ESE1 levels are elevated in the hippocampus after cerebral ischemia/reperfusion injury. This may play a role in neuronal apoptosis via activation of the nuclear factor-κB pathway.
Epithelial-specific ETS-1(ESE1), a member of the ETS transcription factor family, is widely expressed in multiple tissues and performs various functions in inflammation. During neuroinflammation, ESE1 promotes neuronal apoptosis; however, the expression and biological functions of ESE1 remain unclear after cerebral ischemia/reperfusion. We performed in vivo and in vitro experiments to explore the role of ESE1 in cerebral ischemic injury. A modified four vessel occlusion method was used in adult Sprague-Dawley rats. At 6, 12, 24, 48, and 72 hours after model induction, the hippocampus was collected for analysis. Western blot assays and immunohistochemistry showed that the expression of ESE1, phosphorylated p65 and active caspase-3 was significantly up-regulated after ischemia. Double immunofluorescence staining indicated that ESE1 and NeuN were mostly co-located in the hippocampus after ischemia. Furthermore, ESE1 was also co-expressed with active caspase-3. PC12 cells were stimulated with cobalt chloride(CoCl_2) to establish a chemical hypoxia model. After ESE1 knockdown by siRNA for 6 hours, cell viability was detected by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-H-tetrazolium bromide assays. The levels of ESE1, phosphorylated p65 and active caspase-3 were also remarkably increased in PC12 cells after CoCl_2 stimulation. After ESE1 knockdown, PC12 cell viability was increased after hypoxia. siRNA knockdown of ESE1 decreased the level of p-p65 and active caspase-3 after CoCl_2 stimulation. These data reveal that ESE1 levels are elevated in the hippocampus after cerebral ischemia/reperfusion injury. This may play a role in neuronal apoptosis via activation of the nuclear factor-κB pathway.
引文
Azadbakht AA,Radahmadi M,Javanmard SH,Reisi P(2015)The effects of doxepin on stress-induced learning,memory impairments,and TNF-alpha level in the rat hippocampus.Res in Pharmaceut Sci10:460-465.
Bai S1,Li D,Zhou Z,Cao J,Xu T,Zhang X,Wang Y,Guo J,Zhang Y(2015)Interleukin-1 receptor-associated kinase 1/4 as a novel target for inhibiting neointimal formation after carotid balloon injury.JAtheroscler Thromb 22:1317-1337.
Baldwin AS(2001)Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB.J Clin Invest 107:241-246.
Broughton BR,Reutens DC,Sobey CG(2009)Apoptotic mechanisms after cerebral ischemia.Stroke 40:e331-339.
Durukan A,Tatlisumak T(2007)Acute ischemic stroke:overview of major experimental rodent models,pathophysiology,and therapy of focal cerebral ischemia.Comp Biochem Phys C 87:179-197.
Eltzschig HK,Eckle T(2011)Ischemia and reperfusion-from mechanism to translation.Nat Med 17:1391-1401.
Feng Y,Xue H,Zhu J,Yang L,Zhang F,Qian R,Lin W,Wang Y(2016)ESE1 is associated with neuronal apoptosis in lipopolysaccharide induced neuroinflammation.Neurochem Res 41:2752-2762.
Findlay VJ,LaRue AC,Turner DP,Watson PM,Watson DK(2013)Understanding the role of ETS-mediated gene regulation in complex biological processes.Adv Cancer Res 119:1-61.
Gallant S,Gilkeson G.ETS transcription factors and regulation of immunity.Arch Immunol Ther Exp 54:149-163.
Garrett-Sinha LA(2013)Review of Ets1 structure,function,and roles in immunity.Cell Mol Life Sci 70:3375-3390.
George PM,Steinberg GK(2015)Novel stroke therapeutics:unraveling stroke pathophysiology and its impact on clinical treatments.Neuron 87:297-309.
