Curcumin Protects an SH-SY5Y Cell Model of Parkinson’s Disease Against Toxic Injury by Regulating HSP90

Background/Aims: We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson’s disease (PD) and its underlying mechanism. Methods: In this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected...

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Vydané v:	Cellular physiology and biochemistry Ročník 51; číslo 2; s. 681 - 691
Hlavní autori:	Sang, Qiuling, Liu, Xiaoyang, Wang, Libo, Qi, Ling, Sun, Wenping, Wang, Weiyao, Sun, Yajuan , Zhang, Haina
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	Basel, Switzerland S. Karger AG 01.01.2018 Cell Physiol Biochem Press GmbH & Co KG
Predmet:	1-Methyl-4-phenylpyridinium - toxicity Apoptosis Apoptosis - drug effects bcl-2-Associated X Protein - metabolism bcl-X Protein - metabolism Cell Line, Tumor Cell Proliferation - drug effects Curcumin Curcumin - pharmacology Dopamine - analysis Dopamine Plasma Membrane Transport Proteins - metabolism Dopaminergic neurons Gene Regulatory Networks Heat shock proteins HSP90 HSP90 Heat-Shock Proteins - antagonists & inhibitors HSP90 Heat-Shock Proteins - genetics HSP90 Heat-Shock Proteins - metabolism Humans Kinases Models, Biological Morphology MPP Neurodegeneration Original Paper Parkinson Parkinson Disease - metabolism Parkinson Disease - pathology Parkinson's disease RNA Interference RNA, Small Interfering - metabolism SH-SY5Y China Dopaminergic neurons HSP90 SH-SY5Y Curcumin MPP Parkinson
ISSN:	1015-8987, 1421-9778, 1421-9778
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Abstract	Background/Aims: We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson’s disease (PD) and its underlying mechanism. Methods: In this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected genes was downloaded from STITCH, with the interactions analyzed by STRING. We built a mitochondrial toxin 1-methyl-4-phenylpyridinium (MPP + )-induced SH-SY5Y cell model of PD. Cell morphology was observed under an electron microscope. MTT assay was applied to detect cell proliferation rate. Western blot assay was conducted to determine the level of apoptotic markers, including cleaved caspase 3, Bcl-2-associated X protein (Bax) and B-cell lymphoma-extra-large (Bcl-xl). Tyrosine hydroxylase (TH), dopamine transporter (DAT) protein levels and dopamine (DA) concentration were identified as dopaminergic neuron markers and measured by western blotting or Enzyme-linked immunosorbent assay (ELISA). Results: Cur rescued the toxicity effects of MPP + on SH-SY5Y cells, by controlling morphological change, promoting cell proliferation and inhibiting apoptosis. Of all PD-related genes, HSP90 played an important role in Cur-gene network. HSP90 protein level was elevated by MPP + , whereas Cur could reverse this effect. Silencing of HSP90 significantly attenuated the curative effect introduced by Cur, while HSP90 overexpression enhanced the impact of Cur on PD. Conclusion: Cur can effectively inhibit the toxic effect of MPP + on SH-SY5Y cells and significantly reduce the adverse effects of MPP + on dopaminergic neurons via up-regulation of HSP90.
