Drp-1 dependent mitochondrial fragmentation and protective autophagy in dopaminergic SH-SY5Y cells overexpressing alpha-synuclein

Parkinson's disease is a neurodegenerative movement disorder caused by the loss of dopaminergic neurons from substantia nigra. It is characterized by the accumulation of aggregated α-synuclein as the major component of the Lewy bodies. Additional common features of this disease are the mitochon...

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Autor principal: Martinez, J.H
Otros Autores: Alaimo, A., Gorojod, R.M, Porte Alcon, S., Fuentes, F., Coluccio Leskow, F., Kotler, M.L
Formato: Capítulo de libro
Lenguaje:Inglés
Publicado: Academic Press Inc. 2018
Acceso en línea:Registro en Scopus
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024 7 |2 scopus  |a 2-s2.0-85041563990 
024 7 |2 cas  |a alpha synuclein, 154040-18-3; guanosine triphosphatase, 9059-32-9; alpha-Synuclein; DNM1L protein, human; GTP Phosphohydrolases; Microtubule-Associated Proteins; Mitochondrial Proteins; OPA1 protein, human; SNCA protein, human 
040 |a Scopus  |b spa  |c AR-BaUEN  |d AR-BaUEN 
030 |a MOCNE 
100 1 |a Martinez, J.H. 
245 1 0 |a Drp-1 dependent mitochondrial fragmentation and protective autophagy in dopaminergic SH-SY5Y cells overexpressing alpha-synuclein 
260 |b Academic Press Inc.  |c 2018 
270 1 0 |m Kotler, M.L.; Ciudad Universitaria, Avda. Intendente Güiraldes 2160, Argentina; email: kotler@qb.fcen.uba.ar 
506 |2 openaire  |e Política editorial 
504 |a Alaimo, A., Gorojod, R.M., Kotler, M.L., The extrinsic and intrinsic apoptotic pathways are involved in manganese toxicity in rat astrocytoma C6 cells (2011) Neurochem. Int., 59, pp. 297-308 
504 |a Alaimo, A., Gorojod, R.M., Beauquis, J., Muñoz, M.J., Saravia, F., Kotler, M.L., Deregulation of mitochondria-shaping proteins Opa-1 and Drp-1 in manganese-induced apoptosis (2014) PLoS One, 9 
504 |a Ashrafi, G., Schwarz, T.L., The pathways of mitophagy for quality control and clearance of mitochondria (2013) Cell Death Differ., 20, pp. 31-42 
504 |a Bido, S., Soria, F.N., Fan, R.Z., Bezard, E., Tieu, K., Mitochondrial division inhibitor-1 is neuroprotective in the A53T-α-synuclein rat model of Parkinson's disease (2017) Sci. Rep., 7 
504 |a Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding (1976) Anal. Biochem., 72, pp. 248-254 
504 |a Campello, S., Scorrano, L., Mitochondrial shape changes: orchestrating cell pathophysiology (2010) EMBO Rep., 11, pp. 678-684 
504 |a Cassidy-Stone, A., Chipuk, J.E., Ingerman, E., Song, C., Yoo, C., Kuwana, T., Kurth, M.J., Nunnari, J., Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization (2008) Dev. Cell, 14, pp. 193-204 
504 |a Chan, D.C., Fusion and fission: interlinked processes critical for mitochondrial health (2012) Annu. Rev. Genet., 46, pp. 265-287 
504 |a Choubey, V., Safiulina, D., Vaarmann, A., Cagalinec, M., Wareski, P., Kuum, M., Zharkovsky, A., Kaasik, A., Mutant A53T alpha-synuclein induces neuronal death by increasing mitochondrial autophagy (2011) J. Biol. Chem., 286, pp. 10814-10824 
504 |a Cieri, D., Brini, M., Calí, T., Emerging (and converging) pathways in Parkinson's disease: keeping mitochondrial wellness (2017) Biochem. Biophys. Res. Commun., 483, pp. 1020-1030 
504 |a Clark, J., Clore, E.L., Zheng, K., Adame, A., Masliah, E., Simon, D.K., Oral N-acetyl-cysteine attenuates loss of dopaminergic terminals in alpha-synuclein overexpressing mice (2010) PLoS One, 5 
