Resveratrol provides neuroprotective effects through modulation of mitochondrial dynamics and ERK1/2 regulated autophagy

References

• Lang AE, Lozano AM. Parkinson’s disease: first of two parts. N Engl J Med. 1998;339:1044–1053.
   PubMed Web of Science ®Google Scholar
• Grenier K, McLelland GL, Fon EA. Parkin- and PINK1-dependent mitophagy in neurons: will the real pathway please stand up? Front Neurol. 2013;4:100.
   PubMed Web of Science ®Google Scholar
• Obeso JA, Stamelou M, Goetz CG, et al. Past, present, and future of Parkinson’s disease: a special essay on the 200th Anniversary of the Shaking Palsy. Mov Disord. 2017;32:1264–1310.
   PubMed Web of Science ®Google Scholar
• Poewe W, Seppi K, Tanner CM, et al. Parkinson’s disease. Nat Rev Dis Primers. 2017;3:17013.
   PubMed Web of Science ®Google Scholar
• Celardo I, Martins LM, Gandhi S. Unravelling mitochondrial pathways to Parkinson’s disease. Br J Pharmacol. 2014;171:1943–1957.
   PubMed Web of Science ®Google Scholar
• Serrat R, Mirra S, Figueiro-Silva J, et al. The Armc10/SVH gene: genome context, regulation of mitochondrial dynamics and protection against Abeta-induced mitochondrial fragmentation. Cell Death Dis. 2014;5:e1163.
   PubMed Web of Science ®Google Scholar
• Lin T-K, Liou C-W, Chen S-D, et al. Mitochondrial dysfunction and biogenesis in the pathogenesis of Parkinson’s disease. Chang Gung Med J. 2009;32:589–599.
   PubMedGoogle Scholar
• Winklhofer KF, Haass C. Mitochondrial dysfunction in Parkinson’s disease. Biochim Biophys Acta. 2010;1802:29–44.
   PubMed Web of Science ®Google Scholar
• Morimoto N, Nagai M, Miyazaki K, et al. Induction of parkinsonism-related proteins in the spinal motor neurons of transgenic mouse carrying a mutant SOD1 gene. J Neurosci Res. 2010;NA–N8:1804–1811.
   PubMed Web of Science ®Google Scholar
• Hasmetayhan H, Dilek A, Kemal B, et al. Mitochondrial complex I, II/III, and IV activities in familial and sporadic Parkinson’s disease. Int J Neurosci. 2005;115:479–493.
   PubMed Web of Science ®Google Scholar
• Islam MT. Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol Res. 2017;39:73–82.
   PubMed Web of Science ®Google Scholar
• Arnold B, Cassady SJ, VanLaar VS, Berman SB. Integrating multiple aspects of mitochondrial dynamics in neurons: age-related differences and dynamic changes in a chronic rotenone model. Neurobiol Dis. 2011;41:189–200.
   PubMed Web of Science ®Google Scholar
• Lin T-K, Chen S-D, Chuang Y-C, et al. Resveratrol partially prevents rotenone-induced neurotoxicity in dopaminergic SH-SY5Y cells through induction of heme oxygenase-1 dependent autophagy. IJMS. 2014;15:1625–1646.
   Google Scholar
• Peng K, Yang L, Wang J, et al. The interaction of mitochondrial biogenesis and fission/fusion mediated by PGC-1alpha regulates rotenone-induced dopaminergic neurotoxicity. Mol Neurobiol. 2017;54:3783–3797.
   PubMed Web of Science ®Google Scholar
• Sgambato A, Ardito R, Faraglia B, et al. Resveratrol, a natural phenolic compound, inhibits cell proliferation and prevents oxidative DNA damage. Mutat Res. 2001;496:171–180.
   PubMed Web of Science ®Google Scholar
• Harikumar KB, Aggarwal BB. Resveratrol: a multitargeted agent for age-associated chronic diseases. Cell Cycle. 2008;7:1020–1035.
   PubMed Web of Science ®Google Scholar
• Lin T-K, Huang L-T, Huang Y-H, et al. The effect of the red wine polyphenol resveratrol on a rat model of biliary obstructed cholestasis: involvement of anti-apoptotic signalling, mitochondrial biogenesis and the induction of autophagy. Apoptosis. 2012;17:871–879.
   PubMed Web of Science ®Google Scholar
• Zeng W, Zhang W, Lu F, et al. Resveratrol attenuates MPP+-induced mitochondrial dysfunction and cell apoptosis via AKT/GSK-3beta pathway in SN4741 cells. Neurosci Lett. 2017;637:50–56.