AbstractList	Background/Aims: We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson’s disease (PD) and its underlying mechanism. Methods: In this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected genes was downloaded from STITCH, with the interactions analyzed by STRING. We built a mitochondrial toxin 1-methyl-4-phenylpyridinium (MPP+)-induced SH-SY5Y cell model of PD. Cell morphology was observed under an electron microscope. MTT assay was applied to detect cell proliferation rate. Western blot assay was conducted to determine the level of apoptotic markers, including cleaved caspase 3, Bcl-2-associated X protein (Bax) and B-cell lymphoma-extra-large (Bcl-xl). Tyrosine hydroxylase (TH), dopamine transporter (DAT) protein levels and dopamine (DA) concentration were identified as dopaminergic neuron markers and measured by western blotting or Enzyme-linked immunosorbent assay (ELISA). Results: Cur rescued the toxicity effects of MPP+ on SH-SY5Y cells, by controlling morphological change, promoting cell proliferation and inhibiting apoptosis. Of all PD-related genes, HSP90 played an important role in Cur-gene network. HSP90 protein level was elevated by MPP+, whereas Cur could reverse this effect. Silencing of HSP90 significantly attenuated the curative effect introduced by Cur, while HSP90 overexpression enhanced the impact of Cur on PD. Conclusion: Cur can effectively inhibit the toxic effect of MPP+ on SH-SY5Y cells and significantly reduce the adverse effects of MPP+ on dopaminergic neurons via up-regulation of HSP90. We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson's disease (PD) and its underlying mechanism. In this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected genes was downloaded from STITCH, with the interactions analyzed by STRING. We built a mitochondrial toxin 1-methyl-4-phenylpyridinium (MPP+)-induced SH-SY5Y cell model of PD. Cell morphology was observed under an electron microscope. MTT assay was applied to detect cell proliferation rate. Western blot assay was conducted to determine the level of apoptotic markers, including cleaved caspase 3, Bcl-2-associated X protein (Bax) and B-cell lymphoma-extra-large (Bcl-xl). Tyrosine hydroxylase (TH), dopamine transporter (DAT) protein levels and dopamine (DA) concentration were identified as dopaminergic neuron markers and measured by western blotting or Enzyme-linked immunosorbent assay (ELISA). Cur rescued the toxicity effects of MPP+ on SH-SY5Y cells, by controlling morphological change, promoting cell proliferation and inhibiting apoptosis. Of all PD-related genes, HSP90 played an important role in Cur-gene network. HSP90 protein level was elevated by MPP+, whereas Cur could reverse this effect. Silencing of HSP90 significantly attenuated the curative effect introduced by Cur, while HSP90 overexpression enhanced the impact of Cur on PD. Cur can effectively inhibit the toxic effect of MPP+ on SH-SY5Y cells and significantly reduce the adverse effects of MPP+ on dopaminergic neurons via up-regulation of HSP90. We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson's disease (PD) and its underlying mechanism.BACKGROUND/AIMSWe aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson's disease (PD) and its underlying mechanism.In this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected genes was downloaded from STITCH, with the interactions analyzed by STRING. We built a mitochondrial toxin 1-methyl-4-phenylpyridinium (MPP+)-induced SH-SY5Y cell model of PD. Cell morphology was observed under an electron microscope. MTT assay was applied to detect cell proliferation rate. Western blot assay was conducted to determine the level of apoptotic markers, including cleaved caspase 3, Bcl-2-associated X protein (Bax) and B-cell lymphoma-extra-large (Bcl-xl). Tyrosine hydroxylase (TH), dopamine transporter (DAT) protein levels and dopamine (DA) concentration were identified as dopaminergic neuron markers and measured by western blotting or Enzyme-linked immunosorbent assay (ELISA).METHODSIn this study, genes concerned with PD-related keywords were screened within DiGSeE database. The association network between Cur and selected genes was downloaded from STITCH, with the interactions analyzed by STRING. We built a mitochondrial toxin 1-methyl-4-phenylpyridinium (MPP+)-induced SH-SY5Y cell model of PD. Cell morphology was observed under an electron microscope. MTT assay was applied to detect cell proliferation rate. Western blot assay was conducted to determine the level of apoptotic markers, including cleaved caspase 3, Bcl-2-associated X protein (Bax) and B-cell lymphoma-extra-large (Bcl-xl). Tyrosine hydroxylase (TH), dopamine transporter (DAT) protein levels and dopamine (DA) concentration were identified as dopaminergic neuron markers and measured by western blotting or Enzyme-linked immunosorbent assay (ELISA).Cur rescued the toxicity effects of MPP+ on SH-SY5Y cells, by controlling morphological change, promoting cell proliferation and inhibiting apoptosis. Of all PD-related genes, HSP90 played an important role in Cur-gene network. HSP90 protein level was elevated by MPP+, whereas Cur could reverse this effect. Silencing of HSP90 significantly attenuated the curative effect introduced by Cur, while HSP90 overexpression enhanced the impact of Cur on PD.RESULTSCur rescued the toxicity effects of MPP+ on SH-SY5Y cells, by controlling morphological change, promoting cell proliferation and inhibiting apoptosis. Of all PD-related genes, HSP90 played an important role in Cur-gene network. HSP90 protein level was elevated by MPP+, whereas Cur could reverse this effect. Silencing of HSP90 significantly attenuated the curative effect introduced by Cur, while HSP90 overexpression enhanced the impact of Cur on PD.Cur can effectively inhibit the toxic effect of MPP+ on SH-SY5Y cells and significantly reduce the adverse effects of MPP+ on dopaminergic neurons via up-regulation of HSP90.CONCLUSIONCur can effectively inhibit the toxic effect of MPP+ on SH-SY5Y cells and significantly reduce the adverse effects of MPP+ on dopaminergic neurons via up-regulation of HSP90.
Author	Sun, Yajuan Zhang, Haina Wang, Libo Sang, Qiuling Liu, Xiaoyang Qi, Ling Wang, Weiyao Sun, Wenping
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Keywords	Dopaminergic neurons HSP90 SH-SY5Y Curcumin MPP Parkinson
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References	Yang J, Song S, Li J, Liang T: Neuroprotective effect of curcumin on hippocampal injury in 6-OHDA-induced Parkinson’s disease rat. Pathol Res Pract 2014; 210: 357-362. Falsone SF, Kungl AJ, Rek A, Cappai R, Zangger K: The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein alpha-synuclein. J Biol Chem 2009; 284: 31190-31199. Lackie RE, Maciejewski A, Ostapchenko VG, Marques-Lopes J, Choy WY, Duennwald ML, Prado VF, Prado MAM: The Hsp70/Hsp90 Chaperone Machinery in Neurodegenerative Diseases. Front Neurosci 2017; 11: 254. Liu Z, Yu Y, Li X, Ross CA, Smith WW: Curcumin protects against A53T alpha-synuclein-induced toxicity in a PC12 inducible cell model for Parkinsonism. Pharmacol Res 2011; 63: 439-444. Cao J, Wang T, Wang M: Investigation of the anti-cataractogenic mechanisms of curcumin through in vivo and in vitro studies. BMC Ophthalmol 2018; 18: 48. Schneider SA, Obeso JA: Clinical and pathological features of Parkinson’s disease. Curr Top Behav Neurosci 2015; 22: 205-220. Yu S, Wang X, He X, Wang Y, Gao S, Ren L, Shi Y: Curcumin exerts anti-inflammatory and antioxidative properties in 1-methyl-4-phenylpyridinium ion (MPP(+))-stimulated mesencephalic astrocytes by interference with TLR4 and downstream signaling pathway. Cell Stress Chaperones 2016; 21: 697-705. Daturpalli S, Waudby CA, Meehan S, Jackson SE: Hsp90 inhibits alpha-synuclein aggregation by interacting with soluble oligomers. J Mol Biol 2013; 425: 4614-4628. Singh PK, Kotia V, Ghosh D, Mohite GM, Kumar A, Maji SK: Curcumin modulates alpha-synuclein aggregation and toxicity. ACS Chem Neurosci 2013; 4: 393-407. Zhao C, Li H, Zhao XJ, Liu ZX, Zhou P, Liu Y, Feng MJ: Heat shock protein 60 affects behavioral improvement in a rat model of Parkinson’s disease grafted with human umbilical cord mesenchymal stem cell-derived dopaminergic-like neurons. Neurochem Res 2016; 41: 1238-1249. Aridon P, Geraci F, Turturici G, D’Amelio M, Savettieri G, Sconzo G: Protective role of heat shock proteins in Parkinson’s disease. Neurodegener Dis 2011; 8: 155-168. Cui Q, Li X, Zhu H: Curcumin ameliorates dopaminergic neuronal oxidative damage via activation of the Akt/Nrf2 pathway. Mol Med Rep 2016; 13: 1381-1388. Xie H, Hu H, Chang M, Huang D, Gu X, Xiong X, Xiong R, Hu L, Li G: Identification of chaperones in a MPP(+)-induced and ATRA/TPA-differentiated SH-SY5Y cell PD model. Am J Transl Res 2016; 8: 5659-5671. Yang D, Li T, Liu Z, Arbez N, Yan J, Moran TH, Ross CA, Smith WW: LRRK2 kinase activity mediates toxic interactions between genetic mutation and oxidative stress in a Drosophila model: suppression by curcumin. Neurobiol Dis 2012; 47: 385-392. Lee WH, Loo CY, Bebawy M, Luk F, Mason RS, Rohanizadeh R: Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21st century. Curr Neuropharmacol 2013; 11: 338-378. Alani B, Salehi R, Sadeghi P, Zare M, Khodagholi F, Arefian E, Hakemi MG, Digaleh H: Silencing of Hsp90 chaperone expression protects against 6-hydroxydopamine toxicity in PC12 cells. J Mol Neurosci 2014; 52: 392-402. Ojha RP, Rastogi M, Devi BP, Agrawal A, Dubey GP: Neuroprotective effect of curcuminoids against inflammation-mediated dopaminergic neurodegeneration in the MPTP model of Parkinson’s disease. J Neuroimmune Pharmacol 2012; 7: 609-618. Jiang TF, Zhang YJ, Zhou HY, Wang HM, Tian LP, Liu J, Ding JQ, Chen SD: Curcumin ameliorates the neurodegenerative pathology in A53T alpha-synuclein cell model of Parkinson’s disease through the downregulation of mTOR/p70S6K signaling and the recovery of macroautophagy. J Neuroimmune Pharmacol 2013; 8: 356-369. van der Merwe C, van Dyk HC, Engelbrecht L, van der Westhuizen FH, Kinnear C, Loos B, Bardien S: Curcumin Rescues a PINK1 Knock Down SH-SY5Y Cellular Model of Parkinson’s Disease from Mitochondrial Dysfunction and Cell Death. Mol Neurobiol 2017; 54: 2752-2762. Kalia SK, Kalia LV, McLean PJ: Molecular chaperones as rational drug targets for Parkinson’s disease therapeutics. CNS Neurol Disord Drug Targets 2010; 9: 741-753. Lv Y, Gong L, Wang Z, Han F, Liu H, Lu X, Liu L: Curcumin inhibits human cytomegalovirus by downregulating heat shock protein 90. Mol Med Rep 2015; 12: 4789-4793. Darvesh AS, Carroll RT, Bishayee A, Novotny NA, Geldenhuys WJ, Van der Schyf CJ: Curcumin and neurodegenerative diseases: a perspective. Expert Opin Investig Drugs 2012; 21: 1123-1140. Ahsan N, Mishra S, Jain MK, Surolia A, Gupta S: Curcumin Pyrazole and its derivative (N-(3-Nitrophenylpyrazole) Curcumin inhibit aggregation, disrupt fibrils and modulate toxicity of Wild type and Mutant alpha-Synuclein. Sci Rep 2015; 5: 9862. McFarland NR, Dimant H, Kibuuka L, Ebrahimi-Fakhari D, Desjardins CA, Danzer KM, Danzer M, Fan Z, Schwarzschild MA, Hirst W, McLean PJ: Chronic treatment with novel small molecule Hsp90 inhibitors rescues striatal dopamine levels but not alpha-synuclein-induced neuronal cell loss. PLoS One 2014; 9:e86048. Monti C, Bondi H, Urbani A, Fasano M, Alberio T: Systems biology analysis of the proteomic alterations induced by MPP(+), a Parkinson’s disease-related mitochondrial toxin. Front Cell Neurosci 2015; 9: 14.