504 |a Corrado, M., Scorrano, L., Campello, S., Mitochondrial dynamics in cancer and neurodegenerative and neuroinflammatory diseases (2012) Int. J. Cell Biol., 2012 
504 |a Dagda, R.K., Cherra, S.J., III, Kulich, S.M., Tandon, A., Park, D., Chu, C.T., Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission (2009) J. Biol. Chem., 284, pp. 13843-13855 
504 |a Devi, L., Raghavendran, V., Prabhu, B.M., Avadhani, N.G., Anandatheerthavarada, H.K., Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain (2008) J. Biol. Chem., 283, pp. 9089-9100 
504 |a Emadi, S., Kasturirangan, S., Wang, M.S., Schulz, P., Sierks, M.R., Detecting morphologically distinct oligomeric forms of alpha-synuclein (2009) J. Biol. Chem., 284, pp. 11048-11058 
504 |a Emmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S.D., Ntzouni, M., Margaritis, L.H., Stefanis, L., Vekrellis, K., Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival (2010) J. Neurosci., 30, pp. 6838-6851 
504 |a Esteves, A.R., Arduíno, D.M., Swerdlow, R.H., Oliveira, C.R., Cardoso, S.M., Dysfunctional mitochondria uphold calpain activation: contribution to Parkinson's disease pathology (2010) Neurobiol. Dis., 37, pp. 723-730 
504 |a Frezza, C., Cipolat, S., Martins de Brito, O., Micaroni, M., Beznoussenko, G.V., Rudka, T., Bartoli, D., Scorrano, L., OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion (2006) Cell, 126, pp. 177-189 
504 |a Friedman, L.G., Lachenmayer, M.L., Wang, J., He, L., Poulose, S.M., Komatsu, M., Holstein, G.R., Yue, Z., Disrupted autophagy leads to dopaminergic axon and dendrite degeneration and promotes presynaptic accumulation of α-synuclein and LRRK2 in the brain (2012) J. Neurosci., 32, pp. 7585-7593 
504 |a Gara, P.M.D., Garabano, N.I., Portoles, M.J.L., Moreno, M.S., Dodat, D., Casas, O.R., Gonzalez, M.C., Kotler, M.L., ROS enhancement by silicon nanoparticles in X-ray irradiated aqueous suspensions and in glioma C6 cells (2012) J. Nanopart. Res., 14 
504 |a Gomez-Lazaro, M., Bonekamp, N.A., Galindo, M.F., Jordán, J., Schrader, M., 6-Hydroxydopamine (6-OHDA) induces Drp1-dependent mitochondrial fragmentation in SH-SY5Y cells (2008) Free Radic. Biol. Med., 44, pp. 1960-1969 
504 |a Gorojod, R.M., Alaimo, A., Porte Alcon, S., Pomilio, C., Saravia, F., Kotler, M.L., The autophagic- lysosomal pathway determines the fate of glial cells under manganese- induced oxidative stress conditions (2015) Free Radic. Biol. Med., 87, pp. 237-251 
504 |a Green, D.R., Levine, B., To be or not to be? How selective autophagy and cell death govern cell fate (2014) Cell, 157, pp. 65-75 
504 |a Itoh, K., Nakamura, K., Iijima, M., Sesaki, H., Mitochondrial dynamics in neurodegeneration (2013) Trends Cell Biol., 23, pp. 64-71 
504 |a Kamp, F., Exner, N., Lutz, A.K., Wender, N., Hegermann, J., Brunner, B., Nuscher, B., Haass, C., Inhibition of mitochondrial fusion by α-synuclein is rescued by PINK1, Parkin and DJ-1 (2010) EMBO J., 29, pp. 3571-3589 
504 |a Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Guidelines for the use and interpretation of assays for monitoring autophagy (2012) Autophagy, 8, pp. 445-544 
504 |a Koch, J.C., Bitow, F., Haack, J., d'Hedouville, Z., Zhang, J.-N., Tönges, L., Michel, U., Lingor, P., Alpha-Synuclein affects neurite morphology, autophagy, vesicle transport and axonal degeneration in CNS neurons (2015) Cell Death Dis., 6 