Gesuete R,Kohama SG,Stenzel-Poore MP(2014)Toll-like receptors and ischemic brain injury.J Neuropath Exp Neur 73:378-386.
Gorina R,Font-Nieves M,Marquez-Kisinousky L,Santalucia T,Planas AM(2011)Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling,MAPK,and Jak1/Stat1 pathways.Glia 59:242-255.
Grall F,Gu X,Tan L,Cho JY,Inan MS,Pettit AR,Thamrongsak U,Choy BK,Manning C,Akbarali Y,Zerbini L,Rudders S,Goldring SR,Gravallese EM,Oettgen P,Goldring MB,Libermann TA(2003)Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1.Arthritis Rheumatol48:1249-1260.
Grall FT,Prall WC,Wei W,Gu X,Cho JY,Choy BK,Zerbini LF,Inan MS,Goldring SR,Gravallese EM,Goldring MB,Oettgen P,Libermann TA(2005)The Ets transcription factor ESE-1 mediates induction of the COX-2 gene by LPS in monocytes.FEBS J 272:1676-1687.
Guo L,Lan J,Lin Y,Guo P,Nie Q,Mao Q,Ren L,Qiu Y(2013)Hypoxia/ischemia up-regulates Id2 expression in neuronal cells in vivo and in vitro.Neurosci lett 554:88-93.
Hu Y,Duan M,Liang S,Wang Y,Feng Y(2015)Senkyunolide I protects rat brain against focal cerebral ischemia-reperfusion injury by up-regulating p-Erk1/2,Nrf2/HO-1 and inhibiting caspase 3.Brain Res 1605:39-48.
Kim JY,Kawabori M,Yenari MA(2014)Innate inflammatory responses in stroke:mechanisms and potential therapeutic targets.Curr Med Chem 21:2076-2097.
Li L,Miao X,Ni R,Miao X,Wang L,Gu X,Yan L,Tang Q,Zhang D(2015a)Epithelial-specific ETS-1(ESE1/ELF3)regulates apoptosis of intestinal epithelial cells in ulcerative colitis via accelerating NF-kappaB activation.Immunol Res 62:198-212.
Li LX,Cheng YF,Lin HB,Wang C,Xu JP,Zhang HT(2011)Prevention of cerebral ischemia-induced memory deficits by inhibition of phosphodiesterase-4 in rats.Metab Brain Dis 26:37-47.
Li X,Zhao H,Tan X,Kostrzewa RM,Du G,Chen Y,Zhu J,Miao Z,Yu H,Kong J,Xu X(2015b)Inhibition of connexin43 improves functional recovery after ischemic brain injury in neonatal rats.Glia63:1553-1567.
Lo EH(2010)Degeneration and repair in central nervous system disease.Nat Med 16:1205-1209.
Longley DB,Allen WL,McDermott U,Wilson TR,Latif T,Boyer J,Lynch M,Johnston PG(2004)The roles of thymidylate synthase and p53 in regulating Fas-mediated apoptosis in response to antimetabolites.Clin Cancer Res 10:3562-3571.
Longoni N,Sarti M,Albino D,Civenni G,Malek A,Ortelli E,Pinton S,Mello-Grand M,Ostano P,D’Ambrosio G,Sessa F,Garcia-Escudero R,Thalmann GN,Chiorino G,Catapano CV,Carbone GM(2013)ETS transcription factor ESE1/ELF3 orchestrates a positive feedback loop that constitutively activates NF-kappaB and drives prostate cancer progression.Cancer Res 73:4533-4547.
Lozano R,Naghavi M,Foreman K,Lim S,Shibuya K,Aboyans V,Abraham J,Adair T,Aggarwal R,Ahn SY,Alvarado M,Anderson HR,Anderson LM,Andrews KG,Atkinson C,Baddour LM,Barker-Collo S,Bartels DH,Bell ML,Benjamin EJ,et al.(2012)Global and regional mortality from 235 causes of death for 20 age groups in1990 and 2010:a systematic analysis for the Global Burden of Disease Study 2010.Lancet 380:2095-2128.
