Inhibition of α-Synuclein contributes to the ameliorative effects of dietary flavonoids luteolin on arsenite-induced apoptotic cell death in the dopaminergic PC12 cells

References

• Abdul KSM, Jayasinghe SS, Chandana EPS, Jayasumana C, De Silva PMCS. 2015. Arsenic and human health effects: a review. Environ Toxicol Pharmacol. 40:828–846.
   PubMed Web of Science ®Google Scholar
• Ameer SS, Engström K, Harari F, Concha G, Vahter M, Broberg K. 2015. The effects of arsenic exposure on blood pressure and early risk markers of cardiovascular disease: evidence for population differences. Environ Res. 140:32–36.
   PubMed Web of Science ®Google Scholar
• An Z, Qi Y, Huang D, Gu X, Tian Y, Li P, Li H, Zhang Y. 2014. EGCG inhibits Cd(2+)-induced apoptosis through scavenging ROS rather than chelating Cd(2+) in HL-7702 cells. Toxicol Mech Methods. 24:259–267.
   PubMed Web of Science ®Google Scholar
• Angelova PR, Horrocks MH, Klenerman D, Gandhi S, Abramov AY, Shchepinov MS. 2015. Lipid peroxidation is essential for α-synuclein-induced cell death. J Neurochem. 133:582–589.
   PubMed Web of Science ®Google Scholar
• Antony PMA, Diederich NJ, Krüger R, Balling R. 2013. The hallmarks of Parkinson's disease. FEBS J. 280:5981–5993.
   PubMed Web of Science ®Google Scholar
• Chandravanshi LP, Shukla RK, Sultana S, Pant AB, Khanna VK. 2014. Early life arsenic exposure and brain dopaminergic alterations in rats. Int J Dev Neurosci. 38:91–104.
   PubMed Web of Science ®Google Scholar
• Chen C, Gu S, Jiang X, Zhang Z. 2015a. Arsenite-induced endoplasmic reticulum: dependent apoptosis through disturbance of calcium homeostasis in HBE cell line. Environ Toxicol. 32:197–216.
   PubMed Web of Science ®Google Scholar
• Chen C, Gu S, Jiang X, Zhang Z. 2015b. Nuclear translocation of nuclear factor kappa B is regulated by G protein signaling pathway in arsenite-induced apoptosis in HBE cell line. Environ Toxicol. 31:1819–1833.
   PubMed Web of Science ®Google Scholar
• Chen C, Jiang X, Gu S, Lai Y, Lu Y, Zhang Z. 2016. Protection of Nrf2 against arsenite-induced oxidative damage is regulated by the cyclic guanosine monophosphate‐protein kinase G signaling pathway. Environ Toxicol. doi: 10.1002/tox.22374.
   Web of Science ®Google Scholar
• Chen C, Jiang X, Lai Y, Liu Y, Zhang Z. 2015c. Resveratrol protects against arsenic trioxide‐induced oxidative damage through maintenance of glutathione homeostasis and inhibition of apoptotic progression. Environ Mol Mutagen. 56:333–346.
   PubMed Web of Science ®Google Scholar
• Cholanians AB, Phan AV, Ditzel EJ, Camenisch TD, Lau SS, Monks TJ. 2016. From the cover: arsenic induces accumulation of α-synuclein: implications for synucleinopathies and neurodegeneration. Toxicol Sci. 153:271–281.
   PubMed Web of Science ®Google Scholar
• Deas E, Cremades N, Angelova PR, Ludtmann MH, Yao Z, Chen S, Horrocks MH, Banushi B, Little D, Devine MJ. 2015. Alpha-synuclein oligomers interact with metal ions to induce oxidative stress and neuronal death in Parkinson's disease. Antioxid Redox Signal. 24:376–391.
   Web of Science ®Google Scholar
• Gao X, Cassidy A, Schwarzschild MA, Rimm EB, Ascherio A. 2012. Habitual intake of dietary flavonoids and risk of Parkinson disease. Neurology. 78:1138–1145.
   PubMed Web of Science ®Google Scholar
• Gong G, O'Bryant SE. 2010. The arsenic exposure hypothesis for Alzheimer disease. Alzheimer Dis Assoc Disord. 24:311–316.