   PubMed Web of Science ®Google Scholar
• Jin F, Wu Q, Lu Y-F, et al. Neuroprotective effect of resveratrol on 6-OHDA-induced Parkinson’s disease in rats. Eur J Pharmacol. 2008;600:78–82.
   PubMed Web of Science ®Google Scholar
• Rojas-Charry L, Cookson MR, Niño A, et al. Downregulation of Pink1 influences mitochondrial fusion-fission machinery and sensitizes to neurotoxins in dopaminergic cells. Neurotoxicology. 2014;44:140–148.
   PubMed Web of Science ®Google Scholar
• Dhingra R, Kirshenbaum LA. Regulation of mitochondrial dynamics and cell fate [Research Support, Non-U.S]. Circ J. 2014;78:803–810.
   PubMed Web of Science ®Google Scholar
• Haelterman NA, Yoon WH, Sandoval H, et al. A mitocentric view of Parkinson’s disease. Annu Rev Neurosci. 2014;37:137–159.
   PubMed Web of Science ®Google Scholar
• Kieper N, Holmström KM, Ciceri D, et al. Modulation of mitochondrial function and morphology by interaction of Omi/HtrA2 with the mitochondrial fusion factor OPA1. Exp Cell Res. 2010;316:1213–1224.
   PubMed Web of Science ®Google Scholar
• Dickey AS, Strack S. PKA/AKAP1 and PP2A/Bβ2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. J Neurosci. 2011;31:15716–15726.
   PubMed Web of Science ®Google Scholar
• Wakai T, Harada Y, Miyado K, Kono T. Mitochondrial dynamics controlled by mitofusins define organelle positioning and movement during mouse oocyte maturation. Mol Hum Reprod. 2014;20:1090–1100.
   PubMed Web of Science ®Google Scholar
• Huang S-T, Bi K-W, Kuo H-M, et al. Phyllanthus urinaria induces mitochondrial dysfunction in human osteosarcoma 143B cells associated with modulation of mitochondrial fission/fusion proteins. Mitochondrion. 2014;17:22–33.
   PubMed Web of Science ®Google Scholar
• Otera H, Ishihara N, Mihara K. New insights into the function and regulation of mitochondrial fission. Biochim Biophys Acta. 2013;1833:1256–1268.
   PubMed Web of Science ®Google Scholar
• Onoue K, Jofuku A, Ban-Ishihara R, et al. Fis1 acts as a mitochondrial recruitment factor for TBC1D15 that is involved in regulation of mitochondrial morphology. J Cell Sci. 2013;126:176–185.
   PubMed Web of Science ®Google Scholar
• Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim Biophys Acta. 2012;1817:1833–1838.
   PubMed Web of Science ®Google Scholar
• Chen H, Chan DC. Mitochondrial dynamics – fusion, fission, movement, and mitophagy – in neurodegenerative diseases. Hum Mol Genet. 2009;18:R169–R176.
   PubMed Web of Science ®Google Scholar
• Elgass K, Pakay J, Ryan MT, Palmer CS. Recent advances into the understanding of mitochondrial fission. Recent advances into the understanding of mitochondrial fission. Biochim Biophys Acta. 2013;1833:150–161.
   PubMed Web of Science ®Google Scholar
• Santos D, Cardoso SM. Mitochondrial dynamics and neuronal fate in Parkinson’s disease. Mitochondrion. 2012;12:428–437.
   PubMed Web of Science ®Google Scholar
• Ishihara N, Otera H, Oka T, Mihara K. Regulation and physiologic functions of GTPases in mitochondrial fusion and fission in mammals. Antioxid Redox Signal. 2013;1;19:389–399.
   Google Scholar
• Cui T, Fan C, Gu L, et al. Silencing of PINK1 induces mitophagy via mitochondrial permeability transition in dopaminergic MN9D cells. Silencing of PINK1 induces mitophagy via mitochondrial permeability transition in dopaminergic MN9D cells. Brain Res. 2011;1394:1–13.
   PubMed Web of Science ®Google Scholar
• Tanik SA, Schultheiss CE, Volpicelli-Daley LA, et al. Lewy body-like alpha-synuclein aggregates resist degradation and impair macroautophagy. J Biol Chem. 2013;288:15194–15210.
   PubMed Web of Science ®Google Scholar
• Liu K, Shi N, Sun Y, et al. Therapeutic effects of rapamycin on MPTP-induced Parkinsonism in mice. Neurochem Res. 2013;38:201–207.
   PubMed Web of Science ®Google Scholar
• Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci. 2012;125:795–799.