504 |a Li, W.W., Yang, R., Guo, J.C., Ren, H.M., Zha, X.L., Cheng, J.S., Cai, D.F., Localization of alpha-synuclein to mitochondria within midbrain of mice (2007) Neuroreport, 18, pp. 1543-1546 
504 |a Liu, G., Zhang, C., Yin, J., Li, X., Cheng, F., Li, Y., Yang, H., Yu, S., alpha-Synuclein is differentially expressed in mitochondria from different rat brain regions and dose-dependently down-regulates complex I activity (2009) Neurosci. Lett., 454, pp. 187-192 
504 |a Liu, Z., Yu, Y., Li, X., Ross, C.A., Smith, W.W., Curcumin protects against A53T alpha-synuclein-induced toxicity in a PC12 inducible cell model for parkinsonism (2011) Pharmacol. Res., 63, pp. 439-444 
504 |a MacVicar, T., Mitophagy (2013) Essays Biochem., 55, pp. 93-104 
504 |a Maltecca, F., De Stefani, D., Cassina, L., Consolato, F., Wasilewski, M., Scorrano, L., Rizzuto, R., Casari, G., Respiratory dysfunction by AFG3L2 deficiency causes decreased mitochondrial calcium uptake via organellar network fragmentation (2012) Hum. Mol. Genet., 21, pp. 3858-3870 
504 |a Manders, E.M.M., Verbeek, F.J., Aten, J.A., Measurements of co-localization of objects in dual-colour confocal images (1993) J. Microsc., 169, pp. 375-382 
504 |a Manoharan, S., Guillemin, G.J., Abiramasundari, R.S., Essa, M.M., Akbar, M., Akbar, M.D., The role of reactive oxygen species in the pathogenesis of Alzheimer's disease, Parkinson's disease, and Huntington's disease: a mini review (2016) Oxidative Med. Cell. Longev., 2016 
504 |a Martínez, J.H., Fuentes, F., Vanascod, V., Álvarez, S., Alaimo, A., Cassinae, A., Coluccio-Leskow, F., Velazquez, F., Mitochondrial interaction of alpha-synuclein leads to irreversible translocation and Complex I impairment. In preparation; Mazzulli, J.R., Zunke, F., Isacson, O., Studer, L., Krainc, D., α-Synuclein-induced lysosomal dysfunction occurs through disruptions in protein trafficking in human midbrain synucleinopathy models (2016) Proc. Natl. Acad. Sci. U. S. A., 113, pp. 1931-1936 
504 |a McCoy, M.K., Cookson, M.R., Mitochondrial quality control and dynamics in Parkinson's disease (2012) Antioxid. Redox Signal., 16, pp. 869-882 
504 |a Michel, P.P., Hirsch, E.C., Hunot, S., Understanding dopaminergic cell death pathways in Parkinson disease (2016) Neuron, 90, pp. 675-691 
504 |a Nakamura, K., α-Synuclein and mitochondria: partners in crime? (2013) Neurotherapeutics, 10, pp. 391-399 
504 |a Nakamura, K., Nemani, V.M., Wallender, E.K., Kaehlcke, K., Ott, M., Edwards, R.H., Optical reporters for the conformation of alpha-synuclein reveal a specific interaction with mitochondria (2008) J. Neurosci., 28, pp. 12305-12317 
504 |a Nakamura, K., Nemani, V.M., Azarbal, F., Skibinski, G., Levy, J.M., Egami, K., Munishkina, L., Edwards, R.H., Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein (2011) J. Biol. Chem., 286, pp. 20710-20726 
504 |a Ni, H.M., Williams, J.A., Ding, W.X., Mitochondrial dynamics and mitochondrial quality control (2015) Redox Biol., 4, pp. 6-13 
504 |a Olichon, A., Emorine, L.J., Descoins, E., Pelloquin, L., Brichese, L., Gas, N., Guillou, E., Belenguer, P., The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space (2002) FEBS Lett., 523, pp. 171-176 
504 |a Park, S.W., Kim, K.Y., Lindsey, J.D., Dai, Y., Heo, H., Nguyen, D.H., Ellisman, M.H., Ju, W.-K., A selective inhibitor of drp1, mdivi-1, increases retinal ganglion cell survival in acute ischemic mouse retina (2011) Invest. Ophthalmol. Vis. Sci., 52, pp. 2837-2843 
504 |a Perfeito, R., Lázaro, D.F., Outeiro, T.F., Rego, A.C., Linking alpha-synuclein phosphorylation to reactive oxygen species formation and mitochondrial dysfunction in SH-SY5Y cells (2014) Mol. Cell. Neurosci., 62, pp. 51-59 
504 |a Pernas, L., Scorrano, L., Mito-Morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function (2016) Annu. Rev. Physiol., 78, pp. 505-531 
504 |a Ramonet, D., Perier, C., Recasens, A., Dehay, B., Bové, J., Costa, V., Scorrano, L., Vila, M., Optic atrophy 1 mediates mitochondria remodeling and dopaminergic neurodegeneration linked to complex I deficiency (2013) Cell Death Differ., 20, pp. 77-85 
504 |a Roberts, H., Brown, D., Seeking a mechanism for the toxicity of oligomeric α-Synuclein (2015) Biomol. Ther., 5, pp. 282-305 
504 |a Roberts, R.F., Tang, M.Y., Fon, E.A., Durcan, T.M., Defending the mitochondria: the pathways of mitophagy and mitochondrial-derived vesicles (2016) Int. J. Biochem. Cell Biol., 79, pp. 427-436 
504 |a Robinson, K.M., Janes, M.S., Beckman, J.S., The selective detection of mitochondrial superoxide by live cell imaging (2008) Nat. Protoc., 3, pp. 941-947 
504 |a Satoh, M., Hamamoto, T., Seo, N., Kagawa, Y., Endo, H., Differential sublocalization of the dynamin-related protein OPA1 isoforms in mitochondria (2003) Biochem. Biophys. Res. Commun., 300, pp. 482-493 
504 |a Sheridan, C., Martin, S.J., Mitochondrial fission/fusion dynamics and apoptosis (2010) Mitochondrion, 10, pp. 640-648 
504 |a Spencer, B., Potkar, R., Trejo, M., Rockenstein, E., Patrick, C., Gindi, R., Adame, A., Masliah, E., Beclin 1 gene transfer activates autophagy and ameliorates the neurodegenerative pathology in alpha-synuclein models of Parkinson's and Lewy body diseases (2009) J. Neurosci., 29, pp. 13578-13588 
504 |a Spillantini, M.G., Schmidt, M.L., Lee, V.M.Y., Trojanowski, J.Q., Jakes, R., Goedert, M., Alpha-synuclein in Lewy bodies (1997) Nature, 388, pp. 839-840 
504 |a Twig, G., Shirihai, O.S., The interplay between mitochondrial dynamics and mitophagy (2011) Antioxid. Redox Signal., 14, pp. 1939-1951 
504 |a Visanji, N.P., Brotchie, J.M., Kalia, L.V., Koprich, J.B., Tandon, A., Watts, J.C., Lang, A.E., α-Synuclein-based animal models of Parkinson's disease: challenges and opportunities in a new era (2016) Trends Neurosci., 39, pp. 750-762 
504 |a Vives-Bauza, C., Przedborski, S., Mitophagy: the latest problem for Parkinson's disease (2011) Trends Mol. Med., 17, pp. 158-165 
504 |a Wojtala, A., Bonora, M., Malinska, D., Pinton, P., Duszynski, J., Wieckowski, M.R., Methods to monitor ROS production by fluorescence microscopy and fluorometry (2014) Methods Enzymol., 542, pp. 243-262 
504 |a Xicoy, H., Wieringa, B., Martens, G.J.M., The SH-SY5Y cell line in Parkinson's disease research: a systematic review (2017) Mol. Neurodegener., 12 
504 |a Xie, W., Chung, K.K.K., Alpha-synuclein impairs normal dynamics of mitochondria in cell and animal models of Parkinson's disease (2012) J. Neurochem., 122, pp. 404-414 
504 |a Xie, H., Hu, L., Li, G., SH-SY5Y human neuroblastoma cell line: in vitro cell model of dopaminergic neurons in Parkinson's disease (2010) Chin. Med. J., 123, pp. 1086-1092 
504 |a Xie, W., Wan, O.W., Chung, K.K.K., New insights into the role of mitochondrial dysfunction and protein aggregation in Parkinson's disease (2010) Biochim. Biophys. Acta, 1802, pp. 935-941 
504 |a Xilouri, M., Vogiatzi, T., Vekrellis, K., Park, D., Stefanis, L., Abberant alpha-synuclein confers toxicity to neurons in part through inhibition of chaperone-mediated autophagy (2009) PLoS One, 4 
504 |a Xilouri, M., Brekk, O.R., Stefanis, L., Autophagy and alpha-Synuclein: relevance to Parkinson's disease and related Synucleopathies (2016) Mov. Disord., 31, pp. 178-192 
504 |a Yamaguchi, R., Lartigue, L., Perkins, G., Scott, R.T., Dixit, A., Kushnareva, Y., Kuwana, T., Newmeyer, D.D., Opa1-mediated cristae opening is Bax/Bak and BH3 dependent, required for apoptosis, and independent of Bak oligomerization (2008) Mol. Cell, 31, pp. 557-569 
504 |a Zorzano, A., Claret, M., Implications of mitochondrial dynamics on neurodegeneration and on hypothalamic dysfunction (2015) Front. Aging Neurosci., 7 
520 3 |a Parkinson's disease is a neurodegenerative movement disorder caused by the loss of dopaminergic neurons from substantia nigra. It is characterized by the accumulation of aggregated α-synuclein as the major component of the Lewy bodies. Additional common features of this disease are the mitochondrial dysfunction and the activation/inhibition of autophagy both events associated to the intracellular accumulation of α-synuclein. The mechanism by which these events contribute to neural degeneration remains unknown. In the present work we investigated the effect of α-synuclein on mitochondrial dynamics and autophagy/mitophagy in SH-SY5Y cells, an in vitro model of Parkinson disease. We demonstrated that overexpression of wild type α-synuclein causes moderated toxicity, ROS generation and mitochondrial dysfunction. In addition, α-synuclein induces the mitochondrial fragmentation on a Drp-1-dependent fashion. Overexpression of the fusion protein Opa-1 prevented both mitochondrial fragmentation and cytotoxicity. On the other hand, cells expressing α-synuclein showed activated autophagy and particularly mitophagy. Employing a genetic strategy we demonstrated that autophagy is triggered in order to protect cells from α-synuclein-induced cell death. Our results clarify the role of Opa-1 and Drp-1 in mitochondrial dynamics and cell survival, a controversial α-synuclein research issue. The findings presented point to the relevance of mitochondrial homeostasis and autophagy in the pathogenesis of PD. Better understanding of the molecular interaction between these processes could give rise to novel therapeutic methods for PD prevention and amelioration. © 2018 Elsevier Inc.  |l eng 
536 |a Detalles de la financiación: Consejo Nacional de Investigaciones Científicas y Técnicas, CONICET 
536 |a Detalles de la financiación: UBACyT 2014, 0573, 20020130200025BA, PIP No. 0356, 0519, 0771 
536 |a Detalles de la financiación: This work was supported by grants from the Consejo Nacional de Investigaciones Científicas y Técnicas ( CONICET PIP No. 0356 , No. 0771 , No. 0519 and No.0573 ) and UBACyT 2014–2017 No. 20020130200025BA . We thank Dr. Tom Jovin (Max Planck Institute for Biophysical Chemistry, Göttingen, Germany) for providing relevant materials. JHM, RMG and SPA are supported by CONICET scholarships. FF is a member of CPA at CONICET. AA, FCL and MLK are researchers at CONICET. 
593 |a CONICET- Universidad de Buenos Aires, Instituto de Química Biológica Ciencias Exactas y Naturales (IQUIBICEN), Facultad de Ciencias Exactas y Naturales, Departamento de Química Biológica, Laboratorio Interdisciplinario de Dinámica Celular y Nanoherramientas, Argentina 
593 |a CONICET- Universidad de Buenos Aires, Instituto de Química Biológica Ciencias Exactas y Naturales (IQUIBICEN), Facultad de Ciencias Exactas y Naturales, Departamento de Química Biológica, Laboratorio de Disfunción Celular en Enfermedades Neurodegenerativas y Nanomedicina, Buenos Aires, Argentina 
593 |a Instituto de Medicina Experimental (IMEX)-CONICET, Academia Nacional de Medicina, Buenos Aires, Argentina 
690 1 0 |a ALPHA-SYNUCLEIN 
690 1 0 |a AUTOPHAGY 
690 1 0 |a MITOCHONDRIA 
690 1 0 |a MITOCHONDRIAL DYNAMICS 
690 1 0 |a MITOPHAGY 
690 1 0 |a PARKINSON'S DISEASE 
690 1 0 |a ALPHA SYNUCLEIN 
690 1 0 |a DYNAMIN RELATED PROTEIN 1 
690 1 0 |a HYBRID PROTEIN 
690 1 0 |a MITOCHONDRIAL PROTEIN 
690 1 0 |a OPTIC ATROPHY 1 PROTEIN 
690 1 0 |a REACTIVE OXYGEN METABOLITE 
690 1 0 |a UNCLASSIFIED DRUG 
690 1 0 |a ALPHA SYNUCLEIN 
690 1 0 |a DNM1L PROTEIN, HUMAN 
690 1 0 |a GUANOSINE TRIPHOSPHATASE 
690 1 0 |a MICROTUBULE ASSOCIATED PROTEIN 
690 1 0 |a MITOCHONDRIAL PROTEIN 
690 1 0 |a OPA1 PROTEIN, HUMAN 
690 1 0 |a SNCA PROTEIN, HUMAN 
690 1 0 |a ARTICLE 
690 1 0 |a AUTOPHAGY 
690 1 0 |a CELL DEATH 
690 1 0 |a CELL PROTECTION 
690 1 0 |a CELL SURVIVAL 
690 1 0 |a CELL VIABILITY 
690 1 0 |a CONTROLLED STUDY 
690 1 0 |a CYTOTOXICITY 
690 1 0 |a DISORDERS OF MITOCHONDRIAL FUNCTIONS 
690 1 0 |a DOPAMINERGIC NERVE CELL 
690 1 0 |a GENE OVEREXPRESSION 
690 1 0 |a HUMAN 
690 1 0 |a HUMAN CELL 
690 1 0 |a IN VITRO STUDY 
690 1 0 |a MITOCHONDRIAL DYNAMICS 
690 1 0 |a MITOCHONDRIAL FRAGMENTATION 
690 1 0 |a MITOPHAGY 
690 1 0 |a PARKINSON DISEASE 
690 1 0 |a PRIORITY JOURNAL 
690 1 0 |a SH-SY5Y CELL LINE 
690 1 0 |a WILD TYPE 
690 1 0 |a AUTOPHAGY 
690 1 0 |a DOPAMINERGIC NERVE CELL 
690 1 0 |a GENETICS 
690 1 0 |a METABOLISM 
690 1 0 |a MITOCHONDRION 
690 1 0 |a PHYSIOLOGY 
690 1 0 |a SUBSTANTIA NIGRA 
690 1 0 |a TUMOR CELL LINE 
690 1 0 |a ALPHA-SYNUCLEIN 
690 1 0 |a AUTOPHAGY 
690 1 0 |a CELL LINE, TUMOR 
690 1 0 |a DOPAMINERGIC NEURONS 
690 1 0 |a GTP PHOSPHOHYDROLASES 
690 1 0 |a HUMANS 
690 1 0 |a MICROTUBULE-ASSOCIATED PROTEINS 
690 1 0 |a MITOCHONDRIA 
690 1 0 |a MITOCHONDRIAL DEGRADATION 
690 1 0 |a MITOCHONDRIAL DYNAMICS 
690 1 0 |a MITOCHONDRIAL PROTEINS 
690 1 0 |a PARKINSON DISEASE 
690 1 0 |a SUBSTANTIA NIGRA 
700 1 |a Alaimo, A. 
700 1 |a Gorojod, R.M. 
700 1 |a Porte Alcon, S. 
700 1 |a Fuentes, F. 
700 1 |a Coluccio Leskow, F. 
700 1 |a Kotler, M.L. 
773 0 |d Academic Press Inc., 2018  |g v. 88  |h pp. 107-117  |p Mol. Cell. Neurosci.  |x 10447431  |w (AR-BaUEN)CENRE-6139  |t Molecular and Cellular Neuroscience 
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