Oleuropein and rutin protect against 6-OHDA-induced neurotoxicity in PC12 cells through modulation of mitochondrial function and unfolded protein response

Achour I, Arel-Dubeau AM, Renaud J, Legrand M, Attard E, Germain M, Martinoli MG. (2016). Oleuropein Prevents Neuronal Death, Mitigates Mitochondrial Superoxide Production and Modulates Autophagy in a Dopaminergic Cellular Model. Int J Mol Sci 17: E1293.10.3390/ijms17081293500069027517912Open DOISearch in Google Scholar

Alirezaei M, Rezaei M, Hajighahramani S, Sookhtehzari A, Kiani K. (2016). Oleuropein attenuates cognitive dysfunction and oxidative stress induced by some anesthetic drugs in the hippocampal area of rats. J Physiol Sci 67: 131-139.Search in Google Scholar

Ataie A, Shadifar M, Ataee R. (2016). Polyphenolic Antioxidants and Neuronal Regeneration. Basic Clin Neurosci 7: 81-90.Search in Google Scholar

Bali EB, Ergin V, Rackova L, Bayraktar O, Kucukboyaci N, Karasu C. (2014). Olive leaf extracts protect cardiomyocytes against 4-hydroxynonenal-induced toxicity in vitro: comparison with oleuropein, hydroxytyrosol, and quercetin. Planta Med 80: 984-92.Search in Google Scholar

Barbaro B, Toietta G, Maggio R, Arciello M, Tarocchi M, Galli A, Balsano C. (2014). Eff ects of the olive-derived polyphenol oleuropein on human health. Int J Mol Sci 15: 18508-24.10.3390/ijms151018508422722925318054Open DOISearch in Google Scholar

Benyair R, Ron E, Lederkremer GZ. (2011). Protein quality control, retention, and degradation at the endoplasmic reticulum. Int Rev Cell Mol Biol 292: 197-280.Search in Google Scholar

Cai P, Ye J, Zhu J, Liu D, Chen D, Wei X, Johnson NR, Wang Z, Zhang H, Cao G, Xiao J, Ye J, Lin L. (2016). Inhibition of Endoplasmic Reticulum Stress is Involved in the Neuroprotective Eff ect of bFGF in the 6-OHDA-Induced Parkinson’s Disease Model. Aging Dis 7: 336-449.Search in Google Scholar

Calabrese V, Cornelius C, Mancuso C, Lentile R, Stella AM, Butterfi eld DA. (2010). Redox homeostasis and cellular stress response in aging and neurodegeneration. Methods Mol Biol 610: 285-308.Search in Google Scholar

Carrasco-Pozo C, Mizgier ML, Speisky H, Gotteland M. (2012). Diff erential protective eff ects of quercetin, resveratrol, rutin and epigallocatechin gallate against mitochondrial dysfunction induced by indomethacin in Caco-2 cells. Chem Biol Interact 195: 199-205.Search in Google Scholar

Casamenti F, Grossi C, Rigacci S, Pantano D, Luccarini I, Stefani M. (2015). Oleuropein Aglycone: A Possible Drug against Degenerative Conditions. In Vivo Evidence of its Eff ectiveness against Alzheimer’s Disease. J Alzheimers Dis 45: 679-88.Search in Google Scholar

Chao Y, Wong SC, Tan EK. (2014). Evidence of infl ammatory system involvement in Parkinson’s disease. Biomed Res Int 2014: 308654.Search in Google Scholar

Cheng J, Xia X, Rui Y, Zhang Z, Qin L, Han S, Wan Z. (2016). The combination of 1α,25dihydroxyvitaminD3 with resveratrol improves neuronal degeneration by regulating endoplasmic reticulum stress, insulin signaling and inhibiting tau hyperphosphorylation in SH-SY5Y cells. Food Chem Toxicol 93: 32-40.Search in Google Scholar

Choi JH, Choi AY, Yoon H, Choe W, Yoon KS, Ha J, Yeo EJ, Kang I. (2010). Baicalein protects HT22 murine hippocampal neuronal cells against endoplasmic reticulum stress-induced apoptosis through inhibition of reactive oxygen species production and CHOP induction. Exp Mol Med 42(12): 811-22.Search in Google Scholar

