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Erschienen in: NeuroMolecular Medicine 2-3/2017

15.06.2017 | Original Paper

Individual Amino Acid Supplementation Can Improve Energy Metabolism and Decrease ROS Production in Neuronal Cells Overexpressing Alpha-Synuclein

verfasst von: Vedad Delic, Jeddidiah W. D. Griffin, Sandra Zivkovic, Yumeng Zhang, Tam-Anh Phan, Henry Gong, Dale Chaput, Christian Reynes, Vinh B. Dinh, Josean Cruz, Eni Cvitkovic, Devon Placides, Ernide Frederic, Hamed Mirzaei, Stanley M. Stevens Jr., Umesh Jinwal, Daniel C. Lee, Patrick C. Bradshaw

Erschienen in: NeuroMolecular Medicine | Ausgabe 2-3/2017

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Abstract

Parkinson’s disease (PD) is a neurodegenerative disorder characterized by alpha-synuclein accumulation and loss of dopaminergic neurons in the substantia nigra (SN) region of the brain. Increased levels of alpha-synuclein have been shown to result in loss of mitochondrial electron transport chain complex I activity leading to increased reactive oxygen species (ROS) production. WT alpha-synuclein was stably overexpressed in human BE(2)-M17 neuroblastoma cells resulting in increased levels of an alpha-synuclein multimer, but no increase in alpha-synuclein monomer levels. Oxygen consumption was decreased by alpha-synuclein overexpression, but ATP levels did not decrease and ROS levels did not increase. Treatment with ferrous sulfate, a ROS generator, resulted in decreased oxygen consumption in both control and alpha-synuclein overexpressing cells. However, this treatment only decreased ATP levels and increased ROS production in the cells overexpressing alpha-synuclein. Similarly, paraquat, another ROS generator, decreased ATP levels in the alpha-synuclein overexpressing cells, but not in the control cells, further demonstrating how alpha-synuclein sensitized the cells to oxidative insult. Proteomic analysis yielded molecular insights into the cellular adaptations to alpha-synuclein overexpression, such as the increased abundance of many mitochondrial proteins. Many amino acids and citric acid cycle intermediates and their ester forms were individually supplemented to the cells with l-serine, l-proline, l-aspartate, or l-glutamine decreasing ROS production in oxidatively stressed alpha-synuclein overexpressing cells, while diethyl oxaloacetate or l-valine supplementation increased ATP levels. These results suggest that dietary supplementation with individual metabolites could yield bioenergetic improvements in PD patients to delay loss of dopaminergic neurons.
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Literatur
Zurück zum Zitat Andres, D., Keyser, B. M., Petrali, J., Benton, B., Hubbard, K. S., McNutt, P. M., et al. (2013). Morphological and functional differentiation in BE(2)-M17 human neuroblastoma cells by treatment with trans-retinoic acid. BMC Neuroscience, 14, 49.PubMedPubMedCentralCrossRef Andres, D., Keyser, B. M., Petrali, J., Benton, B., Hubbard, K. S., McNutt, P. M., et al. (2013). Morphological and functional differentiation in BE(2)-M17 human neuroblastoma cells by treatment with trans-retinoic acid. BMC Neuroscience, 14, 49.PubMedPubMedCentralCrossRef
Zurück zum Zitat Ayton, S., & Lei, P. (2014). Nigral iron elevation is an invariable feature of Parkinson’s disease and is a sufficient cause of neurodegeneration. BioMed Research International, 2014, 581256.PubMedPubMedCentralCrossRef Ayton, S., & Lei, P. (2014). Nigral iron elevation is an invariable feature of Parkinson’s disease and is a sufficient cause of neurodegeneration. BioMed Research International, 2014, 581256.PubMedPubMedCentralCrossRef
Zurück zum Zitat Balu, D. T., Hoshaw, B. A., Malberg, J. E., Rosenzweig-Lipson, S., Schechter, L. E., & Lucki, I. (2008). Differential regulation of central BDNF protein levels by antidepressant and non-antidepressant drug treatments. Brain Research, 1211, 37–43.PubMedPubMedCentralCrossRef Balu, D. T., Hoshaw, B. A., Malberg, J. E., Rosenzweig-Lipson, S., Schechter, L. E., & Lucki, I. (2008). Differential regulation of central BDNF protein levels by antidepressant and non-antidepressant drug treatments. Brain Research, 1211, 37–43.PubMedPubMedCentralCrossRef
Zurück zum Zitat Bartels, T., Choi, J. G., & Selkoe, D. J. (2011). Alpha-synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature, 477(7362), 107–110.PubMedPubMedCentralCrossRef Bartels, T., Choi, J. G., & Selkoe, D. J. (2011). Alpha-synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature, 477(7362), 107–110.PubMedPubMedCentralCrossRef
Zurück zum Zitat Beal, M. F. (2007). Mitochondria and neurodegeneration. Novartis Foundation Symposium, 287, 183–192. (discussion 192–186).PubMedCrossRef Beal, M. F. (2007). Mitochondria and neurodegeneration. Novartis Foundation Symposium, 287, 183–192. (discussion 192–186).PubMedCrossRef
Zurück zum Zitat Binukumar, B. K., Bal, A., Kandimalla, R. J., & Gill, K. D. (2010). Nigrostriatal neuronal death following chronic dichlorvos exposure: Crosstalk between mitochondrial impairments, alpha synuclein aggregation, oxidative damage and behavioral changes. Molecular Brain, 3, 35.PubMed Binukumar, B. K., Bal, A., Kandimalla, R. J., & Gill, K. D. (2010). Nigrostriatal neuronal death following chronic dichlorvos exposure: Crosstalk between mitochondrial impairments, alpha synuclein aggregation, oxidative damage and behavioral changes. Molecular Brain, 3, 35.PubMed
Zurück zum Zitat Bisaglia, M., Greggio, E., Maric, D., Miller, D. W., Cookson, M. R., & Bubacco, L. (2010). Alpha-synuclein overexpression increases dopamine toxicity in BE2-M17 cells. BMC Neuroscience, 11, 41.PubMedPubMedCentralCrossRef Bisaglia, M., Greggio, E., Maric, D., Miller, D. W., Cookson, M. R., & Bubacco, L. (2010). Alpha-synuclein overexpression increases dopamine toxicity in BE2-M17 cells. BMC Neuroscience, 11, 41.PubMedPubMedCentralCrossRef
Zurück zum Zitat Bourdenx, M., Bezard, E., & Dehay, B. (2014). Lysosomes and alpha-synuclein form a dangerous duet leading to neuronal cell death. Frontiers in Neuroanatomy, 8, 83.PubMedPubMedCentralCrossRef Bourdenx, M., Bezard, E., & Dehay, B. (2014). Lysosomes and alpha-synuclein form a dangerous duet leading to neuronal cell death. Frontiers in Neuroanatomy, 8, 83.PubMedPubMedCentralCrossRef
Zurück zum Zitat Bromme, H. J., Zuhlke, L., Silber, R. E., & Simm, A. (2008). DCFH2 interactions with hydroxyl radicals and other oxidants—Influence of organic solvents. Experimental Gerontology, 43(7), 638–644.PubMedCrossRef Bromme, H. J., Zuhlke, L., Silber, R. E., & Simm, A. (2008). DCFH2 interactions with hydroxyl radicals and other oxidants—Influence of organic solvents. Experimental Gerontology, 43(7), 638–644.PubMedCrossRef
Zurück zum Zitat Caioli, S., Candelotti, E., Pedersen, J. Z., Saba, L., Antonini, A., Incerpi, S., et al. (2016). Baicalein reverts l-valine-induced persistent sodium current up-modulation in primary cortical neurons. Biochimica et Biophysica Acta, 1862(4), 566–575.PubMedCrossRef Caioli, S., Candelotti, E., Pedersen, J. Z., Saba, L., Antonini, A., Incerpi, S., et al. (2016). Baicalein reverts l-valine-induced persistent sodium current up-modulation in primary cortical neurons. Biochimica et Biophysica Acta, 1862(4), 566–575.PubMedCrossRef
Zurück zum Zitat Cannon, J. R., Geghman, K. D., Tapias, V., Sew, T., Dail, M. K., Li, C., et al. (2013). Expression of human E46K-mutated alpha-synuclein in BAC-transgenic rats replicates early-stage Parkinson’s disease features and enhances vulnerability to mitochondrial impairment. Experimental Neurology, 240, 44–56.PubMedCrossRef Cannon, J. R., Geghman, K. D., Tapias, V., Sew, T., Dail, M. K., Li, C., et al. (2013). Expression of human E46K-mutated alpha-synuclein in BAC-transgenic rats replicates early-stage Parkinson’s disease features and enhances vulnerability to mitochondrial impairment. Experimental Neurology, 240, 44–56.PubMedCrossRef