   PubMed Web of Science ®Google Scholar
• Grau-Pérez M, Kuo C-C, Spratlen M, Thayer KA, Mendez MA, Hamman RF, Dabelea D, Adgate JL, Knowler WC, Bell RA. 2017. The association of arsenic exposure and metabolism with type 1 and type 2 diabetes in youth: the SEARCH case-control study. Diabetes Care. 40:46–53.
   PubMed Web of Science ®Google Scholar
• Gu S, Chen C, Jiang X, Zhang Z. 2016. ROS-mediated endoplasmic reticulum stress and mitochondrial dysfunction underlie apoptosis induced by resveratrol and arsenic trioxide in A549 cells. Chem Biol Interact. 245:100–109.
   PubMed Web of Science ®Google Scholar
• Hartmann A, Hunot S, Michel PP, Muriel MP, Vyas S, Faucheux BA, Mouatt-Prigent A, Turmel H, Srinivasan A, Ruberg M, et al. 2000. Caspase-3: a vulnerability factor and final effector in apoptotic death of dopaminergic neurons in Parkinson's disease. Proc Natl Acad Sci USA. 97:2875–2880.
   PubMed Web of Science ®Google Scholar
• Hirsch EC, Hunot S, Faucheux B, Agid Y, Mizuno Y, Mochizuki H, Tatton WG, Tatton N, Olanow WC. 1999. Dopaminergic neurons degenerate by apoptosis in Parkinson's disease. Mov Disord. 14:383–385.
   PubMed Web of Science ®Google Scholar
• Huang C-S, Lii C-K, Lin A-H, Yeh Y-W, Yao H-T, Li C-C, Wang T-S, Chen H-W. 2013. Protection by chrysin, apigenin, and luteolin against oxidative stress is mediated by the Nrf2-dependent up-regulation of heme oxygenase 1 and glutamate cysteine ligase in rat primary hepatocytes. Arch Toxicol. 87:167–178.
   PubMed Web of Science ®Google Scholar
• Ibáñez P, Bonnet A-M, Débarges B, Lohmann E, Tison F, Agid Y, Dürr A, Brice A, Pollak P. 2004. Causal relation between α-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet. 364:1169–1171.
   PubMed Web of Science ®Google Scholar
• Ivanov VN, Hei TK. 2013. Induction of apoptotic death and retardation of neuronal differentiation of human neural stem cells by sodium arsenite treatment. Exp Cell Res. 319:875–887.
   PubMed Web of Science ®Google Scholar
• Jang S, Dilger RN, Johnson RW. 2010. Luteolin inhibits microglia and alters hippocampal-dependent spatial working memory in aged mice. J Nutri. 140:1892–1898.
   PubMed Web of Science ®Google Scholar
• Ju W, Wang X, Shi H, Chen W, Belinsky SA, Lin Y. 2007. A critical role of luteolin-induced reactive oxygen species in blockage of tumor necrosis factor-activated nuclear factor-kappaB pathway and sensitization of apoptosis in lung cancer cells. Mol Pharmacol. 71:1381–1388.
   PubMed Web of Science ®Google Scholar
• Lopez-Lazaro M. 2009. Distribution and biological activities of the flavonoid luteolin. MRMC. 9:31–59.
   Google Scholar
• Maries E, Dass B, Collier TJ, Kordower JH, Steece-Collier K. 2003. The role of alpha-synuclein in Parkinson's disease: insights from animal models. Nat Rev Neurosci. 4:727–738.
   PubMed Web of Science ®Google Scholar
• Mittal M, Flora SJS. 2007. Vitamin E supplementation protects oxidative stress during arsenic and fluoride antagonism in male mice. Drug Chem Toxicol. 30:263–281.
   PubMed Web of Science ®Google Scholar
• Mondal R, Biswas S, Chatterjee A, Mishra R, Mukhopadhyay A, Bhadra RK, Mukhopadhyay PK. 2016. Protection against arsenic-induced hematological and hepatic anomalies by supplementation of vitamin C and vitamin E in adult male rats. J Basic Clin Physiol Pharmacol. 27:643–652.
   PubMedGoogle Scholar
• Perier C, Bové J, Vila M. 2012. Mitochondria and programmed cell death in Parkinson's disease: apoptosis and beyond. Antioxid Redox Signal. 16:883–895.