References_xml	– reference: Alani B, Salehi R, Sadeghi P, Zare M, Khodagholi F, Arefian E, Hakemi MG, Digaleh H: Silencing of Hsp90 chaperone expression protects against 6-hydroxydopamine toxicity in PC12 cells. J Mol Neurosci 2014; 52: 392-402. – reference: Zhao C, Li H, Zhao XJ, Liu ZX, Zhou P, Liu Y, Feng MJ: Heat shock protein 60 affects behavioral improvement in a rat model of Parkinson’s disease grafted with human umbilical cord mesenchymal stem cell-derived dopaminergic-like neurons. Neurochem Res 2016; 41: 1238-1249. – reference: Jiang TF, Zhang YJ, Zhou HY, Wang HM, Tian LP, Liu J, Ding JQ, Chen SD: Curcumin ameliorates the neurodegenerative pathology in A53T alpha-synuclein cell model of Parkinson’s disease through the downregulation of mTOR/p70S6K signaling and the recovery of macroautophagy. J Neuroimmune Pharmacol 2013; 8: 356-369. – reference: Yang J, Song S, Li J, Liang T: Neuroprotective effect of curcumin on hippocampal injury in 6-OHDA-induced Parkinson’s disease rat. Pathol Res Pract 2014; 210: 357-362. – reference: Lackie RE, Maciejewski A, Ostapchenko VG, Marques-Lopes J, Choy WY, Duennwald ML, Prado VF, Prado MAM: The Hsp70/Hsp90 Chaperone Machinery in Neurodegenerative Diseases. Front Neurosci 2017; 11: 254. – reference: Falsone SF, Kungl AJ, Rek A, Cappai R, Zangger K: The molecular chaperone Hsp90 modulates intermediate steps of amyloid assembly of the Parkinson-related protein alpha-synuclein. J Biol Chem 2009; 284: 31190-31199. – reference: Darvesh AS, Carroll RT, Bishayee A, Novotny NA, Geldenhuys WJ, Van der Schyf CJ: Curcumin and neurodegenerative diseases: a perspective. Expert Opin Investig Drugs 2012; 21: 1123-1140. – reference: Ojha RP, Rastogi M, Devi BP, Agrawal A, Dubey GP: Neuroprotective effect of curcuminoids against inflammation-mediated dopaminergic neurodegeneration in the MPTP model of Parkinson’s disease. J Neuroimmune Pharmacol 2012; 7: 609-618. – reference: Aridon P, Geraci F, Turturici G, D’Amelio M, Savettieri G, Sconzo G: Protective role of heat shock proteins in Parkinson’s disease. Neurodegener Dis 2011; 8: 155-168. – reference: Liu Z, Yu Y, Li X, Ross CA, Smith WW: Curcumin protects against A53T alpha-synuclein-induced toxicity in a PC12 inducible cell model for Parkinsonism. Pharmacol Res 2011; 63: 439-444. – reference: Lv Y, Gong L, Wang Z, Han F, Liu H, Lu X, Liu L: Curcumin inhibits human cytomegalovirus by downregulating heat shock protein 90. Mol Med Rep 2015; 12: 4789-4793. – reference: McFarland NR, Dimant H, Kibuuka L, Ebrahimi-Fakhari D, Desjardins CA, Danzer KM, Danzer M, Fan Z, Schwarzschild MA, Hirst W, McLean PJ: Chronic treatment with novel small molecule Hsp90 inhibitors rescues striatal dopamine levels but not alpha-synuclein-induced neuronal cell loss. PLoS One 2014; 9:e86048. – reference: Cao J, Wang T, Wang M: Investigation of the anti-cataractogenic mechanisms of curcumin through in vivo and in vitro studies. BMC Ophthalmol 2018; 18: 48. – reference: Schneider SA, Obeso JA: Clinical and pathological features of Parkinson’s disease. Curr Top Behav Neurosci 2015; 22: 205-220. – reference: Ahsan N, Mishra S, Jain MK, Surolia A, Gupta S: Curcumin Pyrazole and its derivative (N-(3-Nitrophenylpyrazole) Curcumin inhibit aggregation, disrupt fibrils and modulate toxicity of Wild type and Mutant alpha-Synuclein. Sci Rep 2015; 5: 9862. – reference: Daturpalli S, Waudby CA, Meehan S, Jackson SE: Hsp90 inhibits alpha-synuclein aggregation by interacting with soluble oligomers. J Mol Biol 2013; 425: 4614-4628. – reference: Monti C, Bondi H, Urbani A, Fasano M, Alberio T: Systems biology analysis of the proteomic alterations induced by MPP(+), a Parkinson’s disease-related mitochondrial toxin. Front Cell Neurosci 2015; 9: 14. – reference: Singh PK, Kotia V, Ghosh D, Mohite GM, Kumar A, Maji SK: Curcumin modulates alpha-synuclein aggregation and toxicity. ACS Chem Neurosci 2013; 4: 393-407. – reference: Lee WH, Loo CY, Bebawy M, Luk F, Mason RS, Rohanizadeh R: Curcumin and its derivatives: their application in neuropharmacology and neuroscience in the 21st century. Curr Neuropharmacol 2013; 11: 338-378. – reference: Kalia SK, Kalia LV, McLean PJ: Molecular chaperones as rational drug targets for Parkinson’s disease therapeutics. CNS Neurol Disord Drug Targets 2010; 9: 741-753. – reference: Cui Q, Li X, Zhu H: Curcumin ameliorates dopaminergic neuronal oxidative damage via activation of the Akt/Nrf2 pathway. Mol Med Rep 2016; 13: 1381-1388. – reference: Xie H, Hu H, Chang M, Huang D, Gu X, Xiong X, Xiong R, Hu L, Li G: Identification of chaperones in a MPP(+)-induced and ATRA/TPA-differentiated SH-SY5Y cell PD model. Am J Transl Res 2016; 8: 5659-5671. – reference: van der Merwe C, van Dyk HC, Engelbrecht L, van der Westhuizen FH, Kinnear C, Loos B, Bardien S: Curcumin Rescues a PINK1 Knock Down SH-SY5Y Cellular Model of Parkinson’s Disease from Mitochondrial Dysfunction and Cell Death. Mol Neurobiol 2017; 54: 2752-2762. – reference: Yu S, Wang X, He X, Wang Y, Gao S, Ren L, Shi Y: Curcumin exerts anti-inflammatory and antioxidative properties in 1-methyl-4-phenylpyridinium ion (MPP(+))-stimulated mesencephalic astrocytes by interference with TLR4 and downstream signaling pathway. Cell Stress Chaperones 2016; 21: 697-705. – reference: Yang D, Li T, Liu Z, Arbez N, Yan J, Moran TH, Ross CA, Smith WW: LRRK2 kinase activity mediates toxic interactions between genetic mutation and oxidative stress in a Drosophila model: suppression by curcumin. Neurobiol Dis 2012; 47: 385-392.
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Snippet	Background/Aims: We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson’s disease (PD) and its underlying mechanism. Methods:... We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson's disease (PD) and its underlying mechanism. In this study, genes... We aimed to explore the protective role of curcumin (Cur) in a cell model of Parkinson's disease (PD) and its underlying mechanism.BACKGROUND/AIMSWe aimed to...
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SubjectTerms	1-Methyl-4-phenylpyridinium - toxicity Apoptosis Apoptosis - drug effects bcl-2-Associated X Protein - metabolism bcl-X Protein - metabolism Cell Line, Tumor Cell Proliferation - drug effects Curcumin Curcumin - pharmacology Dopamine - analysis Dopamine Plasma Membrane Transport Proteins - metabolism Dopaminergic neurons Gene Regulatory Networks Heat shock proteins HSP90 HSP90 Heat-Shock Proteins - antagonists & inhibitors HSP90 Heat-Shock Proteins - genetics HSP90 Heat-Shock Proteins - metabolism Humans Kinases Models, Biological Morphology MPP Neurodegeneration Original Paper Parkinson Parkinson Disease - metabolism Parkinson Disease - pathology Parkinson's disease RNA Interference RNA, Small Interfering - metabolism SH-SY5Y
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Title	Curcumin Protects an SH-SY5Y Cell Model of Parkinson’s Disease Against Toxic Injury by Regulating HSP90
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