Zurück zum Zitat Carvalho, K. M., De-Laurenzi, V., Melino, G., & Cohen, P. (1993). Human neuroblastoma cells express a novel metallo-endopeptidase activity able to inactivate atrial natriuretic factor: Inhibition during retinoic acid-induced differentiation. Brazilian Journal of Medical and Biological Research, 26(11), 1181–1186.PubMed Carvalho, K. M., De-Laurenzi, V., Melino, G., & Cohen, P. (1993). Human neuroblastoma cells express a novel metallo-endopeptidase activity able to inactivate atrial natriuretic factor: Inhibition during retinoic acid-induced differentiation. Brazilian Journal of Medical and Biological Research, 26(11), 1181–1186.PubMed
Zurück zum Zitat Caudal, D., Alvarsson, A., Bjorklund, A., & Svenningsson, P. (2015). Depressive-like phenotype induced by AAV-mediated overexpression of human alpha-synuclein in midbrain dopaminergic neurons. Experimental Neurology, 273, 243–252.PubMedCrossRef Caudal, D., Alvarsson, A., Bjorklund, A., & Svenningsson, P. (2015). Depressive-like phenotype induced by AAV-mediated overexpression of human alpha-synuclein in midbrain dopaminergic neurons. Experimental Neurology, 273, 243–252.PubMedCrossRef
Zurück zum Zitat Chaput, D., Kirouac, L. H., Bell-Temin, H., Stevens, S. M., Jr., & Padmanabhan, J. (2012). SILAC-based proteomic analysis to investigate the impact of amyloid precursor protein expression in neuronal-like B103 cells. Electrophoresis, 33(24), 3728–3737.PubMedPubMedCentralCrossRef Chaput, D., Kirouac, L. H., Bell-Temin, H., Stevens, S. M., Jr., & Padmanabhan, J. (2012). SILAC-based proteomic analysis to investigate the impact of amyloid precursor protein expression in neuronal-like B103 cells. Electrophoresis, 33(24), 3728–3737.PubMedPubMedCentralCrossRef
Zurück zum Zitat Chatterjee, S., Mizar, P., Cassel, R., Neidl, R., Selvi, B. R., Mohankrishna, D. V., et al. (2013). A novel activator of CBP/p300 acetyltransferases promotes neurogenesis and extends memory duration in adult mice. Journal of Neuroscience, 33(26), 10698–10712.PubMedCrossRef Chatterjee, S., Mizar, P., Cassel, R., Neidl, R., Selvi, B. R., Mohankrishna, D. V., et al. (2013). A novel activator of CBP/p300 acetyltransferases promotes neurogenesis and extends memory duration in adult mice. Journal of Neuroscience, 33(26), 10698–10712.PubMedCrossRef
Zurück zum Zitat Chen, L., Xie, Z., Turkson, S., & Zhuang, X. (2015). A53T human alpha-synuclein overexpression in transgenic mice induces pervasive mitochondria macroautophagy defects preceding dopamine neuron degeneration. Journal of Neuroscience, 35(3), 890–905.PubMedCrossRef Chen, L., Xie, Z., Turkson, S., & Zhuang, X. (2015). A53T human alpha-synuclein overexpression in transgenic mice induces pervasive mitochondria macroautophagy defects preceding dopamine neuron degeneration. Journal of Neuroscience, 35(3), 890–905.PubMedCrossRef
Zurück zum Zitat Chiba-Falek, O., & Nussbaum, R. L. (2001). Effect of allelic variation at the NACP-Rep1 repeat upstream of the alpha-synuclein gene (SNCA) on transcription in a cell culture luciferase reporter system. Human Molecular Genetics, 10(26), 3101–3109.PubMedCrossRef Chiba-Falek, O., & Nussbaum, R. L. (2001). Effect of allelic variation at the NACP-Rep1 repeat upstream of the alpha-synuclein gene (SNCA) on transcription in a cell culture luciferase reporter system. Human Molecular Genetics, 10(26), 3101–3109.PubMedCrossRef
Zurück zum Zitat Cohen, G., Farooqui, R., & Kesler, N. (1997). Parkinson disease: A new link between monoamine oxidase and mitochondrial electron flow. Proceedings of the National Academy of Sciences, 94(10), 4890–4894.CrossRef Cohen, G., Farooqui, R., & Kesler, N. (1997). Parkinson disease: A new link between monoamine oxidase and mitochondrial electron flow. Proceedings of the National Academy of Sciences, 94(10), 4890–4894.CrossRef
Zurück zum Zitat Cole, N. B., Murphy, D. D., Lebowitz, J., Di Noto, L., Levine, R. L., & Nussbaum, R. L. (2005). Metal-catalyzed oxidation of alpha-synuclein: Helping to define the relationship between oligomers, protofibrils, and filaments. Journal of Biological Chemistry, 280(10), 9678–9690.PubMedCrossRef Cole, N. B., Murphy, D. D., Lebowitz, J., Di Noto, L., Levine, R. L., & Nussbaum, R. L. (2005). Metal-catalyzed oxidation of alpha-synuclein: Helping to define the relationship between oligomers, protofibrils, and filaments. Journal of Biological Chemistry, 280(10), 9678–9690.PubMedCrossRef
Zurück zum Zitat Dalfo, E., Portero-Otin, M., Ayala, V., Martinez, A., Pamplona, R., & Ferrer, I. (2005). Evidence of oxidative stress in the neocortex in incidental Lewy body disease. Journal of Neuropathology and Experimental Neurology, 64(9), 816–830.PubMedCrossRef Dalfo, E., Portero-Otin, M., Ayala, V., Martinez, A., Pamplona, R., & Ferrer, I. (2005). Evidence of oxidative stress in the neocortex in incidental Lewy body disease. Journal of Neuropathology and Experimental Neurology, 64(9), 816–830.PubMedCrossRef
Zurück zum Zitat De Zutter, G. S., & Davis, R. J. (2001). Pro-apoptotic gene expression mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Proceedings of the National Academy of Sciences, 98(11), 6168–6173.CrossRef De Zutter, G. S., & Davis, R. J. (2001). Pro-apoptotic gene expression mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Proceedings of the National Academy of Sciences, 98(11), 6168–6173.CrossRef
Zurück zum Zitat Denton, R. M., Rutter, G. A., Midgley, P. J., & McCormack, J. G. (1988). Effects of Ca2+ on the activities of the calcium-sensitive dehydrogenases within the mitochondria of mammalian tissues. Journal of Cardiovascular Pharmacology, 12(Suppl 5), S69–S72.PubMedCrossRef Denton, R. M., Rutter, G. A., Midgley, P. J., & McCormack, J. G. (1988). Effects of Ca2+ on the activities of the calcium-sensitive dehydrogenases within the mitochondria of mammalian tissues. Journal of Cardiovascular Pharmacology, 12(Suppl 5), S69–S72.PubMedCrossRef
Zurück zum Zitat Dettmer, U., Newman, A. J., Soldner, F., Luth, E. S., Kim, N. C., von Saucken, V. E., et al. (2015). Parkinson-causing alpha-synuclein missense mutations shift native tetramers to monomers as a mechanism for disease initiation. Nature Communications, 6, 7314.PubMedPubMedCentralCrossRef Dettmer, U., Newman, A. J., Soldner, F., Luth, E. S., Kim, N. C., von Saucken, V. E., et al. (2015). Parkinson-causing alpha-synuclein missense mutations shift native tetramers to monomers as a mechanism for disease initiation. Nature Communications, 6, 7314.PubMedPubMedCentralCrossRef
Zurück zum Zitat Devi, L., Raghavendran, V., Prabhu, B. M., Avadhani, N. G., & Anandatheerthavarada, H. K. (2008). Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. Journal of Biological Chemistry, 283(14), 9089–9100.PubMedPubMedCentralCrossRef Devi, L., Raghavendran, V., Prabhu, B. M., Avadhani, N. G., & Anandatheerthavarada, H. K. (2008). Mitochondrial import and accumulation of alpha-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain. Journal of Biological Chemistry, 283(14), 9089–9100.PubMedPubMedCentralCrossRef
Zurück zum Zitat Di Maio, R., Barrett, P. J., Hoffman, E. K., Barrett, C. W., Zharikov, A., Borah, A., et al. (2016). Alpha-synuclein binds to TOM20 and inhibits mitochondrial protein import in Parkinson’s disease. Science Translational Medicine, 8(342), 342–378. Di Maio, R., Barrett, P. J., Hoffman, E. K., Barrett, C. W., Zharikov, A., Borah, A., et al. (2016). Alpha-synuclein binds to TOM20 and inhibits mitochondrial protein import in Parkinson’s disease. Science Translational Medicine, 8(342), 342–378.