Credle JJ, Forcelli PA, Delannoy M, Oaks AW, Permaul E, Berry DL, Duka V, Wills J, Sidhu A. (2015). α-Synuclein-mediated inhibition of ATF6 processing into COPII vesicles disrupts UPR signaling in Parkinson’s disease. Neurobiol Dis 76: 112-25.Search in Google Scholar

Cumaoglu A, Ari N, Kartal M, Karasu C. (2011a). Polyphenolic extracts from Olea europea L. protect against cytokine-induced β-cell damage through maintenance of redox homeostasis. Rejuvenation Res 14: 325-34.10.1089/rej.2010.111121745095Search in Google Scholar

Cumaoglu A, Rackova L, Stefek M, Kartal M, Maechler P, Karasu C. (2011b). Eff ects of olive leaf polyphenols against H2O2 toxicity in insulin secreting β-cells. Acta Biochim Pol 58: 45-50.10.18388/abp.2011_2284Search in Google Scholar

Davie CA. (2008). A review of Parkinson’s disease. Br Med Bull 86: 109-27. Search in Google Scholar

Deng C, Tao R, Yu SZ, Jin H. (2012). Inhibition of 6-hydroxydopamine-induced endoplasmic reticulum stress by sulforaphane through the activation of Nrf2 nuclear translocation. Mol Med Rep 6: 215-9.Search in Google Scholar

Dias V, Junn E, Mouradian MM. (2013). The role of oxidative stress in Parkinson’s disease. J Parkinsons Dis 3: 461-91.Search in Google Scholar

Ebrahimi-Fakhari D, Wahlster L, McLean PJ. (2012). Protein degradation pathways in Parkinson’s disease: curse or blessing. Acta Neuropathol 124: 153-72.Search in Google Scholar

El-Horany HE, El-Latif RN, ElBatsh MM, Emam MN. (2016). Ameliorative Eff ect of Quercetin on Neurochemical and Behavioral Defi cits in Rotenone Rat Model of Parkinson’s Disease: Modulating Autophagy (Quercetin on Experimental Parkinson’s Disease). J Biochem Mol Toxicol 30: 360-9.10.1002/jbt.2182127252111Open DOISearch in Google Scholar

Exner N, Lutz AK, Haass C, Winklhofer KF. (2012). Mitochondrial dysfunction in Parkinson’s disease: molecular mechanisms and pathophysiological consequences. EMBO J 31: 3038-62.10.1038/emboj.2012.170340001922735187Open DOISearch in Google Scholar

Fahn S, Sulzer D. (2014). Neurodegeneration and neuroprotection in Parkinson disease. NeuroRx 1: 139-54.Search in Google Scholar

Federico A, Cardaioli E, Da Pozzo P, Formichi P, Gallus GN, Radi E. (2012). Mitochondria, oxidative stress and neurodegeneration. J Neurol Sci 322: 254-62.Search in Google Scholar

Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP. (2010). Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 30: 16938-48.10.1523/JNEUROSCI.1598-10.2010663492621159964Open DOISearch in Google Scholar

Halperin L, Jung J, Michalak M. (2014). The many functions of the endoplasmic reticulum chaperones and folding enzymes. IUBMB Life 66: 318-26.10.1002/iub.127224839203Open DOISearch in Google Scholar

Hauser DN, Hastings TG. (2013). Mitochondrial dysfunction and oxidative stress in Parkinson’s disease and monogenic parkinsonism. Neurobiol Dis 51: 35-42.10.1016/j.nbd.2012.10.011356556423064436Open DOISearch in Google Scholar

Hoozemans JJ, Scheper W. (2012). Endoplasmic reticulum: the unfolded protein response is tangled in neurodegeneration. Int J Biochem Cell Biol 44: 1295-8.Search in Google Scholar

Hosoi T, Ozawa K. (2009). Endoplasmic reticulum stress in disease: mechanisms and therapeutic opportunities. Clin Sci (Lond) 118: 19-29.Search in Google Scholar

Hu LW, Yen JH, Shen YT, Wu KY, Wu MJ. (2014). Luteolin modulates 6-hydroxydopamine- induced transcriptional changes of stress response pathways in PC12 cells. PLoS One 9: e97880.Search in Google Scholar