   PubMed Web of Science ®Google Scholar
• Gelmetti V, De Rosa P, Torosantucci L, et al. PINK1 and BECN1 relocalize at mitochondria-associated membranes during mitophagy and promote ER-mitochondria tethering and autophagosome formation. Autophagy. 2017;13:654–669.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4:151–175.
   PubMed Web of Science ®Google Scholar
• Polson HEJ, de Lartigue J, Rigden DJ, et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy. 2010;6:506–522.
   PubMed Web of Science ®Google Scholar
• Park S, Choi S-G, Yoo S-M, et al. Choline dehydrogenase interacts with SQSTM1/p62 to recruit LC3 and stimulate mitophagy. Autophagy. 2014;10:1906–1920.
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;1;19:5720–5728.
   Google Scholar
• Tai H, Wang Z, Gong H, et al. Autophagy impairment with lysosomal and mitochondrial dysfunction is an important characteristic of oxidative stress-induced senescence. Autophagy. 2017;13:99–113.
   PubMed Web of Science ®Google Scholar
• Bjørkøy G, Lamark T, Pankiv S, et al. Monitoring autophagic degradation of p62/SQSTM1. Meth Enzymol. 2009;452:181–197.
   PubMed Web of Science ®Google Scholar
• Zhang C, Yuan X, Hu Z, et al. Valproic acid protects primary dopamine neurons from MPP+-induced neurotoxicity: involvement of GSK3β phosphorylation by Akt and ERK through the mitochondrial intrinsic apoptotic pathway. Valproic acid protects primary dopamine neurons from MPP+-induced neurotoxicity: involvement of GSK3beta phosphorylation by Akt and ERK through the mitochondrial intrinsic apoptotic pathway. BioMed Res Int. 2017;2017:1.
   Web of Science ®Google Scholar
• Nafar F, Clarke JP, Mearow KM. Coconut oil protects cortical neurons from amyloid beta toxicity by enhancing signaling of cell survival pathways. Neurochem Int. 2017;105:64–79.
   PubMed Web of Science ®Google Scholar
• Caglayan B, Caglayan AB, Beker MC, et al. Evidence that activation of P2X7R does not exacerbate neuronal death after optic nerve transection and focal cerebral ischemia in mice. Exp Neurol. 2017;29;296:23–31.
   Google Scholar
• Sun J, Ren D-D, Wan J-Y, et al. Desensitizing mitochondrial permeability transition by ERK-cyclophilin D Axis contributes to the neuroprotective effect of gallic acid against cerebral ischemia/reperfusion injury. Front Pharmacol. 2017;8:184.
   PubMed Web of Science ®Google Scholar
• Martinez-Lopez N, Athonvarangkul D, Mishall P, et al. Autophagy proteins regulate ERK phosphorylation. Nat Commun. 2013;4:2799.
   PubMed Web of Science ®Google Scholar
• Park K-J, Lee S-H, Lee C-H, et al. Upregulation of Beclin-1 expression and phosphorylation of Bcl-2 and p53 are involved in the JNK-mediated autophagic cell death. Biochem Biophys Res Commun. 2009;382:726–729.
   PubMed Web of Science ®Google Scholar
• Wei Y, Pattingre S, Sinha S, et al. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30:678–688.
   PubMed Web of Science ®Google Scholar
• Brunet A, Sweeney LB, Sturgill JF, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011–2015.
   PubMed Web of Science ®Google Scholar
• Salminen A, Kaarniranta KK. SIRT1: regulation of longevity via autophagy. Cell Signal. 2009;21:1356–1360.
   PubMed Web of Science ®Google Scholar
• Mazucanti C, Cabral-Costa J, Vasconcelos A, et al. Longevity pathways (mTOR, SIRT, insulin/IGF-1) as key modulatory targets on aging and neurodegeneration. CTMC. 2015;15:2116–2138.
   Google Scholar
• Finkel T. The metabolic regulation of aging. Nat Med. 2015;21:1416–1423.
   PubMed Web of Science ®Google Scholar
• Liou CW, Chuang JH, Chen JB, et al. Mitochondrial DNA variants as genetic risk factors for Parkinson disease. Eur J Neurol. 2016;23:1289–1300.
   PubMed Web of Science ®Google Scholar
• Zhao X, Wang J, Hu S, et al. Neuroprotective effect of resveratrol on rotenone-treated C57BL/6 mice. Neuroreport. 2017;28:498–505.
   PubMed Web of Science ®Google Scholar
• Goussetis DJ, Altman JK, Glaser H, et al. Autophagy is a critical mechanism for the induction of the antileukemic effects of arsenic trioxide. J Biol Chem. 2010;285:29989–29997.
   PubMed Web of Science ®Google Scholar
• Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol. 2008;445:77–88.
   PubMedGoogle Scholar
• Zhou YY, Li Y, Jiang WQ, et al. MAPK/JNK signalling: a potential autophagy regulation pathway. Biosci Rep. 2015;35(3).
   Google Scholar
• D'Orsi B, Mateyka J, Prehn JHM. Control of mitochondrial physiology and cell death by the Bcl-2 family proteins Bax and Bok. Neurochem Int. 2017;109:162–170.
   PubMed Web of Science ®Google Scholar
• Eisenberg-Lerner A, Bialik S, Simon H-U, et al. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ. 2009;16:966–975.
   PubMed Web of Science ®Google Scholar
• Albani D, Polito L, Signorini A, et al. Neuroprotective properties of resveratrol in different neurodegenerative disorders. Biofactors. 2010;36:370–376.
   PubMed Web of Science ®Google Scholar
• Lu M, Su C, Qiao C, et al. Metformin prevents dopaminergic neuron death in MPTP/P-induced mouse model of Parkinson’s disease via autophagy and mitochondrial ROS clearance. IJNPPY. 2016;19:pyw047.
   Google Scholar
• Chance B, Cohen P, Jobsis F, et al. Intracellular oxidation–reduction states in vivo. Science. 1962;137:499–508.
   PubMed Web of Science ®Google Scholar
• Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. 2014;94:909–950.
   PubMed Web of Science ®Google Scholar
• Bhattacharjee N, Borah A. Oxidative stress and mitochondrial dysfunction are the underlying events of dopaminergic neurodegeneration in homocysteine rat model of Parkinson’s disease. Neurochem Int. 2016;101:48–55.
   PubMed Web of Science ®Google Scholar
• Cho D-H, Nakamura T, Fang J, et al. Nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science. 2009;324:102–105.
   PubMed Web of Science ®Google Scholar
• Büeler H. Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson’s disease. Exp Neurol. 2009;218:235–246.
   PubMed Web of Science ®Google Scholar
• Von Stockum S, Nardin A, Schrepfer E, et al. Mitochondrial dynamics and mitophagy in Parkinson’s disease: a fly point of view. Neurobiol Dis. 2016;90:58–67.
   PubMed Web of Science ®Google Scholar
• Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science. 2012;337:1062–1065.
   PubMed Web of Science ®Google Scholar
• Rambold AS, Kostelecky B, Elia N, et al. Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci USA. 2011;108:10190–10195.
   PubMed Web of Science ®Google Scholar
• Twig G, Elorza A, Molina AJA, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27:433–446.
   PubMed Web of Science ®Google Scholar
• Rusten TE, Stenmark H. p62, an autophagy hero or culprit? Nat Cell Biol. 2010;12:207–209.
   PubMed Web of Science ®Google Scholar
• Roy B, Pattanaik AK, Das J, et al. Role of PI3K/Akt/mTOR and MEK/ERK pathway in concanavalin A induced autophagy in HeLa cells. Chem Biol Interact. 2014;210:96–102.
   PubMed Web of Science ®Google Scholar
• Mun-Ock K, Hyun-Sun L, Young-Won C, et al. Gartanin induces autophagy through JNK activation which extenuates caspase-dependent apoptosis. Oncol Rep. 2015;34:139–146.
   PubMed Web of Science ®Google Scholar
• Shinojima N, Yokoyama T, Kondo Y, et al. Roles of the Akt/mTOR/p70s6K and ERK1/2 signaling pathways in curcumin-induced autophagy. Autophagy. 2007;3:635–637.
   PubMed Web of Science ®Google Scholar
• Wang J, Whiteman MW, Lian H, et al. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J Biol Chem. 2009;284:21412–21424.
   PubMed Web of Science ®Google Scholar
• Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signaling for suicide and survival. J Cell Physiol. 2002;192:1–15.
   PubMed Web of Science ®Google Scholar
• Matos TJ, Duarte CB, Gonçalo M, et al. Role of oxidative stress in ERK and p38 MAPK activation induced by the chemical sensitizer DNFB in a fetal skin dendritic cell line. Immunol Cell Biol. 2005;83:607–614.
   PubMed Web of Science ®Google Scholar
• Son Y, Cheong Y-K, Kim N-H, et al. Mitogen-activated protein kinases and reactive oxygen species: How can ROS activate MAPK pathways? J Signal Transduct. 2011;2011:1.
   Google Scholar