Zurück zum Zitat Dickey, A. S., & Strack, S. (2011). PKA/AKAP1 and PP2A/Bbeta2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. Journal of Neuroscience, 31(44), 15716–15726.PubMedPubMedCentralCrossRef Dickey, A. S., & Strack, S. (2011). PKA/AKAP1 and PP2A/Bbeta2 regulate neuronal morphogenesis via Drp1 phosphorylation and mitochondrial bioenergetics. Journal of Neuroscience, 31(44), 15716–15726.PubMedPubMedCentralCrossRef
Zurück zum Zitat Edmondson, D. E. (2014). Hydrogen peroxide produced by mitochondrial monoamine oxidase catalysis: Biological implications. Current Pharmaceutical Design, 20(2), 155–160.PubMedCrossRef Edmondson, D. E. (2014). Hydrogen peroxide produced by mitochondrial monoamine oxidase catalysis: Biological implications. Current Pharmaceutical Design, 20(2), 155–160.PubMedCrossRef
Zurück zum Zitat Edwards, C., Canfield, J., Copes, N., Brito, A., Rehan, M., Lipps, D., et al. (2015). Mechanisms of amino acid-mediated lifespan extension in Caenorhabditis elegans. BMC Genetics, 16, 8.PubMedPubMedCentralCrossRef Edwards, C., Canfield, J., Copes, N., Brito, A., Rehan, M., Lipps, D., et al. (2015). Mechanisms of amino acid-mediated lifespan extension in Caenorhabditis elegans. BMC Genetics, 16, 8.PubMedPubMedCentralCrossRef
Zurück zum Zitat Elkon, H., Don, J., Melamed, E., Ziv, I., Shirvan, A., & Offen, D. (2002). Mutant and wild-type alpha-synuclein interact with mitochondrial cytochrome C oxidase. Journal of Molecular Neuroscience, 18(3), 229–238.PubMedCrossRef Elkon, H., Don, J., Melamed, E., Ziv, I., Shirvan, A., & Offen, D. (2002). Mutant and wild-type alpha-synuclein interact with mitochondrial cytochrome C oxidase. Journal of Molecular Neuroscience, 18(3), 229–238.PubMedCrossRef
Zurück zum Zitat Eschbach, J., von Einem, B., Muller, K., Bayer, H., Scheffold, A., Morrison, B. E., et al. (2015). Mutual exacerbation of peroxisome proliferator-activated receptor gamma coactivator 1alpha deregulation and alpha-synuclein oligomerization. Annals of Neurology, 77(1), 15–32.PubMedCrossRef Eschbach, J., von Einem, B., Muller, K., Bayer, H., Scheffold, A., Morrison, B. E., et al. (2015). Mutual exacerbation of peroxisome proliferator-activated receptor gamma coactivator 1alpha deregulation and alpha-synuclein oligomerization. Annals of Neurology, 77(1), 15–32.PubMedCrossRef
Zurück zum Zitat Filograna, R., Civiero, L., Ferrari, V., Codolo, G., Greggio, E., Bubacco, L., et al. (2015). Analysis of the catecholaminergic phenotype in human SH-SY5Y and BE(2)-M17 neuroblastoma cell lines upon differentiation. PLoS ONE, 10(8), e0136769.PubMedPubMedCentralCrossRef Filograna, R., Civiero, L., Ferrari, V., Codolo, G., Greggio, E., Bubacco, L., et al. (2015). Analysis of the catecholaminergic phenotype in human SH-SY5Y and BE(2)-M17 neuroblastoma cell lines upon differentiation. PLoS ONE, 10(8), e0136769.PubMedPubMedCentralCrossRef
Zurück zum Zitat Fitzgerald, J. C., Ufer, C., De Girolamo, L. A., Kuhn, H., & Billett, E. E. (2007). Monoamine oxidase-A modulates apoptotic cell death induced by staurosporine in human neuroblastoma cells. Journal of Neurochemistry, 103(6), 2189–2199.PubMedCrossRef Fitzgerald, J. C., Ufer, C., De Girolamo, L. A., Kuhn, H., & Billett, E. E. (2007). Monoamine oxidase-A modulates apoptotic cell death induced by staurosporine in human neuroblastoma cells. Journal of Neurochemistry, 103(6), 2189–2199.PubMedCrossRef
Zurück zum Zitat Fitzgerald, J. C., Ugun-Klusek, A., Allen, G., De Girolamo, L. A., Hargreaves, I., Ufer, C., et al. (2014). Monoamine oxidase-A knockdown in human neuroblastoma cells reveals protection against mitochondrial toxins. The FASEB Journal, 28(1), 218–229.PubMedCrossRef Fitzgerald, J. C., Ugun-Klusek, A., Allen, G., De Girolamo, L. A., Hargreaves, I., Ufer, C., et al. (2014). Monoamine oxidase-A knockdown in human neuroblastoma cells reveals protection against mitochondrial toxins. The FASEB Journal, 28(1), 218–229.PubMedCrossRef
Zurück zum Zitat Fong, C. S., Wu, R. M., Shieh, J. C., Chao, Y. T., Fu, Y. P., Kuao, C. L., et al. (2007). Pesticide exposure on southwestern Taiwanese with MnSOD and NQO1 polymorphisms is associated with increased risk of Parkinson’s disease. Clinica Chimica Acta, 378(1–2), 136–141.CrossRef Fong, C. S., Wu, R. M., Shieh, J. C., Chao, Y. T., Fu, Y. P., Kuao, C. L., et al. (2007). Pesticide exposure on southwestern Taiwanese with MnSOD and NQO1 polymorphisms is associated with increased risk of Parkinson’s disease. Clinica Chimica Acta, 378(1–2), 136–141.CrossRef
Zurück zum Zitat Fowler, C. J., Wiberg, A., Oreland, L., Marcusson, J., & Winblad, B. (1980). The effect of age on the activity and molecular properties of human brain monoamine oxidase. Journal of Neural Transmission, 49(1–2), 1–20.PubMedCrossRef Fowler, C. J., Wiberg, A., Oreland, L., Marcusson, J., & Winblad, B. (1980). The effect of age on the activity and molecular properties of human brain monoamine oxidase. Journal of Neural Transmission, 49(1–2), 1–20.PubMedCrossRef
Zurück zum Zitat Frohlich, C., Zschiebsch, K., Groger, V., Paarmann, K., Steffen, J., Thurm, C., et al. (2016). Activation of mitochondrial complex II-dependent respiration is beneficial for alpha-synucleinopathies. Molecular Neurobiology, 53(7), 4728–4744.PubMedCrossRef Frohlich, C., Zschiebsch, K., Groger, V., Paarmann, K., Steffen, J., Thurm, C., et al. (2016). Activation of mitochondrial complex II-dependent respiration is beneficial for alpha-synucleinopathies. Molecular Neurobiology, 53(7), 4728–4744.PubMedCrossRef
Zurück zum Zitat Fry, M., & Green, D. E. (1981). Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. Journal of Biological Chemistry, 256(4), 1874–1880.PubMed Fry, M., & Green, D. E. (1981). Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. Journal of Biological Chemistry, 256(4), 1874–1880.PubMed
Zurück zum Zitat Garcia de Yebenes, J., Yebenes, J., & Mena, M. A. (2000). Neurotrophic factors in neurodegenerative disorders: Model of Parkinson’s disease. Neurotoxicity Research, 2(2–3), 115–137.PubMedCrossRef Garcia de Yebenes, J., Yebenes, J., & Mena, M. A. (2000). Neurotrophic factors in neurodegenerative disorders: Model of Parkinson’s disease. Neurotoxicity Research, 2(2–3), 115–137.PubMedCrossRef