Jha SK, Jha NK, Kumar D, Ambasta RK, Kumar P. (2017). Linking mitochondrial dysfunction, metabolic syndrome and stress signaling in Neurodegeneration. Biochim Biophys Acta 1863: 1132-1146.10.1016/j.bbadis.2016.06.01527345267Open DOISearch in Google Scholar

Joshi DC, Bakowska JC. (2011). Determination of mitochondrial membrane potential and reactive oxygen species in live rat cortical neurons. J Vis Exp 51: pii. 2704.Search in Google Scholar

Khan MM, Raza SS, Javed H, Ahmad A, Khan A, Islam F, Safhi MM, Islam F. (2012). Rutin protects dopaminergic neurons from oxidative stress in an animal model of Parkinson’s disease. Neurotox Res 22: 1-15.10.1007/s12640-011-9295-222194158Open DOISearch in Google Scholar

Kim-Han JS, O’Malley KL. (2007). Cell stress induced by the parkinsonian mimetic, 6-hydroxydopamine, is concurrent with oxidation of the chaperone, ERp57, and aggresome formation. Antioxid Redox Signal 9: 2255-64.Search in Google Scholar

Kim Y, Li E, Park S. (2012). Insulin-like growth factor-1 inhibits 6-hydroxydopamine- mediated endoplasmic reticulum stress-induced apoptosis via regulation of heme oxygenase-1 and Nrf2 expression in PC12 cells. Int J Neurosci 122: 641-9.Search in Google Scholar

Kondratyev M, Avezov E, Shenkman M, Groisman B, Lederkremer GZ. (2007). PERK-dependent compartmentalization of ERAD and unfolded protein response machineries during ER stress. Exp Cell Res 313: 3395-407.Search in Google Scholar

Kulich SM, Horbinski C, Patel M, Chu CT. (2007). 6-Hydroxydopamine induces mitochondrial ERK activation. Free Radic Biol Med 43: 372-83.Search in Google Scholar

Lee AH, Iwakoshi NN, Glimcher LH. (2003). XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-59.10.1128/MCB.23.21.7448-7459.200320764314559994Open DOISearch in Google Scholar

Leitman J, Ron E, Ogen-Shtern N, Lederkremer GZ. (2013). Compartmentalization of endoplasmic reticulum quality control and ER-associated degradation factors. DNA Cell Biol 32: 2-7.10.1089/dna.2012.188923194074Open DOISearch in Google Scholar

Li B, Xiao L, Wang ZY, Zheng PS. (2014). Knockdown of STIM1 inhibits 6-hydroxydopamine- induced oxidative stress through attenuating calcium-dependent ER stress and mitochondrial dysfunction in undiff erentiated PC12 cells. Free Radic Res 48: 758-68.Search in Google Scholar

Li Y, Li J, Li S, Li Y, Wang X, Liu B, Fu Q, Ma S. (2015). Curcumin attenuates glutamate neurotoxicity in the hippocampus by suppression of ER stress-associated TXNIP/NLRP3 infl ammasome activation in a manner dependent on AMPK. Toxicol Appl Pharmacol 286: 53-63.Search in Google Scholar

Magalingam KB, Radhakrishnan A, Haleagrahara N. (2016). Protective eff ects of quercetin glycosides, rutin, and isoquercetrin against 6-hydroxydopamine (6-OHDA)-induced neurotoxicity in rat pheochromocytoma (PC-12) cells. Int J Immunopathol Pharmacol 29: 30-9.Search in Google Scholar

Martin-Aragon S, Jimenez-Aliaga KL, Benedi J, Bermejo-Bescos P. (2016). Neurohormetic responses of quercetin and rutin in a cell line over-expressing the amyloid precursor protein (APPswe cells). Phytomedicine 23(12): 1285-1294.Search in Google Scholar

Martorell M, Forman K, Castro N, Capo X, Tejada S, Sureda A. (2016). Potential Therapeutic Eff ects of Oleuropein Aglycone in Alzheimer’s Disease. Curr Pharm Biotechnol 17: 994-1001.10.2174/138920101766616072512065627455905Open DOISearch in Google Scholar

Mattson MP, Cheng A. (2006). Neurohormetic phytochemicals: Low-dose toxins that induce adaptive neuronal stress responses. Trends Neurosci 29 (11): 632-9.10.1016/j.tins.2006.09.00117000014Open DOISearch in Google Scholar

Meng H, Li C, Feng L, Cheng B, Wu F, Wang X, Li Z, Liu S. (2007). Eff ects of Ginkgolide B on 6-OHDA-induced apoptosis and calcium over load in cultured PC12. Int J Dev Neurosci 25: 509-14.10.1016/j.ijdevneu.2007.09.01017981425Open DOISearch in Google Scholar

Mercado G, Castillo V, Vidal R, Hetz C. (2015). ER proteostasis disturbances in Parkinson’s disease: novel insights. Front Aging Neurosci 7: 39.Search in Google Scholar

Mercado G, Valdes P, Hetz C. (2013). An ERcentric view of Parkinson’s disease. Trends Mol Med 19: 165-75.10.1016/j.molmed.2012.12.00523352769Open DOISearch in Google Scholar

Muralidharan S, Mandrekar P. (2013). Cellular stress response and innate immune signaling: integrating pathways in host defense and infl ammation. J Leukoc Biol 94: 1167-84.Search in Google Scholar

Murugaiyah V, Mattson MP. (2015). Neurohormetic phytochemicals: An evolutionary- bioenergetic perspective. Neurochem Int 89: 271-80.Search in Google Scholar

Ogen-Shtern N, Ben David T, Lederkremer GZ. (2016). Protein aggregation and ER stress. Brain Res 1648: 658-666.10.1016/j.brainres.2016.03.04427037184Open DOISearch in Google Scholar

Pantano D, Luccarini I, Nardiello P, Servili M, Stefani M, Casamenti F. (2017). Oleuropein aglycone and polyphenols from olive mill wastewater ameliorate cognitive defi cits and neuropathology. Br J Clin Pharmacol 83: 54-62.10.1111/bcp.12993533813527131215Open DOISearch in Google Scholar

Pasban-Aliabadi H, Esmaeili-Mahani S, Sheibani V, Abbasnejad M, Mehdizadeh A, Yaghoobi MM. (2013). Inhibition of 6-hydroxydopamine-induced PC12 cell apoptosis by olive (Olea europaea L.) leaf extract is performed by its main component oleuropein. Rejuvenation Res 16: 134-42.Search in Google Scholar

Penke B, Bogar F, Fulop L. (2016). Protein Folding and Misfolding, Endoplasmic Reticulum Stress in Neurodegenerative Diseases: in Trace of Novel Drug Targets. Curr Protein Pept Sci 17: 169-82.Search in Google Scholar

Perri ER, Thomas CJ, Parakh S, Spencer DM, Atkin JD. (2016). The Unfolded Protein Response and the Role of Protein Disulfi de Isomerase in Neurodegeneration. Front Cell Dev Biol 3: 80.Search in Google Scholar

Pourkhodadad S, Alirezaei M, Moghaddasi M, Ahmadvand H, Karami M, Delfan B, Khanipour Z. (2016). Neuroprotective eff ects of oleuropein against cognitive dysfunction induced by colchicine in hippocampal CA1 area in rats. J Physiol Sci 66: 397-405.Search in Google Scholar

Rieger AM, Nelson KL, Konowalchuk JD, Barreda DR. (2011). Modifi ed annexin V/propidium iodide apoptosis assay for accurate assessment of cell death. J Vis Exp 50: 2597.Search in Google Scholar

Rigacci S, Stefani M. (2016). Nutraceutical Properties of Olive Oil Polyphenols. An Itinerary from Cultured Cells through Animal Models to Humans. Int J Mol Sci 17: E843.10.3390/ijms17060843492637727258251Open DOISearch in Google Scholar

Rodriguez-Morato J, Xicota L, Fito M, Farre M, Dierssen M, de la Torre R. (2015). Potential role of olive oil phenolic compounds in the prevention of neurodegenerative diseases. Molecules 20: 4655-80.Search in Google Scholar

Sarbishegi M, Mehraein F, Soleimani M. (2014). Antioxidant role of oleuropein on midbrain and dopaminergic neurons of substantia nigra in aged rats. Iran Biomed J 18: 16-22.Search in Google Scholar

Schroder M, Kaufman RJ. (2005). ER stress and the unfolded protein response. Mutat Res 569: 29-63.Search in Google Scholar

Sun X, Liu J, Crary JF, Malagelada C, Sulzer D, Greene LA, Levy OA. (2013). ATF4 protects against neuronal death in cellular Parkinson’s disease models by maintaining levels of parkin. J Neurosci 33: 2398-407.10.1523/JNEUROSCI.2292-12.2013371161823392669Open DOISearch in Google Scholar

Szegezdi E, Logue SE, Gorman AM, Samali A. (2006). Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880-5.10.1038/sj.embor.7400779155967616953201Open DOISearch in Google Scholar

Taylor JM, Main BS, Crack PJ. (2013). Neuroinfl ammation and oxidative stress: co-conspirators in the pathology of Parkinson’s disease. Neurochem Int 62: 803-19.10.1016/j.neuint.2012.12.01623291248Open DOISearch in Google Scholar

Tsai YC, Weissman AM. (2010). The Unfolded Protein Response, Degradation from Endoplasmic Reticulum and Cancer. Genes Cancer 1: 764-778.Search in Google Scholar

Tsuru A, Imai Y, Saito M, Kohno K. (2016). Novel mechanism of enhancing IRE1α-XBP1 signalling via the PERK-ATF4 pathway. Sci Rep 6: 24217.Search in Google Scholar

Valdes P, Mercado G, Vidal RL, Molina C, Parsons G, Court FA, Martinez A, Galleguillos D, Armentano D, Schneider BL, Hetz C. (2014). Control of dopaminergic neuron survival by the unfolded protein response transcription factor XBP1. Proc Natl Acad Sci U S A 111: 6804-9.Search in Google Scholar

Wang YH, Xuan ZH, Tian S, Du GH. (2015). Echinacoside Protects against 6-Hydroxydopamine-Induced Mitochondrial Dysfunction and Infl ammatory Responses in PC12 Cells via Reducing ROS Production. Evid. Based Complement. Alternat Med 2015: 189239.Search in Google Scholar

Wu PS, Yen JH, Kou MC, Wu MJ. (2015). Luteolin and Apigenin Attenuate 4-Hydroxy-2-Nonenal-Mediated Cell Death through Modulation of UPR, Nrf2-ARE and MAPK Pathways in PC12 Cells. PLoS One 10: e0130599.Search in Google Scholar

Zeeshan HM, Lee GH, Kim HR, Chae HJ. (2016). Endoplasmic Reticulum Stress and Associated ROS. Int J Mol Sci 17: 327.10.3390/ijms17030327481318926950115Open DOISearch in Google Scholar

Zhai X, Ding Y, Wang Q, Zhang H, Li F. (2016). Rutin Acid Ameliorates Neural Apoptosis Induced by Traumatic Brain Injury via Mitochondrial Pathways in Mice. Neuroimmunomodulation 23: 179-187.10.1159/00044871627644033Open DOISearch in Google Scholar

Zhang C, Li C, Chen S, Li Z, Jia X, Wang K, Bao J, Liang Y, Wang X, Chen M, Li P, Su H, Wan JB, Lee SMY, Liu K, He C. (2017). Berberine protects against 6-OHDA-induced neurotoxicity in PC12 cells and zebrafi sh through hormetic mechanisms involving PI3K/AKT/Bcl-2 and Nrf2/HO-1 pathways. Redox Biol 11: 1-11.10.1016/j.biologicals.2017.04.00228427828Open DOISearch in Google Scholar

Zhang C, Li C, Chen S, Li Z, Ma L, Jia X, Wang K, Bao J, Liang Y, Chen M, Li P, Su H, Lee SM, Liu K, Wan JB, He C. (2017). Hormetic eff ect of panaxatriol saponins confers neuroprotection in PC12 cells and zebrafi sh through PI3K/ AKT/mTOR and AMPK/SIRT1/FOXO3 pathways. Sci Rep 7: 41082.Search in Google Scholar

Zuo L, Motherwell MS. (2013). The impact of reactive oxygen species and genetic mitochondrial mutations in Parkinson’s disease. Gene 532: 18-23.Search in Google Scholar