Lu Q,Tucker D,Dong Y,Zhao N,Zhang Q(2016)Neuroprotective and functional improvement effects of methylene blue in global cerebral ischemia.Mol Neurobiol 53:5344-5355.
Machado RA,Constantino Lde S,Tomasi CD,Rojas HA,Vuolo FS,Vitto MF,Cesconetto PA,de Souza CT,Ritter C,Dal-Pizzol F(2012)Sodium butyrate decreases the activation of NF-kappaB reducing inflammation and oxidative damage in the kidney of rats subjected to contrast-induced nephropathy.Nephrol Dial Transplant 27:3136-3140.
Maroulakou IG,Bowe DB(2000)Expression and function of Ets transcription factors in mammalian development:a regulatory network.Oncogene 19:6432-6442.
Mozaffarian D,Benjamin EJ,Go AS,Arnett DK,Blaha MJ,Cushman M(2015).Heart disease and stroke statistics-2015 update:a report from the American Heart Association.Circulation 131:e29-e322.
Mirzayans R,Andrais B,Kumar P,Murray D(2016)The growing complexity of cancer cell response to dna-damaging agents:caspase 3mediates cell death or survival?Int J Mol Sci 17:E708.
Mitani A,Andou Y,Kataoka K(1992)Selective vulnerability of hippocampal CA1 neurons cannot be explained in terms of an increase in glutamate concentration during ischemia in the gerbil:brain microdialysis study.Neuroscience 48:307-313.
Molinaro P,Viggiano D,Nistico R,Sirabella R,Secondo A,Boscia F,Pannaccione A,Scorziello A,Mehdawy B,Sokolow S,Herchuelz A,Di Renzo GF,Annunziato L(2011)Na+-Ca2+exchanger(NCX3)knock-out mice display an impairment in hippocampal long-term potentiation and spatial learning and memory.J Neurosci 31:7312-7321.
Oettgen P,Alani RM,Barcinski MA,Brown L,Akbarali Y,Boltax J,Kunsch C,Munger K,Libermann TA(1997)Isolation and characterization of a novel epithelium-specific transcription factor,ESE-1,a member of the ets family.Mol Cell Biol 17:4419-4433.
Okabe N,Miyamoto O(2018)Role and limitations of rehabilitation-induced neural network remodeling after stroke.Neural Regen Res13:2087-2088.
Oliver JR,Kushwah R,Hu J(2012)Multiple roles of the epithelium-specific ETS transcription factor,ESE-1,in development and disease.Lab Invest 92:320-330.
Powers WJ,Rabinstein AA,Ackerson T,Adeoye OM,Bambakidis NC,Becker K(2018)2018 Guidelines for the early management of patients with acute ischemic stroke:a guideline for healthcare professionals from the American Heart Association/American Stroke Association.Stroke 49:e46-e110.
Roset R,Ortet L,Gil-Gomez G(2007)Role of Bcl-2 family members on apoptosis:what we have learned from knock-out mice.Front Biosci12:4722-4730.
Saver JL,Fonarow GC,Smith EE,Reeves MJ,Grau-Sepulveda MV,Pan W(2013)Time to treatment with intravenous tissue plasminogen activator and outcome from acute ischemic stroke.JAMA 309:2480-2488.
Seidel JJ,Graves BJ(2002)An ERK2 docking site in the pointed domain distinguishes a subset of ETS transcription factors.Genes Dev16:127-137.
Seth A,Watson DK(2005)ETS transcription factors and their emerging roles in human cancer.Eur J Cancer Care 41:2462-2478.
Shichita T,Sakaguchi R,Suzuki M,Yoshimura A(2012)Post-ischemic inflammation in the brain.Front Immunol 3:132.
Sinh N D,Endo K,Miyazawa K(2017)Ets1 and ESE1 reciprocally regulate expression of ZEB1/ZEB2,dependent on ERK1/2 activity,in breast cancer cells.Cancer Sci 108:952-960.