Zurück zum Zitat Gegg, M. E., & Schapira, A. H. (2011). PINK1-parkin-dependent mitophagy involves ubiquitination of mitofusins 1 and 2: Implications for Parkinson disease pathogenesis. Autophagy, 7(2), 243–245.PubMedPubMedCentralCrossRef Gegg, M. E., & Schapira, A. H. (2011). PINK1-parkin-dependent mitophagy involves ubiquitination of mitofusins 1 and 2: Implications for Parkinson disease pathogenesis. Autophagy, 7(2), 243–245.PubMedPubMedCentralCrossRef
Zurück zum Zitat Gibson, G. E., Kingsbury, A. E., Xu, H., Lindsay, J. G., Daniel, S., Foster, O. J., et al. (2003). Deficits in a tricarboxylic acid cycle enzyme in brains from patients with Parkinson’s disease. Neurochemistry International, 43(2), 129–135.PubMedCrossRef Gibson, G. E., Kingsbury, A. E., Xu, H., Lindsay, J. G., Daniel, S., Foster, O. J., et al. (2003). Deficits in a tricarboxylic acid cycle enzyme in brains from patients with Parkinson’s disease. Neurochemistry International, 43(2), 129–135.PubMedCrossRef
Zurück zum Zitat Goldstein, D. S., Sullivan, P., Holmes, C., Miller, G. W., Alter, S., Strong, R., et al. (2013). Determinants of buildup of the toxic dopamine metabolite DOPAL in Parkinson’s disease. Journal of Neurochemistry, 126(5), 591–603.PubMedPubMedCentralCrossRef Goldstein, D. S., Sullivan, P., Holmes, C., Miller, G. W., Alter, S., Strong, R., et al. (2013). Determinants of buildup of the toxic dopamine metabolite DOPAL in Parkinson’s disease. Journal of Neurochemistry, 126(5), 591–603.PubMedPubMedCentralCrossRef
Zurück zum Zitat Gould, N., Mor, D. E., Lightfoot, R., Malkus, K., Giasson, B., & Ischiropoulos, H. (2014). Evidence of native alpha-synuclein conformers in the human brain. Journal of Biological Chemistry, 289(11), 7929–7934.PubMedPubMedCentralCrossRef Gould, N., Mor, D. E., Lightfoot, R., Malkus, K., Giasson, B., & Ischiropoulos, H. (2014). Evidence of native alpha-synuclein conformers in the human brain. Journal of Biological Chemistry, 289(11), 7929–7934.PubMedPubMedCentralCrossRef
Zurück zum Zitat Grishina, E. V., Khaustova, Y. V., Vasilieva, A. A., & Mayevsky, E. I. (2015). Age-related peculiarities of succinate effect on induced lipid peroxidation in rat liver mitochondria. Biofizika, 60(4), 708–715.PubMed Grishina, E. V., Khaustova, Y. V., Vasilieva, A. A., & Mayevsky, E. I. (2015). Age-related peculiarities of succinate effect on induced lipid peroxidation in rat liver mitochondria. Biofizika, 60(4), 708–715.PubMed
Zurück zum Zitat Hanus, L., Shohami, E., Bab, I., & Mechoulam, R. (2014). N-Acyl amino acids and their impact on biological processes. BioFactors, 40(4), 381–388.PubMedCrossRef Hanus, L., Shohami, E., Bab, I., & Mechoulam, R. (2014). N-Acyl amino acids and their impact on biological processes. BioFactors, 40(4), 381–388.PubMedCrossRef
Zurück zum Zitat Hassel, B., Brathe, A., & Petersen, D. (2002). Cerebral dicarboxylate transport and metabolism studied with isotopically labelled fumarate, malate and malonate. Journal of Neurochemistry, 82(2), 410–419.PubMedCrossRef Hassel, B., Brathe, A., & Petersen, D. (2002). Cerebral dicarboxylate transport and metabolism studied with isotopically labelled fumarate, malate and malonate. Journal of Neurochemistry, 82(2), 410–419.PubMedCrossRef
Zurück zum Zitat Hauptmann, N., Grimsby, J., Shih, J. C., & Cadenas, E. (1996). The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Archives of Biochemistry and Biophysics, 335(2), 295–304.PubMedCrossRef Hauptmann, N., Grimsby, J., Shih, J. C., & Cadenas, E. (1996). The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Archives of Biochemistry and Biophysics, 335(2), 295–304.PubMedCrossRef
Zurück zum Zitat He, Q., Song, N., Xu, H., Wang, R., Xie, J., & Jiang, H. (2011). Alpha-synuclein aggregation is involved in the toxicity induced by ferric iron to SK-N-SH neuroblastoma cells. J Neural Transm, 118(3), 397–406.PubMedCrossRef He, Q., Song, N., Xu, H., Wang, R., Xie, J., & Jiang, H. (2011). Alpha-synuclein aggregation is involved in the toxicity induced by ferric iron to SK-N-SH neuroblastoma cells. J Neural Transm, 118(3), 397–406.PubMedCrossRef
Zurück zum Zitat Hunt, J. B., Jr., Nash, K. R., Placides, D., Moran, P., Selenica, M. L., Abuqalbeen, F., et al. (2015). Sustained arginase 1 expression modulates pathological tau deposits in a mouse model of tauopathy. Journal of Neuroscience, 35(44), 14842–14860.PubMedCrossRef Hunt, J. B., Jr., Nash, K. R., Placides, D., Moran, P., Selenica, M. L., Abuqalbeen, F., et al. (2015). Sustained arginase 1 expression modulates pathological tau deposits in a mouse model of tauopathy. Journal of Neuroscience, 35(44), 14842–14860.PubMedCrossRef
Zurück zum Zitat Jeninga, E. H., Schoonjans, K., & Auwerx, J. (2010). Reversible acetylation of PGC-1: Connecting energy sensors and effectors to guarantee metabolic flexibility. Oncogene, 29(33), 4617–4624.PubMedCrossRef Jeninga, E. H., Schoonjans, K., & Auwerx, J. (2010). Reversible acetylation of PGC-1: Connecting energy sensors and effectors to guarantee metabolic flexibility. Oncogene, 29(33), 4617–4624.PubMedCrossRef
Zurück zum Zitat Jinsmaa, Y., Sullivan, P., Gross, D., Cooney, A., Sharabi, Y., & Goldstein, D. S. (2014). Divalent metal ions enhance DOPAL-induced oligomerization of alpha-synuclein. Neuroscience Letters, 569, 27–32.PubMedPubMedCentralCrossRef Jinsmaa, Y., Sullivan, P., Gross, D., Cooney, A., Sharabi, Y., & Goldstein, D. S. (2014). Divalent metal ions enhance DOPAL-induced oligomerization of alpha-synuclein. Neuroscience Letters, 569, 27–32.PubMedPubMedCentralCrossRef
Zurück zum Zitat Katayama, S., & Mine, Y. (2007). Antioxidative activity of amino acids on tissue oxidative stress in human intestinal epithelial cell model. Journal of Agriculture and Food Chemistry, 55(21), 8458–8464.CrossRef Katayama, S., & Mine, Y. (2007). Antioxidative activity of amino acids on tissue oxidative stress in human intestinal epithelial cell model. Journal of Agriculture and Food Chemistry, 55(21), 8458–8464.CrossRef
Zurück zum Zitat Keane, P. C., Kurzawa, M., Blain, P. G., & Morris, C. M. (2011). Mitochondrial dysfunction in Parkinson’s disease. Parkinsons Disease, 2011, 716871. Keane, P. C., Kurzawa, M., Blain, P. G., & Morris, C. M. (2011). Mitochondrial dysfunction in Parkinson’s disease. Parkinsons Disease, 2011, 716871.