   PubMed Web of Science ®Google Scholar
• Pratheeshkumar P, Son Y-O, Divya SP, Roy RV, Hitron JA, Wang L, Kim D, Dai J, Asha P, Zhang Z, et al. 2014. Luteolin inhibits Cr(VI)-induced malignant cell transformation of human lung epithelial cells by targeting ROS mediated multiple cell signaling pathways. Toxicol Appl Pharmacol. 281:230–241.
   PubMed Web of Science ®Google Scholar
• Qiao H, Dong L, Zhang X, Zhu C, Zhang X, Wang L, Liu Z, Chen L, Xing Y, Wang C, et al. 2012. Protective effect of luteolin in experimental ischemic stroke: upregulated SOD1, CAT, Bcl-2 and claudin-5, down-regulated MDA and Bax expression. Neurochem Res. 37:2014–2024.
   PubMed Web of Science ®Google Scholar
• Russo M, Spagnuolo C, Tedesco I, Bilotto S, Russo GL. 2012. The flavonoid quercetin in disease prevention and therapy: facts and fancies. Biochem Pharmacol. 83:6–15.
   PubMed Web of Science ®Google Scholar
• Sárközi K, Papp A, Horváth E, Máté Z, Ferencz Á, Hermesz E, Krisch J, Paulik E, Szabó A. 2016. Green tea and vitamin C ameliorate some neuro-functional and biochemical signs of arsenic toxicity in rats. Nutr Neurosci. 19:102–109.
   PubMed Web of Science ®Google Scholar
• Shavali S, Sens DA. 2008. Synergistic neurotoxic effects of arsenic and dopamine in human dopaminergic neuroblastoma SH-SY5Y cells. Toxicol Sci. 102:254–261.
   PubMed Web of Science ®Google Scholar
• Siracusa R, Paterniti I, Impellizzeri D, Cordaro M, Crupi R, Navarra M, Cuzzocrea S, Esposito E. 2015. The association of palmitoylethanolamide with luteolin decreases neuroinflammation and stimulates autophagy in Parkinson's disease model. CNS Neurol Disord Drug Targets. 14:1350–1365.
   PubMed Web of Science ®Google Scholar
• Vahidnia A, Van Der Voet G, De Wolff F. 2007. Arsenic neurotoxicity-a review. Hum Exp Toxicol. 26:823–832.
   PubMed Web of Science ®Google Scholar
• Vila M, Przedborski S. 2003. Targeting programmed cell death in neurodegenerative diseases. Nat Rev Neurosci. 4:365–375.
   PubMed Web of Science ®Google Scholar
• Wang H, Wang H, Cheng H, Che Z. 2016. Ameliorating effect of luteolin on memory impairment in an Alzheimer's disease model. Mol Med Rep. 13:4215–4220.
   PubMed Web of Science ®Google Scholar
• Xu J, Wang H, Ding K, Zhang L, Wang C, Li T, Wei W, Lu X. 2014. Luteolin provides neuroprotection in models of traumatic brain injury via the Nrf2-ARE pathway. Free Radic Biol Med. 71:186–195.
   PubMed Web of Science ®Google Scholar
• Yasuda T, Mochizuki H. 2010. The regulatory role of α-synuclein and parkin in neuronal cell apoptosis; possible implications for the pathogenesis of Parkinson's disease. Apoptosis. 15:1312–1321.
   PubMed Web of Science ®Google Scholar
• Yasuda T, Nakata Y, Mochizuki H. 2013. α-Synuclein and neuronal cell death. Mol Neurobiol. 47:466–483.
   PubMed Web of Science ®Google Scholar
• Yu D, Li M, Tian Y, Liu J, Shang J. 2015. Luteolin inhibits ROS-activated MAPK pathway in myocardial ischemia/reperfusion injury. Life Sci. 122:15–25.
   PubMed Web of Science ®Google Scholar
• Zarazúa S, Bürger S, Delgado JM, Jiménez-Capdeville ME, Schliebs R. 2011. Arsenic affects expression and processing of amyloid precursor protein (APP) in primary neuronal cells overexpressing the Swedish mutation of human APP. Int J Dev Neurosci. 29:389–396.
   PubMed Web of Science ®Google Scholar
• Zhou W, Hurlbert MS, Schaack J, Prasad KN, Freed CR. 2000. Overexpression of human alpha-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalon-derived cells. Brain Res. 866:33–43.
   PubMed Web of Science ®Google Scholar