Neuroprotective Effects of Necrostatin-1 Against Oxidative Stress–Induced Cell Damage: an Involvement of Cathepsin D Inhibition
Tóm tắt
Necroptosis, a recently discovered form of non-apoptotic programmed cell death, can be implicated in many pathological conditions including neuronal cell death. Moreover, an inhibition of this process by necrostatin-1 (Nec-1) has been shown to be neuroprotective in in vitro and in vivo models of cerebral ischemia. However, the involvement of this type of cell death in oxidative stress–induced neuronal cell damage is less recognized. Therefore, we tested the effects of Nec-1, an inhibitor of necroptosis, in the model of hydrogen peroxide (H2O2)-induced cell damage in human neuroblastoma SH-SY5Y and murine hippocampal HT-22 cell lines. The data showed that Nec-1 (10–40 μM) attenuated the cell death induced by H2O2 in undifferentiated (UN-) and neuronal differentiated (RA-) SH-SY5Y cells with a higher efficacy in the former cell type. Moreover, Nec-1 partially reduced cell damage induced by 6-hydroxydopamine in UN- and RA-SH-SY5Y cells. The protective effect of Nec-1 was of similar magnitude as the effect of a caspase-3 inhibitor in both cell phenotypes and this effect were not potentiated after combined treatment. Furthermore, the non-specific apoptosis and necroptosis inhibitor curcumin augmented the beneficial effect of Nec-1 against H2O2-evoked cell damage albeit only in RA-SH-SY5Y cells. Next, it was found that the mechanisms of neuroprotective effect of Nec-1 against H2O2-induced cell damage in SH-SY5Y cells involved the inhibition of lysosomal protease, cathepsin D, but not caspase-3 or calpain activities. In HT-22 cells, Nec-1 was protective in two models of oxidative stress (H2O2 and glutamate) and that effect was blocked by a caspase inhibitor. Our data showed neuroprotective effects of the necroptosis inhibitor, Nec-1, against oxidative stress–induced cell damage and pointed to involvement of cathepsin D inhibition in the mechanism of its action. Moreover, a cell type–specific interplay between necroptosis and apoptosis has been demonstrated.
Từ khóa
Tài liệu tham khảo
Agholme L, Lindström T, Kågedal K, Marcusson J, Hallbeck M (2010) An in vitro model for neuroscience: differentiation of SH-SY5Y cells into cells with morphological and biochemical characteristics of mature neurons. J Alzheimers Dis 20:1069–1082
Arrázola MS, Saquel C, Catalán RJ, Barrientos SA, Hernandez DE, Martínez NW, Catenaccio A, Court FA (2019) Axonal degeneration is mediated by necroptosis activation. J Neurosci 39:3832–3844
Askalan R, Gabarin N, Armstrong EA, Fang Liu Y, Couchman D, Yager JY (2015) Mechanisms of neurodegeneration after severe hypoxic-ischemic injury in the neonatal rat brain. Brain Res 1629:94–103
Biton S, Ashkenazi A (2011) NEMO and RIP1 control cell fate in response to extensive DNA damage via TNF-α feedforward signaling. Cell 145:92–103
Bollino D, Balan I, Aurelian L (2015) Valproic acid induces neuronal cell death through a novel calpain-dependent necroptosis pathway. J Neurochem 133:174–186