Zurück zum Zitat Keeney, P. M., Xie, J., Capaldi, R. A., & Bennett, J. P., Jr. (2006). Parkinson’s disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. Journal of Neuroscience, 26(19), 5256–5264.PubMedCrossRef Keeney, P. M., Xie, J., Capaldi, R. A., & Bennett, J. P., Jr. (2006). Parkinson’s disease brain mitochondrial complex I has oxidatively damaged subunits and is functionally impaired and misassembled. Journal of Neuroscience, 26(19), 5256–5264.PubMedCrossRef
Zurück zum Zitat Ko, L., Mehta, N. D., Farrer, M., Easson, C., Hussey, J., Yen, S., et al. (2000). Sensitization of neuronal cells to oxidative stress with mutated human alpha-synuclein. Journal of Neurochemistry, 75(6), 2546–2554.PubMedCrossRef Ko, L., Mehta, N. D., Farrer, M., Easson, C., Hussey, J., Yen, S., et al. (2000). Sensitization of neuronal cells to oxidative stress with mutated human alpha-synuclein. Journal of Neurochemistry, 75(6), 2546–2554.PubMedCrossRef
Zurück zum Zitat Kohno, R., Sawada, H., Kawamoto, Y., Uemura, K., Shibasaki, H., & Shimohama, S. (2004). BDNF is induced by wild-type alpha-synuclein but not by the two mutants, A30P or A53T, in glioma cell line. Biochemical and Biophysical Research Communications, 318(1), 113–118.PubMedCrossRef Kohno, R., Sawada, H., Kawamoto, Y., Uemura, K., Shibasaki, H., & Shimohama, S. (2004). BDNF is induced by wild-type alpha-synuclein but not by the two mutants, A30P or A53T, in glioma cell line. Biochemical and Biophysical Research Communications, 318(1), 113–118.PubMedCrossRef
Zurück zum Zitat Kontopoulos, E., Parvin, J. D., & Feany, M. B. (2006). Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. Human Molecular Genetics, 15(20), 3012–3023.PubMedCrossRef Kontopoulos, E., Parvin, J. D., & Feany, M. B. (2006). Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. Human Molecular Genetics, 15(20), 3012–3023.PubMedCrossRef
Zurück zum Zitat Kroe, D., Kinney, T. D., Kaufman, N., & Klavins, J. V. (1963). The influence of amino acids on iron absorption. Blood, 21, 546–552.PubMed Kroe, D., Kinney, T. D., Kaufman, N., & Klavins, J. V. (1963). The influence of amino acids on iron absorption. Blood, 21, 546–552.PubMed
Zurück zum Zitat Kumar, M. J., Nicholls, D. G., & Andersen, J. K. (2003). Oxidative alpha-ketoglutarate dehydrogenase inhibition via subtle elevations in monoamine oxidase B levels results in loss of spare respiratory capacity: Implications for Parkinson’s disease. Journal of Biological Chemistry, 278(47), 46432–46439.PubMedCrossRef Kumar, M. J., Nicholls, D. G., & Andersen, J. K. (2003). Oxidative alpha-ketoglutarate dehydrogenase inhibition via subtle elevations in monoamine oxidase B levels results in loss of spare respiratory capacity: Implications for Parkinson’s disease. Journal of Biological Chemistry, 278(47), 46432–46439.PubMedCrossRef
Zurück zum Zitat Levin, J., Hogen, T., Hillmer, A. S., Bader, B., Schmidt, F., Kamp, F., et al. (2011). Generation of ferric iron links oxidative stress to alpha-synuclein oligomer formation. Journal of Parkinson’s Disease, 1(2), 205–216.PubMed Levin, J., Hogen, T., Hillmer, A. S., Bader, B., Schmidt, F., Kamp, F., et al. (2011). Generation of ferric iron links oxidative stress to alpha-synuclein oligomer formation. Journal of Parkinson’s Disease, 1(2), 205–216.PubMed
Zurück zum Zitat Li, J., Uversky, V. N., & Fink, A. L. (2001). Effect of familial Parkinson’s disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry, 40(38), 11604–11613.PubMedCrossRef Li, J., Uversky, V. N., & Fink, A. L. (2001). Effect of familial Parkinson’s disease point mutations A30P and A53T on the structural properties, aggregation, and fibrillation of human alpha-synuclein. Biochemistry, 40(38), 11604–11613.PubMedCrossRef
Zurück zum Zitat Li, W. W., Yang, R., Guo, J. C., Ren, H. M., Zha, X. L., Cheng, J. S., et al. (2007). Localization of alpha-synuclein to mitochondria within midbrain of mice. NeuroReport, 18(15), 1543–1546.PubMedCrossRef Li, W. W., Yang, R., Guo, J. C., Ren, H. M., Zha, X. L., Cheng, J. S., et al. (2007). Localization of alpha-synuclein to mitochondria within midbrain of mice. NeuroReport, 18(15), 1543–1546.PubMedCrossRef
Zurück zum Zitat Liu, L., Peritore, C., Ginsberg, J., Shih, J., Arun, S., & Donmez, G. (2015). Protective role of SIRT5 against motor deficit and dopaminergic degeneration in MPTP-induced mice model of Parkinson’s disease. Behavioural Brain Research, 281, 215–221.PubMedCrossRef Liu, L., Peritore, C., Ginsberg, J., Shih, J., Arun, S., & Donmez, G. (2015). Protective role of SIRT5 against motor deficit and dopaminergic degeneration in MPTP-induced mice model of Parkinson’s disease. Behavioural Brain Research, 281, 215–221.PubMedCrossRef
Zurück zum Zitat Ludtmann, M. H., Angelova, P. R., Ninkina, N. N., Gandhi, S., Buchman, V. L., & Abramov, A. Y. (2016). Monomeric alpha-synuclein exerts a physiological role on brain ATP synthase. Journal of Neuroscience, 36(41), 10510–10521.PubMedPubMedCentralCrossRef Ludtmann, M. H., Angelova, P. R., Ninkina, N. N., Gandhi, S., Buchman, V. L., & Abramov, A. Y. (2016). Monomeric alpha-synuclein exerts a physiological role on brain ATP synthase. Journal of Neuroscience, 36(41), 10510–10521.PubMedPubMedCentralCrossRef
Zurück zum Zitat Luth, E. S., Bartels, T., Dettmer, U., Kim, N. C., & Selkoe, D. J. (2015). Purification of alpha-synuclein from human brain reveals an instability of endogenous multimers as the protein approaches purity. Biochemistry, 54(2), 279–292.PubMedCrossRef Luth, E. S., Bartels, T., Dettmer, U., Kim, N. C., & Selkoe, D. J. (2015). Purification of alpha-synuclein from human brain reveals an instability of endogenous multimers as the protein approaches purity. Biochemistry, 54(2), 279–292.PubMedCrossRef
Zurück zum Zitat Luth, E. S., Stavrovskaya, I. G., Bartels, T., Kristal, B. S., & Selkoe, D. J. (2014). Soluble, prefibrillar alpha-synuclein oligomers promote complex I-dependent, Ca2+-induced mitochondrial dysfunction. Journal of Biological Chemistry, 289(31), 21490–21507.PubMedPubMedCentralCrossRef Luth, E. S., Stavrovskaya, I. G., Bartels, T., Kristal, B. S., & Selkoe, D. J. (2014). Soluble, prefibrillar alpha-synuclein oligomers promote complex I-dependent, Ca2+-induced mitochondrial dysfunction. Journal of Biological Chemistry, 289(31), 21490–21507.PubMedPubMedCentralCrossRef
Zurück zum Zitat Mallajosyula, J. K., Kaur, D., Chinta, S. J., Rajagopalan, S., Rane, A., Nicholls, D. G., et al. (2008). MAO-B elevation in mouse brain astrocytes results in Parkinson’s pathology. PLoS ONE, 3(2), e1616.PubMedPubMedCentralCrossRef Mallajosyula, J. K., Kaur, D., Chinta, S. J., Rajagopalan, S., Rane, A., Nicholls, D. G., et al. (2008). MAO-B elevation in mouse brain astrocytes results in Parkinson’s pathology. PLoS ONE, 3(2), e1616.PubMedPubMedCentralCrossRef
Zurück zum Zitat Maraganore, D. M., de Andrade, M., Elbaz, A., Farrer, M. J., Ioannidis, J. P., Kruger, R., et al. (2006). Collaborative analysis of alpha-synuclein gene promoter variability and Parkinson disease. JAMA, 296(6), 661–670.PubMedCrossRef Maraganore, D. M., de Andrade, M., Elbaz, A., Farrer, M. J., Ioannidis, J. P., Kruger, R., et al. (2006). Collaborative analysis of alpha-synuclein gene promoter variability and Parkinson disease. JAMA, 296(6), 661–670.PubMedCrossRef