Tan KO,Fu NY,Sukumaran SK,Chan SL,Kang JH,Poon KL,Chen BS,Yu VC(2005)MAP-1 is a mitochondrial effector of Bax.Proc Natl Acad Sci U S A 102:14623-14628.
Tao T,Zhao M,Yang W,Bo Y,Li W(2014)Neuroprotective effects of therapeutic hypercapnia on spatial memory and sensorimotor impairment via anti-apoptotic mechanisms after focal cerebral ischemia/reperfusion.Neurosci Lett 573:1-6.
Terao S,Yilmaz G,Stokes KY,Ishikawa M,Kawase T,Granger DN(2008)Inflammatory and injury responses to ischemic stroke in obese mice.Stroke 39:943-950.
Wang JL,Chen ZF,Chen HM,Wang MY,Kong X,Wang YC,Sun TT,Hong J,Zou W,Xu J,Fang JY(2014)Elf3 drives beta-catenin transactivation and associates with poor prognosis in colorectal cancer.Cell Death Dis 5:e1263.
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.
Xiao L,Lan A,Mo L,Xu W,Jiang N,Hu F,Feng J,Zhang C(2012)Hydrogen sulfide protects PC12 cells against reactive oxygen species and extracellular signal-regulated kinase 1/2-mediated downregulation of glutamate transporter-1 expression induced by chemical hypoxia.Int J Mol Med 30:1126-1132.
Yang X,Lee SH(2016)Identification of ESE1 as aβ-catenin binding protein.Anticancer Res 36:2697.
Yang YF,Chen Z,Hu SL,Hu J,Li B,Li JT,Wei LJ,Qian ZM,Lin JK,Feng H,Zhu G(2011)Interleukin-1 receptor associated kinases-1/4inhibition protects against acute hypoxia/ischemia-induced neuronal injury in vivo and in vitro.Neuroscience 196:25-34.
Yi JH,Park SW,Kapadia R,Vemuganti R(2007)Role of transcription factors in mediating post-ischemic cerebral inflammation and brain damage.Neurochem Int 50:1014-1027.
Zhan Y,Yuan L,Kondo M,Oettgen P(2010)The counter-regulatory effects of ESE-1 during angiotensin II-mediated vascular inflammation and remodeling.Am J Hypertens 23:1312-1317.
Zhang DL,Li D,Wang MJ(2018)Mechanism and application of stem cell transplantation in the treatment of ischemic stroke.Zhongguo Zuzhi Gongcheng Yanjiu 22:5393-5398.
Zheng PD,Mungur R,Zhou HJ,Hassan M,Jiang SN,Zheng JS(2018)Ginkgolide B promotes the proliferation and differentiation of neural stem cells following cerebral ischemia/reperfusion injury,both in vivo and in vitro.Neural Regen Res 13:1204-1211.
Bai S1,Li D,Zhou Z,Cao J,Xu T,Zhang X,Wang Y,Guo J,Zhang Y(2015)Interleukin-1 receptor-associated kinase 1/4 as a novel target for inhibiting neointimal formation after carotid balloon injury.JAtheroscler Thromb 22:1317-1337.
Baldwin AS(2001)Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB.J Clin Invest 107:241-246.
Broughton BR,Reutens DC,Sobey CG(2009)Apoptotic mechanisms after cerebral ischemia.Stroke 40:e331-339.
Durukan A,Tatlisumak T(2007)Acute ischemic stroke:overview of major experimental rodent models,pathophysiology,and therapy of focal cerebral ischemia.Comp Biochem Phys C 87:179-197.
Eltzschig HK,Eckle T(2011)Ischemia and reperfusion-from mechanism to translation.Nat Med 17:1391-1401.
Feng Y,Xue H,Zhu J,Yang L,Zhang F,Qian R,Lin W,Wang Y(2016)ESE1 is associated with neuronal apoptosis in lipopolysaccharide induced neuroinflammation.Neurochem Res 41:2752-2762.
Findlay VJ,LaRue AC,Turner DP,Watson PM,Watson DK(2013)Understanding the role of ETS-mediated gene regulation in complex biological processes.Adv Cancer Res 119:1-61.
Gallant S,Gilkeson G.ETS transcription factors and regulation of immunity.Arch Immunol Ther Exp 54:149-163.
Garrett-Sinha LA(2013)Review of Ets1 structure,function,and roles in immunity.Cell Mol Life Sci 70:3375-3390.
George PM,Steinberg GK(2015)Novel stroke therapeutics:unraveling stroke pathophysiology and its impact on clinical treatments.Neuron 87:297-309.
Gesuete R,Kohama SG,Stenzel-Poore MP(2014)Toll-like receptors and ischemic brain injury.J Neuropath Exp Neur 73:378-386.
Gorina R,Font-Nieves M,Marquez-Kisinousky L,Santalucia T,Planas AM(2011)Astrocyte TLR4 activation induces a proinflammatory environment through the interplay between MyD88-dependent NFkappaB signaling,MAPK,and Jak1/Stat1 pathways.Glia 59:242-255.
Grall F,Gu X,Tan L,Cho JY,Inan MS,Pettit AR,Thamrongsak U,Choy BK,Manning C,Akbarali Y,Zerbini L,Rudders S,Goldring SR,Gravallese EM,Oettgen P,Goldring MB,Libermann TA(2003)Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1.Arthritis Rheumatol48:1249-1260.
Grall FT,Prall WC,Wei W,Gu X,Cho JY,Choy BK,Zerbini LF,Inan MS,Goldring SR,Gravallese EM,Goldring MB,Oettgen P,Libermann TA(2005)The Ets transcription factor ESE-1 mediates induction of the COX-2 gene by LPS in monocytes.FEBS J 272:1676-1687.
Guo L,Lan J,Lin Y,Guo P,Nie Q,Mao Q,Ren L,Qiu Y(2013)Hypoxia/ischemia up-regulates Id2 expression in neuronal cells in vivo and in vitro.Neurosci lett 554:88-93.
Hu Y,Duan M,Liang S,Wang Y,Feng Y(2015)Senkyunolide I protects rat brain against focal cerebral ischemia-reperfusion injury by up-regulating p-Erk1/2,Nrf2/HO-1 and inhibiting caspase 3.Brain Res 1605:39-48.
Kim JY,Kawabori M,Yenari MA(2014)Innate inflammatory responses in stroke:mechanisms and potential therapeutic targets.Curr Med Chem 21:2076-2097.
Li L,Miao X,Ni R,Miao X,Wang L,Gu X,Yan L,Tang Q,Zhang D(2015a)Epithelial-specific ETS-1(ESE1/ELF3)regulates apoptosis of intestinal epithelial cells in ulcerative colitis via accelerating NF-kappaB activation.Immunol Res 62:198-212.
Li LX,Cheng YF,Lin HB,Wang C,Xu JP,Zhang HT(2011)Prevention of cerebral ischemia-induced memory deficits by inhibition of phosphodiesterase-4 in rats.Metab Brain Dis 26:37-47.
Li X,Zhao H,Tan X,Kostrzewa RM,Du G,Chen Y,Zhu J,Miao Z,Yu H,Kong J,Xu X(2015b)Inhibition of connexin43 improves functional recovery after ischemic brain injury in neonatal rats.Glia63:1553-1567.
Lo EH(2010)Degeneration and repair in central nervous system disease.Nat Med 16:1205-1209.
Longley DB,Allen WL,McDermott U,Wilson TR,Latif T,Boyer J,Lynch M,Johnston PG(2004)The roles of thymidylate synthase and p53 in regulating Fas-mediated apoptosis in response to antimetabolites.Clin Cancer Res 10:3562-3571.
Longoni N,Sarti M,Albino D,Civenni G,Malek A,Ortelli E,Pinton S,Mello-Grand M,Ostano P,D’Ambrosio G,Sessa F,Garcia-Escudero R,Thalmann GN,Chiorino G,Catapano CV,Carbone GM(2013)ETS transcription factor ESE1/ELF3 orchestrates a positive feedback loop that constitutively activates NF-kappaB and drives prostate cancer progression.Cancer Res 73:4533-4547.
Lozano R,Naghavi M,Foreman K,Lim S,Shibuya K,Aboyans V,Abraham J,Adair T,Aggarwal R,Ahn SY,Alvarado M,Anderson HR,Anderson LM,Andrews KG,Atkinson C,Baddour LM,Barker-Collo S,Bartels DH,Bell ML,Benjamin EJ,et al.(2012)Global and regional mortality from 235 causes of death for 20 age groups in1990 and 2010:a systematic analysis for the Global Burden of Disease Study 2010.Lancet 380:2095-2128.
Lu Q,Tucker D,Dong Y,Zhao N,Zhang Q(2016)Neuroprotective and functional improvement effects of methylene blue in global cerebral ischemia.Mol Neurobiol 53:5344-5355.
Machado RA,Constantino Lde S,Tomasi CD,Rojas HA,Vuolo FS,Vitto MF,Cesconetto PA,de Souza CT,Ritter C,Dal-Pizzol F(2012)Sodium butyrate decreases the activation of NF-kappaB reducing inflammation and oxidative damage in the kidney of rats subjected to contrast-induced nephropathy.Nephrol Dial Transplant 27:3136-3140.
Maroulakou IG,Bowe DB(2000)Expression and function of Ets transcription factors in mammalian development:a regulatory network.Oncogene 19:6432-6442.
Mozaffarian D,Benjamin EJ,Go AS,Arnett DK,Blaha MJ,Cushman M(2015).Heart disease and stroke statistics-2015 update:a report from the American Heart Association.Circulation 131:e29-e322.
Mirzayans R,Andrais B,Kumar P,Murray D(2016)The growing complexity of cancer cell response to dna-damaging agents:caspase 3mediates cell death or survival?Int J Mol Sci 17:E708.
Mitani A,Andou Y,Kataoka K(1992)Selective vulnerability of hippocampal CA1 neurons cannot be explained in terms of an increase in glutamate concentration during ischemia in the gerbil:brain microdialysis study.Neuroscience 48:307-313.
Molinaro P,Viggiano D,Nistico R,Sirabella R,Secondo A,Boscia F,Pannaccione A,Scorziello A,Mehdawy B,Sokolow S,Herchuelz A,Di Renzo GF,Annunziato L(2011)Na+-Ca2+exchanger(NCX3)knock-out mice display an impairment in hippocampal long-term potentiation and spatial learning and memory.J Neurosci 31:7312-7321.
Oettgen P,Alani RM,Barcinski MA,Brown L,Akbarali Y,Boltax J,Kunsch C,Munger K,Libermann TA(1997)Isolation and characterization of a novel epithelium-specific transcription factor,ESE-1,a member of the ets family.Mol Cell Biol 17:4419-4433.
Okabe N,Miyamoto O(2018)Role and limitations of rehabilitation-induced neural network remodeling after stroke.Neural Regen Res13:2087-2088.
Oliver JR,Kushwah R,Hu J(2012)Multiple roles of the epithelium-specific ETS transcription factor,ESE-1,in development and disease.Lab Invest 92:320-330.
Powers WJ,Rabinstein AA,Ackerson T,Adeoye OM,Bambakidis NC,Becker K(2018)2018 Guidelines for the early management of patients with acute ischemic stroke:a guideline for healthcare professionals from the American Heart Association/American Stroke Association.Stroke 49:e46-e110.
Roset R,Ortet L,Gil-Gomez G(2007)Role of Bcl-2 family members on apoptosis:what we have learned from knock-out mice.Front Biosci12:4722-4730.
Saver JL,Fonarow GC,Smith EE,Reeves MJ,Grau-Sepulveda MV,Pan W(2013)Time to treatment with intravenous tissue plasminogen activator and outcome from acute ischemic stroke.JAMA 309:2480-2488.
Seidel JJ,Graves BJ(2002)An ERK2 docking site in the pointed domain distinguishes a subset of ETS transcription factors.Genes Dev16:127-137.
Seth A,Watson DK(2005)ETS transcription factors and their emerging roles in human cancer.Eur J Cancer Care 41:2462-2478.
Shichita T,Sakaguchi R,Suzuki M,Yoshimura A(2012)Post-ischemic inflammation in the brain.Front Immunol 3:132.
Sinh N D,Endo K,Miyazawa K(2017)Ets1 and ESE1 reciprocally regulate expression of ZEB1/ZEB2,dependent on ERK1/2 activity,in breast cancer cells.Cancer Sci 108:952-960.
Tan KO,Fu NY,Sukumaran SK,Chan SL,Kang JH,Poon KL,Chen BS,Yu VC(2005)MAP-1 is a mitochondrial effector of Bax.Proc Natl Acad Sci U S A 102:14623-14628.
Tao T,Zhao M,Yang W,Bo Y,Li W(2014)Neuroprotective effects of therapeutic hypercapnia on spatial memory and sensorimotor impairment via anti-apoptotic mechanisms after focal cerebral ischemia/reperfusion.Neurosci Lett 573:1-6.
Terao S,Yilmaz G,Stokes KY,Ishikawa M,Kawase T,Granger DN(2008)Inflammatory and injury responses to ischemic stroke in obese mice.Stroke 39:943-950.
Wang JL,Chen ZF,Chen HM,Wang MY,Kong X,Wang YC,Sun TT,Hong J,Zou W,Xu J,Fang JY(2014)Elf3 drives beta-catenin transactivation and associates with poor prognosis in colorectal cancer.Cell Death Dis 5:e1263.
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.
Xiao L,Lan A,Mo L,Xu W,Jiang N,Hu F,Feng J,Zhang C(2012)Hydrogen sulfide protects PC12 cells against reactive oxygen species and extracellular signal-regulated kinase 1/2-mediated downregulation of glutamate transporter-1 expression induced by chemical hypoxia.Int J Mol Med 30:1126-1132.
Yang X,Lee SH(2016)Identification of ESE1 as aβ-catenin binding protein.Anticancer Res 36:2697.
Yang YF,Chen Z,Hu SL,Hu J,Li B,Li JT,Wei LJ,Qian ZM,Lin JK,Feng H,Zhu G(2011)Interleukin-1 receptor associated kinases-1/4inhibition protects against acute hypoxia/ischemia-induced neuronal injury in vivo and in vitro.Neuroscience 196:25-34.
Yi JH,Park SW,Kapadia R,Vemuganti R(2007)Role of transcription factors in mediating post-ischemic cerebral inflammation and brain damage.Neurochem Int 50:1014-1027.
Zhan Y,Yuan L,Kondo M,Oettgen P(2010)The counter-regulatory effects of ESE-1 during angiotensin II-mediated vascular inflammation and remodeling.Am J Hypertens 23:1312-1317.
Zhang DL,Li D,Wang MJ(2018)Mechanism and application of stem cell transplantation in the treatment of ischemic stroke.Zhongguo Zuzhi Gongcheng Yanjiu 22:5393-5398.
Zheng PD,Mungur R,Zhou HJ,Hassan M,Jiang SN,Zheng JS(2018)Ginkgolide B promotes the proliferation and differentiation of neural stem cells following cerebral ischemia/reperfusion injury,both in vivo and in vitro.Neural Regen Res 13:1204-1211.