Caccamo A, Branca C, Piras IS, Ferreira E, Huentelman MJ, Liang WS, Readhead B, Dudley JT, Spangenberg EE, Green KN, Belfiore R, Winslow W, Oddo S (2017) Necroptosis activation in Alzheimer’s disease. Nat Neurosci 20:1236–1246
Castelli V, Benedetti E, Antonosante A, Catanesi M, Pitari G, Ippoliti R, Cimini A, d’Angelo M (2019) Neuronal cells rearrangement during aging and neurodegenerative disease: metabolism, oxidative stress and organelles dynamic. Front Mol Neurosci 12:132
Castino R, Bellio N, Nicotra G, Follo C, Trincheri NF, Isidoro C (2007) Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells. Free Radic Biol Med 42:1305–1316
Castino R, Thepparit C, Bellio N, Murphy D, Isidoro C (2008) Akt induces apoptosis in neuroblastoma cells expressing a C98X vasopressin mutant following autophagy suppression. J Neuroendocrinol 20:1165–1175
Castino R, Bellio N, Follo C, Murphy D, Isidoro C (2010) Inhibition of PI3k class III-dependent autophagy prevents apoptosis and necrosis by oxidative stress in dopaminergic neuroblastoma cells. Toxicol Sci 117:152–162
Castino R, Fiorentino I, Cagnin M, Giovia A, Isidoro C (2011) Chelation of lysosomal iron protects dopaminergic SH-SY5Y neuroblastoma cells from hydrogen peroxide toxicity by precluding autophagy and Akt dephosphorylation. Toxicol Sci 123:523–541
Cenini G, Lloret A, Cascella R (2019) Oxidative stress in neurodegenerative diseases: from a mitochondrial point of view. Oxidative Med Cell Longev 2019:2105607
Chahory S, Keller N, Martin E, Omri B, Crisanti P, Torriglia A (2010) Light induced retinal degeneration activates a caspase-independent pathway involving cathepsin D. Neurochem Int 57:278–287
Chavez-Valdez R, Martin LJ, Flock DL, Northington FJ (2012) Necrostatin-1 attenuates mitochondrial dysfunction in neurons and astrocytes following neonatal hypoxia-ischemia. Neuroscience 219:192–203
Chavez-Valdez R, Flock DL, Martin LJ, Northington FJ (2016) Endoplasmic reticulum pathology and stress response in neurons precede programmed necrosis after neonatal hypoxia-ischemia. Int J Dev Neurosci 48:58–70
Chen S, Zhou C, Yu H, Tao L, An Y, Zhang X, Wang Y, Wang Y, Xiao R (2019) 27-Hydroxycholesterol contributes to lysosomal membrane permeabilization-mediated pyroptosis in co-cultured SH-SY5Y cells and C6 cells. Front Mol Neurosci 12:14
Cheung YT, Lau WK, Yu MS, Lai CS, Yeung SC, So KF, Chang RC (2009) Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research. Neurotoxicology 30:127–135
Chinskey ND, Besirli CG, Zacks DN (2014) Retinal cell death and current strategies in retinal neuroprotection. Curr Opin Ophthalmol 25:228–233
Chwastek J, Jantas D, Lasoń W (2017) The ATM kinase inhibitor KU-55933 provides neuroprotection against hydrogen peroxide-induced cell damage via a γH2AX/p-p53/caspase-3-independent mechanism: inhibition of calpain and cathepsin D. Int J Biochem Cell Biol 87:38–53
Cole KK, Perez-Polo JR (2002) Poly(ADP-ribose) polymerase inhibition prevents both apoptotic-like delayed neuronal death and necrosis after H(2)O(2) injury. J Neurochem 82:19–29
Crabtree D, Dodson M, Ouyang X, Boyer-Guittaut M, Liang Q, Ballestas ME, Fineberg N, Zhang J (2014) Over-expression of an inactive mutant cathepsin D increases endogenous alpha-synuclein and cathepsin B activity in SH-SY5Y cells. J Neurochem 128:950–961
Dai MC, Zhong ZH, Sun YH, Sun QF, Wang YT, Yang GY, Bian LG (2013) Curcumin protects against iron induced neurotoxicity in primary cortical neurons by attenuating necroptosis. Neurosci Lett 536:41–46
Degterev A, Huang Z, Boyce M, Li Y, Jagtap P, Mizushima N, Cuny GD, Mitchison TJ, Moskowitz MA, Yuan J (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112–119
Degterev A, Hitomi J, Germscheid M, Ch’en IL, Korkina O, Teng X, Abbott D, Cuny GD, Yuan C, Wagner G, Hedrick SM, Gerber SA, Lugovskoy A, Yuan J (2008) Identification of RIP1 kinase as a specific cellular target of necrostatins. Nat Chem Biol 4:313–321
Degterev A, Maki JL, Yuan J (2013) Activity and specificity of necrostatin-1, small molecule inhibitor of RIP1 kinase. Cell Death Differ 20:366
Degterev A, Zhou W, Maki JL, Yuan J (2014) Assays for necroptosis and activity of RIP kinases. Methods Enzymol 545:1–33
Delehouzé C, Leverrier-Penna S, Le Cann F, Comte A, Jacquard-Fevai M, Delalande O, Desban N, Baratte B, Gallais I, Faurez F, Bonnet MC, Hauteville M, Goekjian PG, Thuillier R, Favreau F, Vandenabeele P, Hauet T, Dimanche-Boitrel MT, Bach S (2017) 6E11, a highly selective inhibitor of Receptor-Interacting Protein Kinase 1, protects cells against cold hypoxia-reoxygenation injury. Sci Rep 7:12931
Do YJ, Sul JW, Jang KH, Kang NS, Kim YH, Kim YG, Kim E (2017) A novel RIPK1 inhibitor that prevents retinal degeneration in a rat glaucoma model. Exp Cell Res 359:30–38
Dolga AM, Netter MF, Perocchi F, Doti N, Meissner L, Tobaben S, Grohm J, Zischka H, Plesnila N, Decher N, Culmsee C (2013) Mitochondrial small conductance SK2 channels prevent glutamate-induced oxytosis and mitochondrial dysfunction. J Biol Chem 288:10792–10804
Dong K, Zhu H, Song Z, Gong Y, Wang F, Wang W, Zheng Z, Yu Z, Gu Q, Xu X, Sun X (2012) Necrostatin-1 protects photoreceptors from cell death and improves functional outcome after experimental retinal detachment. Am J Pathol 181:1634–1641
Espinosa-Oliva AM, García-Revilla J, Alonso-Bellido IM, Burguillos MA (2019) Brainiac caspases: beyond the wall of apoptosis. Front Cell Neurosci 13:500
Follo C, Castino R, Nicotra G, Trincheri NF, Isidoro C (2007) Folding, activity and targeting of mutated human cathepsin D that cannot be processed into the double-chain form. Int J Biochem Cell Biol 39:638–649
Fraczek-Szczypta A, Jantas D, Ciepiela F, Grzonka J, Bernasik A, Marzec M (2018) Carbon nanomaterials coatings – properties and influence on nerve cells response. Diam Relat Mater 84:127–140
Funakoshi T, Aki T, Tajiri M, Unuma K, Uemura K (2016) Necroptosis-like neuronal cell death caused by cellular cholesterol accumulation. J Biol Chem 291:25050–25065
Ito K, Eguchi Y, Imagawa Y, Akai S, Mochizuki H, Tsujimoto Y (2017) MPP+ induces necrostatin-1- and ferrostatin-1-sensitive necrotic death of neuronal SH-SY5Y cells. Cell Death Discov 3:17013
Jantas D, Krawczyk S, Lason W (2014a) The predominant protective effect of tianeptine over other antidepressants in models of neuronal apoptosis: the effect blocked by inhibitors of MAPK/ERK1/2 and PI3-K/Akt pathways. Neurotox Res 25:208–225
Jantas D, Greda A, Golda S, Korostynski M, Grygier B, Roman A, Pilc A, Lason W (2014b) Neuroprotective effects of metabotropic glutamate receptor group II and III activators against MPP(+)-induced cell death in human neuroblastoma SH-SY5Y cells: the impact of cell differentiation state. Neuropharmacology 83:36–53
Jantas D, Piotrowski M, Lason W (2015a) An involvement of PI3-K/Akt activation and inhibition of AIF translocation in neuroprotective effects of undecylenic acid (UDA) against pro-apoptotic factors-induced cell death in human neuroblastoma SH-SY5Y cells. J Cell Biochem 116:2882–2895
Jantas D, Greda A, Leskiewicz M, Grygier B, Pilc A, Lason W (2015b) Neuroprotective effects of mGluR II and III activators against staurosporine- and doxorubicin-induced cellular injury in SH-SY5Y cells: new evidence for a mechanism involving inhibition of AIF translocation. Neurochem Int 88:124–137
Jantas D, Grygier B, Gołda S, Chwastek J, Zatorska J, Tertil M (2018a) An endogenous and ectopic expression of metabotropic glutamate receptor 8 (mGluR8) inhibits proliferation and increases chemosensitivity of human neuroblastoma and glioma cells. Cancer Lett 432:1–16
Jantas D, Grygier B, Zatorska J, Lasoń W (2018b) Allosteric and orthosteric activators of mglur8 differentially affect the chemotherapeutic-induced human neuroblastoma SH-SY5Y cell damage: the impact of cell differentiation state. Basic Clin Pharmacol Toxicol 123:443–451
Ji D, Kamalden TA, del Olmo-Aguado S, Osborne NN (2011) Light- and sodium azide-induced death of RGC-5 cells in culture occurs via different mechanisms. Apoptosis 16:425–437
Kanamori S, Waguri S, Shibata M, Isahara K, Ohsawa Y, Konishi A, Kametaka S, Watanabe T, Ebisu S, Kominami E, Uchiyama Y (1998) Overexpression of cation-dependent mannose 6-phosphate receptor prevents cell death induced by serum deprivation in PC12 cells. Biochem Biophys Res Commun 251:204–208
Kim S, Dayani L, Rosenberg PA, Li J (2010) RIP1 kinase mediates arachidonic acid-induced oxidative death of oligodendrocyte precursors. Int J Physiol Pathophysiol Pharmacol 2:137–147
Knaryan VH, Samantaray S, Park S, Azuma M, Inoue J, Banik NL (2014) SNJ-1945, a calpain inhibitor, protects SH-SY5Y cells against MPP(+) and rotenone. J Neurochem 130:280–290
Koshinuma S, Miyamae M, Kaneda K, Kotani J, Figueredo VM (2014) Combination of necroptosis and apoptosis inhibition enhances cardioprotection against myocardial ischemia-reperfusion injury. J Anesth 28:235–241
Lee DC, Mason CW, Goodman CB, Holder MS, Kirksey OW, Womble TA, Severs WB, Palm DE (2007) Hydrogen peroxide induces lysosomal protease alterations in PC12 cells. Neurochem Res 32:1499–1510
Lee HO, Byun YJ, Cho KO, Kim SY, Lee SB, Kim HS, Kwon OJ, Jeong SW (2011) GS28 protects neuronal cell death induced by hydrogen peroxide under glutathione-depleted condition. Korean J Physiol Pharmacol 15:149–156
Lee JS, Lipatov A, Ha L, Shekhirev M, Andalib MN, Sinitskii A, Lim JY (2015) Graphene substrate for inducing neurite outgrowth. Biochem Biophys Res Commun 460:267–273
Li N, He Y, Wang L, Mo C, Zhang J, Zhang W, Li J, Liao Z, Tang X, Xiao H (2011) D-galactose induces necroptotic cell death in neuroblastoma cell lines. J Cell Biochem 112:3834–3844
Li W, Liu J, Chen JR, Zhu YM, Gao X, Ni Y, Lin B, Li H, Qiao SG, Wang C, Zhang HL, Ao GZ (2018) Neuroprotective effects of DTIO, a novel analogue of Nec-1, in acute and chronic stages after ischemic stroke. 390:12–29
Liu Q, Qiu J, Liang M, Golinski J, van Leyen K, Jung JE, You Z, Lo EH, Degterev A, Whalen MJ (2014) Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis 5:e1084
Lopes FM, Schroder R, da Frota ML Jr, Zanotto-Filho A, Muller CB, Pires AS, Meurer RT, Colpo GD, Gelain DP, Kapczinski F, Moreira JC, Fernandes MC, Klamt F (2010) Comparison between proliferative and neuron-like SH-SY5Y cells as an in vitro model for Parkinson disease studies. Brain Res 1337:85–94
Mhillaj E, Tarozzi A, Pruccoli L, Cuomo V, Trabace L, Mancuso C (2019) Curcumin and heme oxygenase: neuroprotection and beyond. Int J Mol Sci 20:E2419
Miloso M, Villa D, Crimi M, Galbiati S, Donzelli E, Nicolini G, Tredici G (2004) Retinoic acid-induced neuritogenesis of human neuroblastoma SH-SY5Y cells is ERK independent and PKC dependent. J Neurosci Res 75:241–252
Nath R, Raser KJ, McGinnis K, Nadimpalli R, Stafford D, Wang KK (1996) Effects of ICE-like protease and calpain inhibitors on neuronal apoptosis. Neuroreport 8:249–255
Ni Y, Gu WW, Liu ZH, Zhu YM, Rong JG, Kent TA, Li M, Qiao SG, An JZ, Zhang HL (2018) RIP1K contributes to neuronal and astrocytic cell death in ischemic stroke via activating autophagic-lysosomal pathway. 371:60–74
Nicotra G, Castino R, Follo C, Peracchio C, Valente G, Isidoro C (2010) The dilemma: does tissue expression of cathepsin D reflect tumor malignancy? The question: does the assay truly mirror cathepsin D mis-function in the tumor? Cancer Biomark 7:47–64
No H, Bang Y, Lim J, Kim SS, Choi HS, Choi HJ (2010) Involvement of induction and mitochondrial targeting of orphan nuclear receptor Nur77 in 6-OHDA-induced SH-SY5Y cell death. Neurochem Int 56:620–626
Northington FJ, Chavez-Valdez R, Graham EM, Razdan S, Gauda EB, Martin LJ (2011) Necrostatin decreases oxidative damage, inflammation, and injury after neonatal HI. J Cereb Blood Flow Metab 31:178–189
Park SY, Kim DY, Kang JK, Park G, Choi YW (2014) Involvement of activation of the Nrf2/ARE pathway in protection against 6-OHDA-induced SH-SY5Y cell death by α-iso-cubebenol. Neurotoxicology 44:160–168
Park JH, Kim CK, Lee SB, Lee KH, Cho SW, Ahn JY (2016) Akt attenuates apoptotic death through phosphorylation of H2A under hydrogen peroxide-induced oxidative stress in PC12 cells and hippocampal neurons. Sci Rep 6:21857
Polito L, Bortolotti M, Pedrazzi M, Mercatelli D, Battelli MG, Bolognesi A (2016) Apoptosis and necroptosis induced by stenodactylin in neuroblastoma cells can be completely prevented through caspase inhibition plus catalase or necrostatin-1. Phytomedicine 23:32–41
Qinli Z, Meiqing L, Xia J, Li X, Weili G, Xiuliang J, Junwei J, Hailan Y, Ce Z, Qiao N (2013) Necrostatin-1 inhibits the degeneration of neural cells induced by aluminum exposure. Restor Neurol Neurosci 31:543–555
Re DB, Le Verche V, Yu C, Amoroso MW, Politi KA, Phani S, Ikiz B, Hoffmann L, Koolen M, Nagata T, Papadimitriou D, Nagy P, Mitsumoto H, Kariya S, Wichterle H, Henderson CE, Przedborski S (2014) Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron 81:1001–1008
Rosenbaum DM, Degterev A, David J, Rosenbaum PS, Roth S, Grotta JC, Cuny GD, Yuan J, Savitz SI (2010) Necroptosis, a novel form of caspase-independent cell death, contributes to neuronal damage in a retinal ischemia-reperfusion injury model. J Neurosci Res 88:1569–1576
Sang Q, Sun D, Chen Z, Zhao W (2018) NGF and PI3K/Akt signaling participate in the ventral motor neuronal protection of curcumin in sciatic nerve injury rat models. Biomed Pharmacother 103:1146–1153
Szczepanowicz K, Jantas D, Piotrowski M, Staroń J, Leśkiewicz M, Regulska M, Lasoń W, Warszyński P (2016) Encapsulation of curcumin in polyelectrolyte nanocapsules and their neuroprotective activity. Nanotechnology 27:355101
Tieu K, Zuo DM, Yu PH (1999) Differential effects of staurosporine and retinoic acid on the vulnerability of the SH-SY5Y neuroblastoma cells: involvement of bcl-2 and p53 proteins. J Neurosci Res 58:426–435
Uğuz AC, Öz A, Nazıroğlu M (2016) Curcumin inhibits apoptosis by regulating intracellular calcium release, reactive oxygen species and mitochondrial depolarization levels in SH-SY5Y neuronal cells. J Recept Signal Transduct Res 36:395–401
Vieira M, Fernandes J, Carreto L, Anuncibay-Soto B, Santos M, Han J, Fernández-López A, Duarte CB, Carvalho AL, Santos AE (2014) Ischemic insults induce necroptotic cell death in hippocampal neurons through the up-regulation of endogenous RIP3. Neurobiol Dis 68:26–36
Wang Y, Wang H, Tao Y, Zhang S, Wang J, Feng X (2014) Necroptosis inhibitor necrostatin-1 promotes cell protection and physiological function in traumatic spinal cord injury. Neuroscience 266:91–101
Wang W, Wang WH, Azadzoi KM, Su N, Dai P, Sun J, Wang Q, Liang P, Zhang W, Lei X, Yan Z, Yang JH (2016) Activation of innate antiviral immune response via double-stranded RNA-dependent RLR receptor-mediated necroptosis. Sci Rep 6:22550
Wang J, Liu Y, Li XH, Zeng XC, Li J, Zhou J, Xiao B, Hu K (2017) Curcumin protects neuronal cells against status-epilepticus-induced hippocampal damage through induction of autophagy and inhibition of necroptosis. Can J Physiol Pharmacol 95:501–509
Wang S, Yuan YH, Chen NH, Wang HB (2019) The mechanisms of NLRP3 inflammasome/pyroptosis activation and their role in Parkinson’s disease. Int Immunopharmacol 67:458–464
Wenker SD, Chamorro ME, Vota DM, Callero MA, Vittori DC, Nesse AB (2010) Differential antiapoptotic effect of erythropoietin on undifferentiated and retinoic acid-differentiated SH-SY5Y cells. J Cell Biochem 110:151–161
Wu JR, Wang J, Zhou SK, Yang L, Yin JL, Cao JP, Cheng YB (2015) Necrostatin-1 protection of dopaminergic neurons. Neural Regen Res 10:1120–1124
Xie T, Peng W, Yan C, Wu J, Gong X, Shi Y (2013) Structural insights into RIP3-mediated necroptotic signaling. Cell Rep 5:70–78
Xiong K, Liao H, Long L, Ding Y, Huang J, Yan J (2016) Necroptosis contributes to methamphetamine-induced cytotoxicity in rat cortical neurons. Toxicol in Vitro 35:163–168
Xu X, Chua CC, Kong J, Kostrzewa RM, Kumaraguru U, Hamdy RC, Chua BH (2007) Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells. J Neurochem 103(5):2004–2014
Xu X, Chua KW, Chua CC, Liu CF, Hamdy RC, Chua BH (2010a) Synergistic protective effects of humanin and necrostatin-1 on hypoxia and ischemia/reperfusion injury. Brain Res 1355:189–194
Xu X, Chua CC, Zhang M, Geng D, Liu CF, Hamdy RC, Chua BH (2010b) The role of PARP activation in glutamate-induced necroptosis in HT-22 cells. Brain Res 1343:206–212
Xu Y, Wang J, Song X, Qu L, Wei R, He F, Wang K, Luo B (2016) RIP3 induces ischemic neuronal DNA degradation and programmed necrosis in rat via AIF. Sci Rep 6:29362
Xu L, Ding L, Su Y, Shao R, Liu J, Huang Y (2019) Neuroprotective effects of curcumin against rats with focal cerebral ischemia-reperfusion injury. Int J Mol Med 43:1879–1887
Yamanaka K, Saito Y, Yamamori T, Urano Y, Noguchi N (2011) 24(S)-hydroxycholesterol induces neuronal cell death through necroptosis, a form of programmed necrosis. J Biol Chem 286:24666–24673
Yang R, Hu K, Chen J, Zhu S, Li L, Lu H, Li P, Dong R (2017a) Necrostatin-1 protects hippocampal neurons against ischemia/reperfusion injury via the RIP3/DAXX signaling pathway in rats. Neurosci Lett 651:207–215
Yang SH, Lee DK, Shin J, Lee S, Baek S, Kim J, Jung H, Hah JM, Kim Y (2017b) Nec-1 alleviates cognitive impairment with reduction of Aβ and tau abnormalities in APP/PS1 mice. EMBO Mol Med 9:61–77
Yang SH, Shin J, Shin NN, Hwang JH, Hong SC, Park K, Lee JW, Lee S, Baek S, Kim K, Cho I, Kim Y (2019) A small molecule Nec-1 directly induces amyloid clearance in the brains of aged APP/PS1 mice. Sci Rep 9:4183
Yin B, Xu Y, Wei RL, He F, Luo BY, Wang JY (2015) Inhibition of receptor-interacting protein 3 upregulation and nuclear translocation involved in necrostatin-1 protection against hippocampal neuronal programmed necrosis induced by ischemia/reperfusion injury. Brain Res 1609:63–71
Zhan L, Lu Z, Zhu X, Xu W, Li L, Li X, Chen S, Sun W, Xu E (2019) Hypoxic preconditioning attenuates necroptotic neuronal death induced by global cerebral ischemia via Drp1-dependent signaling pathway mediated by CaMKIIα inactivation in adult rats. FASEB J 33:1313–1329
Zhang QL, Niu Q, Ji XL, Conti P, Boscolo P (2008) Is necroptosis a death pathway in aluminum-induced neuroblastoma cell demise? Int J Immunopathol Pharmacol 21:787–796
Zhang M, Li J, Geng R, Ge W, Zhou Y, Zhang C, Cheng Y, Geng D (2013) The inhibition of ERK activation mediates the protection of necrostatin-1 on glutamate toxicity in HT-22 cells. Neurotox Res 24:64–70
Zhang S, Wang Y, Li D, Wu J, Si W, Wu Y (2016) Necrostatin-1 attenuates inflammatory response and improves cognitive function in chronic ischemic stroke mice. Medicines (Basel) 3:E16
Zhao H, Jaffer T, Eguchi S, Wang Z, Linkermann A, Ma D (2015) Role of necroptosis in the pathogenesis of solid organ injury. Cell Death Dis 6:e1975
Zhao MW, Yang P, Zhao LL (2019a) Chlorpyrifos activates cell pyroptosis and increases susceptibility on oxidative stress-induced toxicity by miR-181/SIRT1/PGC-1α/Nrf2 signaling pathway in human neuroblastoma SH-SY5Y cells: Implication for association between chlorpyrifos and Parkinson’s disease. Environ Toxicol 34:699–707