Zurück zum Zitat Markham, A., Bains, R., Franklin, P., & Spedding, M. (2014). Changes in mitochondrial function are pivotal in neurodegenerative and psychiatric disorders: How important is BDNF? British Journal of Pharmacology, 171(8), 2206–2229.PubMedPubMedCentralCrossRef Markham, A., Bains, R., Franklin, P., & Spedding, M. (2014). Changes in mitochondrial function are pivotal in neurodegenerative and psychiatric disorders: How important is BDNF? British Journal of Pharmacology, 171(8), 2206–2229.PubMedPubMedCentralCrossRef
Zurück zum Zitat Markham, A., Cameron, I., Franklin, P., & Spedding, M. (2004). BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II. European Journal of Neuroscience, 20(5), 1189–1196.PubMedCrossRef Markham, A., Cameron, I., Franklin, P., & Spedding, M. (2004). BDNF increases rat brain mitochondrial respiratory coupling at complex I, but not complex II. European Journal of Neuroscience, 20(5), 1189–1196.PubMedCrossRef
Zurück zum Zitat Martin, L. J., Pan, Y., Price, A. C., Sterling, W., Copeland, N. G., Jenkins, N. A., et al. (2006). Parkinson’s disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. Journal of Neuroscience, 26(1), 41–50.PubMedCrossRef Martin, L. J., Pan, Y., Price, A. C., Sterling, W., Copeland, N. G., Jenkins, N. A., et al. (2006). Parkinson’s disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. Journal of Neuroscience, 26(1), 41–50.PubMedCrossRef
Zurück zum Zitat Martin, F. L., Williamson, S. J., Paleologou, K. E., Hewitt, R., El-Agnaf, O. M., & Allsop, D. (2003). Fe(II)-induced DNA damage in alpha-synuclein-transfected human dopaminergic BE(2)-M17 neuroblastoma cells: Detection by the Comet assay. Journal of Neurochemistry, 87(3), 620–630.PubMedCrossRef Martin, F. L., Williamson, S. J., Paleologou, K. E., Hewitt, R., El-Agnaf, O. M., & Allsop, D. (2003). Fe(II)-induced DNA damage in alpha-synuclein-transfected human dopaminergic BE(2)-M17 neuroblastoma cells: Detection by the Comet assay. Journal of Neurochemistry, 87(3), 620–630.PubMedCrossRef
Zurück zum Zitat Martinez, T. N., & Greenamyre, J. T. (2012). Toxin models of mitochondrial dysfunction in Parkinson’s disease. Antioxidants & Redox Signaling, 16(9), 920–934.CrossRef Martinez, T. N., & Greenamyre, J. T. (2012). Toxin models of mitochondrial dysfunction in Parkinson’s disease. Antioxidants & Redox Signaling, 16(9), 920–934.CrossRef
Zurück zum Zitat Marttila, R. J., Lorentz, H., & Rinne, U. K. (1988). Oxygen toxicity protecting enzymes in Parkinson’s disease. Increase of superoxide dismutase-like activity in the substantia nigra and basal nucleus. Journal of the Neurological Sciences, 86(2–3), 321–331.PubMedCrossRef Marttila, R. J., Lorentz, H., & Rinne, U. K. (1988). Oxygen toxicity protecting enzymes in Parkinson’s disease. Increase of superoxide dismutase-like activity in the substantia nigra and basal nucleus. Journal of the Neurological Sciences, 86(2–3), 321–331.PubMedCrossRef
Zurück zum Zitat Mena, N. P., Urrutia, P. J., Lourido, F., Carrasco, C. M., & Nunez, M. T. (2015). Mitochondrial iron homeostasis and its dysfunctions in neurodegenerative disorders. Mitochondrion, 21, 92–105.PubMedCrossRef Mena, N. P., Urrutia, P. J., Lourido, F., Carrasco, C. M., & Nunez, M. T. (2015). Mitochondrial iron homeostasis and its dysfunctions in neurodegenerative disorders. Mitochondrion, 21, 92–105.PubMedCrossRef
Zurück zum Zitat Mogi, M., Togari, A., Kondo, T., Mizuno, Y., Komure, O., Kuno, S., et al. (1999). Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson’s disease. Neuroscience Letters, 270(1), 45–48.PubMedCrossRef Mogi, M., Togari, A., Kondo, T., Mizuno, Y., Komure, O., Kuno, S., et al. (1999). Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson’s disease. Neuroscience Letters, 270(1), 45–48.PubMedCrossRef
Zurück zum Zitat Murer, M. G., Yan, Q., & Raisman-Vozari, R. (2001). Brain-derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Progress in Neurobiology, 63(1), 71–124.PubMedCrossRef Murer, M. G., Yan, Q., & Raisman-Vozari, R. (2001). Brain-derived neurotrophic factor in the control human brain, and in Alzheimer’s disease and Parkinson’s disease. Progress in Neurobiology, 63(1), 71–124.PubMedCrossRef
Zurück zum Zitat Musgrove, R. E., King, A. E., & Dickson, T. C. (2011). Neuroprotective upregulation of endogenous alpha-synuclein precedes ubiquitination in cultured dopaminergic neurons. Neurotoxicity Research, 19(4), 592–602.PubMedCrossRef Musgrove, R. E., King, A. E., & Dickson, T. C. (2011). Neuroprotective upregulation of endogenous alpha-synuclein precedes ubiquitination in cultured dopaminergic neurons. Neurotoxicity Research, 19(4), 592–602.PubMedCrossRef
Zurück zum Zitat Nalls, M. A., Plagnol, V., Hernandez, D. G., Sharma, M., Sheerin, U. M., Saad, M., et al. (2011). Imputation of sequence variants for identification of genetic risks for Parkinson’s disease: A meta-analysis of genome-wide association studies. Lancet, 377(9766), 641–649.PubMedCrossRef Nalls, M. A., Plagnol, V., Hernandez, D. G., Sharma, M., Sheerin, U. M., Saad, M., et al. (2011). Imputation of sequence variants for identification of genetic risks for Parkinson’s disease: A meta-analysis of genome-wide association studies. Lancet, 377(9766), 641–649.PubMedCrossRef
Zurück zum Zitat Negida, A., Menshawy, A., El Ashal, G., Elfouly, Y., Hani, Y., Hegazy, Y., et al. (2016). Coenzyme Q10 for patients with Parkinson’s disease: A systematic review and meta-analysis. CNS & Neurological Disorders: Drug Targets, 15(1), 45–53.CrossRef Negida, A., Menshawy, A., El Ashal, G., Elfouly, Y., Hani, Y., Hegazy, Y., et al. (2016). Coenzyme Q10 for patients with Parkinson’s disease: A systematic review and meta-analysis. CNS & Neurological Disorders: Drug Targets, 15(1), 45–53.CrossRef
Zurück zum Zitat Olmos, Y., Valle, I., Borniquel, S., Tierrez, A., Soria, E., Lamas, S., et al. (2009). Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. Journal of Biological Chemistry, 284(21), 14476–14484.PubMedPubMedCentralCrossRef Olmos, Y., Valle, I., Borniquel, S., Tierrez, A., Soria, E., Lamas, S., et al. (2009). Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. Journal of Biological Chemistry, 284(21), 14476–14484.PubMedPubMedCentralCrossRef
Zurück zum Zitat Ostrerova-Golts, N., Petrucelli, L., Hardy, J., Lee, J. M., Farer, M., & Wolozin, B. (2000). The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. Journal of Neuroscience, 20(16), 6048–6054.PubMed Ostrerova-Golts, N., Petrucelli, L., Hardy, J., Lee, J. M., Farer, M., & Wolozin, B. (2000). The A53T alpha-synuclein mutation increases iron-dependent aggregation and toxicity. Journal of Neuroscience, 20(16), 6048–6054.PubMed
Zurück zum Zitat Pacheco, C. R., Morales, C. N., Ramirez, A. E., Munoz, F. J., Gallegos, S. S., Caviedes, P. A., et al. (2015). Extracellular alpha-synuclein alters synaptic transmission in brain neurons by perforating the neuronal plasma membrane. Journal of Neurochemistry, 132(6), 731–741.PubMedCrossRef Pacheco, C. R., Morales, C. N., Ramirez, A. E., Munoz, F. J., Gallegos, S. S., Caviedes, P. A., et al. (2015). Extracellular alpha-synuclein alters synaptic transmission in brain neurons by perforating the neuronal plasma membrane. Journal of Neurochemistry, 132(6), 731–741.PubMedCrossRef
Zurück zum Zitat Parihar, M. S., Parihar, A., Fujita, M., Hashimoto, M., & Ghafourifar, P. (2009). Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells. International Journal of Biochemistry & Cell Biology, 41(10), 2015–2024.CrossRef Parihar, M. S., Parihar, A., Fujita, M., Hashimoto, M., & Ghafourifar, P. (2009). Alpha-synuclein overexpression and aggregation exacerbates impairment of mitochondrial functions by augmenting oxidative stress in human neuroblastoma cells. International Journal of Biochemistry & Cell Biology, 41(10), 2015–2024.CrossRef
Zurück zum Zitat Perfeito, R., Lazaro, D. F., Outeiro, T. F., & Rego, A. C. (2014). Linking alpha-synuclein phosphorylation to reactive oxygen species formation and mitochondrial dysfunction in SH-SY5Y cells. Molecular and Cellular Neuroscience, 62, 51–59.PubMedCrossRef Perfeito, R., Lazaro, D. F., Outeiro, T. F., & Rego, A. C. (2014). Linking alpha-synuclein phosphorylation to reactive oxygen species formation and mitochondrial dysfunction in SH-SY5Y cells. Molecular and Cellular Neuroscience, 62, 51–59.PubMedCrossRef
Zurück zum Zitat Perfeito, R., Ribeiro, M., & Rego, A. C. (2017). Alpha-synuclein-induced oxidative stress correlates with altered superoxide dismutase and glutathione synthesis in human neuroblastoma SH-SY5Y cells. Archives of Toxicology, 91(3), 1245–1259.PubMedCrossRef Perfeito, R., Ribeiro, M., & Rego, A. C. (2017). Alpha-synuclein-induced oxidative stress correlates with altered superoxide dismutase and glutathione synthesis in human neuroblastoma SH-SY5Y cells. Archives of Toxicology, 91(3), 1245–1259.PubMedCrossRef
Zurück zum Zitat Poeggeler, B., Sambamurti, K., Siedlak, S. L., Perry, G., Smith, M. A., & Pappolla, M. A. (2010). A novel endogenous indole protects rodent mitochondria and extends rotifer lifespan. PLoS ONE, 5(4), e10206.PubMedPubMedCentralCrossRef Poeggeler, B., Sambamurti, K., Siedlak, S. L., Perry, G., Smith, M. A., & Pappolla, M. A. (2010). A novel endogenous indole protects rodent mitochondria and extends rotifer lifespan. PLoS ONE, 5(4), e10206.PubMedPubMedCentralCrossRef
Zurück zum Zitat Porritt, M. J., Batchelor, P. E., & Howells, D. W. (2005). Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Experimental Neurology, 192(1), 226–234.PubMedCrossRef Porritt, M. J., Batchelor, P. E., & Howells, D. W. (2005). Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Experimental Neurology, 192(1), 226–234.PubMedCrossRef
Zurück zum Zitat Possel, H., Noack, H., Augustin, W., Keilhoff, G., & Wolf, G. (1997). 2,7-Dihydrodichlorofluorescein diacetate as a fluorescent marker for peroxynitrite formation. FEBS Letters, 416(2), 175–178.PubMedCrossRef Possel, H., Noack, H., Augustin, W., Keilhoff, G., & Wolf, G. (1997). 2,7-Dihydrodichlorofluorescein diacetate as a fluorescent marker for peroxynitrite formation. FEBS Letters, 416(2), 175–178.PubMedCrossRef
Zurück zum Zitat Protter, D., Lang, C., & Cooper, A. A. (2012). Alpha-synuclein and mitochondrial dysfunction: A pathogenic partnership in Parkinson’s disease? Parkinsons Disease, 2012, 829207. Protter, D., Lang, C., & Cooper, A. A. (2012). Alpha-synuclein and mitochondrial dysfunction: A pathogenic partnership in Parkinson’s disease? Parkinsons Disease, 2012, 829207.
Zurück zum Zitat Pryde, K. R., Taanman, J. W., & Schapira, A. H. (2016). A LON-ClpP proteolytic axis degrades complex I to extinguish ROS production in depolarized mitochondria. Cell Reports, 17(10), 2522–2531.PubMedPubMedCentralCrossRef Pryde, K. R., Taanman, J. W., & Schapira, A. H. (2016). A LON-ClpP proteolytic axis degrades complex I to extinguish ROS production in depolarized mitochondria. Cell Reports, 17(10), 2522–2531.PubMedPubMedCentralCrossRef
Zurück zum Zitat Radunovic, A., Porto, W. G., Zeman, S., & Leigh, P. N. (1997). Increased mitochondrial superoxide dismutase activity in Parkinson’s disease but not amyotrophic lateral sclerosis motor cortex. Neuroscience Letters, 239(2–3), 105–108.PubMedCrossRef Radunovic, A., Porto, W. G., Zeman, S., & Leigh, P. N. (1997). Increased mitochondrial superoxide dismutase activity in Parkinson’s disease but not amyotrophic lateral sclerosis motor cortex. Neuroscience Letters, 239(2–3), 105–108.PubMedCrossRef
Zurück zum Zitat Ren, Y., Jiang, H., Ma, D., Nakaso, K., & Feng, J. (2011). Parkin degrades estrogen-related receptors to limit the expression of monoamine oxidases. Human Molecular Genetics, 20(6), 1074–1083.PubMedCrossRef Ren, Y., Jiang, H., Ma, D., Nakaso, K., & Feng, J. (2011). Parkin degrades estrogen-related receptors to limit the expression of monoamine oxidases. Human Molecular Genetics, 20(6), 1074–1083.PubMedCrossRef
Zurück zum Zitat Rettig, W. J., Spengler, B. A., Chesa, P. G., Old, L. J., & Biedler, J. L. (1987). Coordinate changes in neuronal phenotype and surface antigen expression in human neuroblastoma cell variants. Cancer Research, 47(5), 1383–1389.PubMed Rettig, W. J., Spengler, B. A., Chesa, P. G., Old, L. J., & Biedler, J. L. (1987). Coordinate changes in neuronal phenotype and surface antigen expression in human neuroblastoma cell variants. Cancer Research, 47(5), 1383–1389.PubMed
Zurück zum Zitat Riley, B. E., Gardai, S. J., Emig-Agius, D., Bessarabova, M., Ivliev, A. E., Schule, B., et al. (2014). Systems-based analyses of brain regions functionally impacted in Parkinson’s disease reveals underlying causal mechanisms. PLoS ONE, 9(8), e102909.PubMedPubMedCentralCrossRef Riley, B. E., Gardai, S. J., Emig-Agius, D., Bessarabova, M., Ivliev, A. E., Schule, B., et al. (2014). Systems-based analyses of brain regions functionally impacted in Parkinson’s disease reveals underlying causal mechanisms. PLoS ONE, 9(8), e102909.PubMedPubMedCentralCrossRef
Zurück zum Zitat Robakis, D., & Fahn, S. (2015). Defining the role of the monoamine oxidase-B inhibitors for Parkinson’s disease. CNS Drugs, 29(6), 433–441.PubMedCrossRef Robakis, D., & Fahn, S. (2015). Defining the role of the monoamine oxidase-B inhibitors for Parkinson’s disease. CNS Drugs, 29(6), 433–441.PubMedCrossRef
Zurück zum Zitat Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., et al. (2016). Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell, 167(6), 1469.e1412–1480.e1412.CrossRef Sampson, T. R., Debelius, J. W., Thron, T., Janssen, S., Shastri, G. G., Ilhan, Z. E., et al. (2016). Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson’s disease. Cell, 167(6), 1469.e1412–1480.e1412.CrossRef
Zurück zum Zitat Sanchez-Ramos, J. R., Hefti, F., & Weiner, W. J. (1987). Paraquat and Parkinson’s disease. Neurology, 37(4), 728.PubMedCrossRef Sanchez-Ramos, J. R., Hefti, F., & Weiner, W. J. (1987). Paraquat and Parkinson’s disease. Neurology, 37(4), 728.PubMedCrossRef
Zurück zum Zitat Santiago, J. A., Scherzer, C. R., & Potashkin, J. A. (2014). Network analysis identifies SOD2 mRNA as a potential biomarker for Parkinson’s disease. PLoS ONE, 9(10), e109042.PubMedPubMedCentralCrossRef Santiago, J. A., Scherzer, C. R., & Potashkin, J. A. (2014). Network analysis identifies SOD2 mRNA as a potential biomarker for Parkinson’s disease. PLoS ONE, 9(10), e109042.PubMedPubMedCentralCrossRef
Zurück zum Zitat Satpute, R., Lomash, V., Kaushal, M., & Bhattacharya, R. (2013). Neuroprotective effects of alpha-ketoglutarate and ethyl pyruvate against motor dysfunction and oxidative changes caused by repeated 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine exposure in mice. Human and Experimental Toxicology, 32(7), 747–758.PubMedCrossRef Satpute, R., Lomash, V., Kaushal, M., & Bhattacharya, R. (2013). Neuroprotective effects of alpha-ketoglutarate and ethyl pyruvate against motor dysfunction and oxidative changes caused by repeated 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine exposure in mice. Human and Experimental Toxicology, 32(7), 747–758.PubMedCrossRef
Zurück zum Zitat Schneider, L., Giordano, S., Zelickson, B. R., Johnson, M. S., Benavides, G. A., Ouyang, X., et al. (2011). Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radical Biology and Medicine, 51(11), 2007–2017.PubMedPubMedCentralCrossRef Schneider, L., Giordano, S., Zelickson, B. R., Johnson, M. S., Benavides, G. A., Ouyang, X., et al. (2011). Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radical Biology and Medicine, 51(11), 2007–2017.PubMedPubMedCentralCrossRef
Zurück zum Zitat Shen, J., Du, T., Wang, X., Duan, C., Gao, G., Zhang, J., et al. (2014). alpha-Synuclein amino terminus regulates mitochondrial membrane permeability. Brain Research, 1591, 14–26.PubMedCrossRef Shen, J., Du, T., Wang, X., Duan, C., Gao, G., Zhang, J., et al. (2014). alpha-Synuclein amino terminus regulates mitochondrial membrane permeability. Brain Research, 1591, 14–26.PubMedCrossRef
Zurück zum Zitat Shimoda-Matsubayashi, S., Hattori, T., Matsumine, H., Shinohara, A., Yoritaka, A., Mori, H., et al. (1997). Mn SOD activity and protein in a patient with chromosome 6-linked autosomal recessive Parkinsonism in comparison with Parkinson’s disease and control. Neurology, 49(5), 1257–1262.PubMedCrossRef Shimoda-Matsubayashi, S., Hattori, T., Matsumine, H., Shinohara, A., Yoritaka, A., Mori, H., et al. (1997). Mn SOD activity and protein in a patient with chromosome 6-linked autosomal recessive Parkinsonism in comparison with Parkinson’s disease and control. Neurology, 49(5), 1257–1262.PubMedCrossRef
Zurück zum Zitat Shrivastava, A. N., Redeker, V., Fritz, N., Pieri, L., Almeida, L. G., Spolidoro, M., et al. (2015). alpha-synuclein assemblies sequester neuronal alpha3-Na+/K+-ATPase and impair Na+ gradient. EMBO Journal, 34(19), 2408–2423.PubMedPubMedCentralCrossRef Shrivastava, A. N., Redeker, V., Fritz, N., Pieri, L., Almeida, L. G., Spolidoro, M., et al. (2015). alpha-synuclein assemblies sequester neuronal alpha3-Na+/K+-ATPase and impair Na+ gradient. EMBO Journal, 34(19), 2408–2423.PubMedPubMedCentralCrossRef
Zurück zum Zitat Siddiqui, A., Chinta, S. J., Mallajosyula, J. K., Rajagopolan, S., Hanson, I., Rane, A., et al. (2012a). Selective binding of nuclear alpha-synuclein to the PGC1alpha promoter under conditions of oxidative stress may contribute to losses in mitochondrial function: Implications for Parkinson’s disease. Free Radical Biology and Medicine, 53(4), 993–1003.PubMedPubMedCentralCrossRef Siddiqui, A., Chinta, S. J., Mallajosyula, J. K., Rajagopolan, S., Hanson, I., Rane, A., et al. (2012a). Selective binding of nuclear alpha-synuclein to the PGC1alpha promoter under conditions of oxidative stress may contribute to losses in mitochondrial function: Implications for Parkinson’s disease. Free Radical Biology and Medicine, 53(4), 993–1003.PubMedPubMedCentralCrossRef
Zurück zum Zitat Siddiqui, A., Hanson, I., & Andersen, J. K. (2012b). Mao-B elevation decreases Parkin’s ability to efficiently clear damaged mitochondria: Protective effects of rapamycin. Free Radical Research, 46(8), 1011–1018.PubMedPubMedCentralCrossRef Siddiqui, A., Hanson, I., & Andersen, J. K. (2012b). Mao-B elevation decreases Parkin’s ability to efficiently clear damaged mitochondria: Protective effects of rapamycin. Free Radical Research, 46(8), 1011–1018.PubMedPubMedCentralCrossRef
Zurück zum Zitat Stichel, C. C., Zhu, X. R., Bader, V., Linnartz, B., Schmidt, S., & Lubbert, H. (2007). Mono- and double-mutant mouse models of Parkinson’s disease display severe mitochondrial damage. Human Molecular Genetics, 16(20), 2377–2393.PubMedCrossRef Stichel, C. C., Zhu, X. R., Bader, V., Linnartz, B., Schmidt, S., & Lubbert, H. (2007). Mono- and double-mutant mouse models of Parkinson’s disease display severe mitochondrial damage. Human Molecular Genetics, 16(20), 2377–2393.PubMedCrossRef
Zurück zum Zitat Subramaniam, S. R., Vergnes, L., Franich, N. R., Reue, K., & Chesselet, M. F. (2014). Region specific mitochondrial impairment in mice with widespread overexpression of alpha-synuclein. Neurobiology of Diseases, 70, 204–213.CrossRef Subramaniam, S. R., Vergnes, L., Franich, N. R., Reue, K., & Chesselet, M. F. (2014). Region specific mitochondrial impairment in mice with widespread overexpression of alpha-synuclein. Neurobiology of Diseases, 70, 204–213.CrossRef
Zurück zum Zitat Taylor, E. B., & Rutter, J. (2011). Mitochondrial quality control by the ubiquitin-proteasome system. Biochemical Society Transactions, 39(5), 1509–1513.PubMedCrossRef Taylor, E. B., & Rutter, J. (2011). Mitochondrial quality control by the ubiquitin-proteasome system. Biochemical Society Transactions, 39(5), 1509–1513.PubMedCrossRef
Zurück zum Zitat Thakur, P., & Nehru, B. (2015). Inhibition of neuroinflammation and mitochondrial dysfunctions by carbenoxolone in the rotenone model of Parkinson’s disease. Molecular Neurobiology, 51(1), 209–219.PubMedCrossRef Thakur, P., & Nehru, B. (2015). Inhibition of neuroinflammation and mitochondrial dysfunctions by carbenoxolone in the rotenone model of Parkinson’s disease. Molecular Neurobiology, 51(1), 209–219.PubMedCrossRef
Zurück zum Zitat Thiessen, A., Schmidt, M. M., & Dringen, R. (2010). Fumaric acid dialkyl esters deprive cultured rat oligodendroglial cells of glutathione and upregulate the expression of heme oxygenase 1. Neuroscience Letters, 475(1), 56–60.PubMedCrossRef Thiessen, A., Schmidt, M. M., & Dringen, R. (2010). Fumaric acid dialkyl esters deprive cultured rat oligodendroglial cells of glutathione and upregulate the expression of heme oxygenase 1. Neuroscience Letters, 475(1), 56–60.PubMedCrossRef
Zurück zum Zitat Toivola, D. M., Boor, P., Alam, C., & Strnad, P. (2015). Keratins in health and disease. Current Opinion in Cell Biology, 32, 73–81.PubMedCrossRef Toivola, D. M., Boor, P., Alam, C., & Strnad, P. (2015). Keratins in health and disease. Current Opinion in Cell Biology, 32, 73–81.PubMedCrossRef
Zurück zum Zitat Valerio, A., D’Antona, G., & Nisoli, E. (2011). Branched-chain amino acids, mitochondrial biogenesis, and healthspan: An evolutionary perspective. Aging, 3(5), 464–478.PubMedPubMedCentralCrossRef Valerio, A., D’Antona, G., & Nisoli, E. (2011). Branched-chain amino acids, mitochondrial biogenesis, and healthspan: An evolutionary perspective. Aging, 3(5), 464–478.PubMedPubMedCentralCrossRef
Zurück zum Zitat Ved, R., Saha, S., Westlund, B., Perier, C., Burnam, L., Sluder, A., et al. (2005). Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. Journal of Biological Chemistry, 280(52), 42655–42668.PubMedPubMedCentralCrossRef Ved, R., Saha, S., Westlund, B., Perier, C., Burnam, L., Sluder, A., et al. (2005). Similar patterns of mitochondrial vulnerability and rescue induced by genetic modification of alpha-synuclein, parkin, and DJ-1 in Caenorhabditis elegans. Journal of Biological Chemistry, 280(52), 42655–42668.PubMedPubMedCentralCrossRef
Zurück zum Zitat Wegrzyn, J., