Neuroprotective effect of topiramate against 6-hydroxydopamine-induced cell death in Parkinson’s disease cell mode

authors:

avatar Fahimeh Fallah , avatar Azadeh Aminzadeh , *


how to cite: Fallah F, Aminzadeh A. Neuroprotective effect of topiramate against 6-hydroxydopamine-induced cell death in Parkinson’s disease cell mode. koomesh. 2019;21(4):e153135. 

Abstract

Introduction: Parkinson;#39s disease (PD) is a common neurodegenerative disorder characterized by progressive neuronal dysfunction. Growing evidence has shown that oxidative stress plays a crucial role in the pathogenesis of Parkinson;#39s disease. Correspondingly, the current study evaluated the protective effect of topiramate in 6-hydroxydopamine induced oxidative stress and apoptosis in PC12 cells as an in vitro model for PD. Materials and Methods: PC12 cells, a cellular model of PD, were treated with topiramate for 24 h. Then they were treated with 75 μM 6-hydroxydopamine for 24 h. Cell viability was examined by 3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2-tetrazolium bromide (MTT) assay. Intracellular reactive oxygen species (ROS) levels were measured using 2, 7 dichlorodihydrofluorescein diacetate (DCF-DA) assay. The levels of lipid peroxidation and total antioxidant power (TAP) were also measured. Results: Remarkably, topiramate at concentration of 8 μM increased survival of PC12 cells exposed to 6-hydroxydopamine. Cell viability of PC12 cells on 6-hydroxydopamine was decreased compared to controls, which was reversed by topiramate. Topiramate also reduced intracellular reactive oxygen species (ROS) level and cellular lipid peroxidation. In addition, topiramate significantly increased total antioxidant power in 6-OHDA-treated cells. Conclusion: Findings of this study showed that the topiramate protects PC12 cells against 6-OHDA-induced neurotoxicity through its potent antioxidant activity

References

  • 1.

    Dexter DT, Jenner P. Parkinson disease: from pathology to molecular disease mechanisms. Free Radic Biol Med 2013; 62: 132-144.

  • 2.

    Taylor JM, Main BS, Crack PJ. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinsons disease. Neurochem Int 2013; 62: 803-819.

  • 3.

    Bov J, Prou D, Perier C, Przedborski S. Toxin-induced models of Parkinson's disease. Neuro Rx 2005; 2: 484-494.

  • 4.

    Ryu EJ, Angelastro JM, Greene LA. Analysis of gene expression changes in a cellular model of Parkinson disease. Neurobiol Dis 2005; 18: 54-74.

  • 5.

    RodriguezPallares J, Parga J, Munoz A, Rey P, Guerra M, LabandeiraGarcia J. Mechanism of 6hydroxydopamine neurotoxicity: the role of NADPH oxidase and microglial activation in 6hydroxydopamineinduced degeneration of dopaminergic neurons. J Neurochem 2007; 103: 145-156.

  • 6.

    Tang SY, Whiteman M, Peng ZF, Jenner A, Yong EL, Halliwell B. Characterization of antioxidant and antiglycation properties and isolation of active ingredients from traditional Chinese medicines. Free Radic Biol Med 2004; 36: 1575-1587.

  • 7.

    Paradies G, Petrosillo G, Paradies V, Ruggiero FM. Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int 2011; 58: 447-457.

  • 8.

    Simola N, Morelli M, Carta AR. The 6-hydroxydopamine model of Parkinsons disease. Neurotox Res 2007; 11: 151-167.

  • 9.

    Liu Y, Barks JD, Xu G, Silverstein FS. Topiramate extends the therapeutic window for hypothermia-mediated neuroprotection after stroke in neonatal rats. Stroke 2004; 35: 1460-1465.

  • 10.

    Edmonds HL Jr, Jiang YD, Zhang PY, Shank R. Topiramate as a neuroprotectant in a rat model of global ischemia-induced neurodegeneration. Life Sci 2001; 69: 2265-2277.

  • 11.

    Lee SR, Kim SP, Kim JE. Protective effect of topiramate against hippocampal neuronal damage after global ischemia the gerbils. Neurosci Lett 2000; 281: 183-186.

  • 12.

    Angehagen M, Ben-Menachem E, Rnnbck L, Hansson E. Topiramate protects against glutamate- and kainate-induced neurotoxicity in primary neuronalastroglial cultures. Epilepsy Res 2003; 54: 63-71.

  • 13.

    Kurul S, Yi U, Kumral A, Tuyan K, Cilaker S, Kolatan E, et al. Protective effects of topiramate against hyperoxic brain injury in the developing brain. Neuropediatrics 2009; 40: 22-27.

  • 14.

    Price TO, Eranki V, Banks WA, Ercal N, Shah GN. Topiramate treatment protects blood-brain barrier pericytes from hyperglycemia-induced oxidative damage in diabetic mice. Endocrinology 2012; 153: 362-372.

  • 15.

    Shah GN, Price TO, Banks WA, Morofuji Y, Kovac A, Ercal N, et al. Pharmacological inhibition of mitochondrial carbonic anhydrases protects mouse cerebral pericytes from high glucose-induced oxidative stress and apoptosis. J Pharmacol Exp Ther 2013; 344: 637-645.

  • 16.

    Price TO, Farr SA, Niehoff ML, Ercal N, Morley JE, Shah GN. Protective effect of topiramate on hyperglycemia-induced cerebral oxidative stress, pericyte loss and learning behavior in diabetic mice. Int Libr Diabetes Metab 2015; 1: 6-12.

  • 17.

    Tian Y, Guo SX, Li JR, Du HG, Wang CH, Zhang JM, et al. Topiramate attenuates early brain injury following subarachnoid haemorrhage in rats via duplex protection against inflammation and neuronal cell death. Brain Res 2015; 1622: 174-185.

  • 18.

    Feng L, Meng H, Wu F, Cheng B, He X, Wang X, et al. Olfactory ensheathing cells conditioned medium prevented apoptosis induced by 6-OHDA in PC12 cells through modulation of intrinsic apoptotic pathways. Int J Dev Neurosci 2008; 26: 323-329.

  • 19.

    Walkinshaw G, Waters C. Neurotoxin-induced cell death in neuronal PC12 cells is mediated by induction of apoptosis. Neuroscience 1994; 63: 975-987.

  • 20.

    Saito Y, Nishio K, Ogawa Y, Kinumi T, Yoshida Y, Masuo Y, et al. Molecular mechanisms of 6-hydroxydopamine-induced cytotoxicity in PC12 cells: involvement of hydrogen peroxide-dependent and-independent action. Free Radic Biol Med 2007; 42: 675-685.

  • 21.

    Tamadoni M, Haji ghasem kashani M, Ghorbanian M, Abrari K, Arashpour R. Neuroprotective effects of carnosic acid on the hippocampus of 6-hydroxydopamine injured rats. Koomesh 2014; 15: 232-241. (Persian).

  • 22.

    Safari M, Badban L, Sameni H, Bandegi A, Rashidypour A, Vafaei A. Comparison the protective effects of aqueous extract of Iranian propolis in 6-hydroxydopamine-induced model of parkinsonism in male rat with L-DOPA: A behavioral and histological evaluation. Koomesh 2014; 15: 584-591. (Persian).

  • 23.

    Fujita H, Ogino T, Kobuchi H, Fujiwara T, Yano H, Akiyama J, et al. Cell-permeable cAMP analog suppresses 6-hydroxydopamine-induced apoptosis in PC12 cells through the activation of the Akt pathway. Brain Res 2006; 1113: 10-23.

  • 24.

    Padiglia A, Medda R, Lorrai A, Biggio G, Sanna E, Floris G. Modulation of 6-hydroxydopamine oxidation by various proteins. Biochem Pharmacol 1997; 53: 1065-1068.

  • 25.

    Yamada K, Umegaki H, Maezawa I, Iguchi A, Kameyama T, Nabeshima T. Possible involvement of catalase in the protective effect of interleukin-6 against 6-hydroxydopamine toxicity in PC12 cells. Brain Res Bull 1997; 43: 573-577.

  • 26.

    Nie G, Jin C, Cao Y, Shen S, Zhao B. Distinct effects of tea catechins on 6-hydroxydopamine-induced apoptosis in PC12 cells. Arch Biochem Biophys 2002; 397: 84-90.

  • 27.

    Aminzadeh A, Mehrzadi S. Melatonin attenuates homocysteineinduced injury in human umbilical vein endothelial cells. Fundam Clin Pharmacol 2018; 32: 261-269.

  • 28.

    Aminzadeh A, Mehrzadi S. Cardioprotective effect of levosimendan against homocysteine-induced mitochondrial stress and apoptotic cell death in H9C2. Biochem Biophys Res Commun 2018; 507: 395-399.

  • 29.

    Tian LL, Wang XJ, Sun YN, Li CR, Xing YL, Zhao HB, et al. Salvianolic acid B, an antioxidant from Salvia miltiorrhiza, prevents 6-hydroxydopamine induced apoptosis in SH-SY5Y cells. Int J Biochem Cell Biol 2008; 40: 409-422.

  • 30.

    Mao XY, Cao YG, Ji Z, Zhou HH, Liu ZQ, Sun HL. Topiramate protects against glutamate excitotoxicity via activating BDNF/TrkB-dependent ERK pathway in rodent hippocampal neurons. Prog Neuro-Psychopharmacol Biol Psychiatry 2015; 60: 11-17.

  • 31.

    Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007; 39: 44-84.

  • 32.

    Aminzadeh A, Salarinejad A. Citicoline protects against lead-induced oxidative injury in neuronal PC12 cells. Biochem Cell Biol. 2019.

  • 33.

    Nazirolu M, Kutluhan S, Yilmaz M. Selenium and topiramate modulates brain microsomal oxidative stress values, Ca2+-ATPase activity, and EEG records in pentylentetrazol-induced seizures in rats. J Membr Biol 2008; 225: 39-49.

  • 34.

    Kurt A, Kalkan Y, Turut H, Cure MC, Tumkaya L, Cure E. Topiramate reduces aortic cross clamping-induced lung injury in male rats. Acta Medica (Hradec Kralove) 2018; 61: 144-149.

  • 35.

    Motaghinejad M, Motevalian M, Fatima S, Beiranvand T, Mozaffari S. Topiramate via NMDA, AMPA/kainate, GABAA and Alpha2 receptors and by modulation of CREB/BDNF and Akt/GSK3 signaling pathway exerts neuroprotective effects against methylphenidate-induced neurotoxicity in rats. J Neural Transm 2017; 9: 1-19.

  • 36.

    Motaghinejad M, Motevalian M, Babalouei F, Abdollahi M, Heidari M, Madjd Z. Possible involvement of CREB/BDNF signaling pathway in neuroprotective effects of topiramate against methylphenidate induced apoptosis, oxidative stress and inflammation in isolated hippocampus of rats: molecular, biochemical and histological evidences. Brain Res Bull 2017; 132: 82-98.##.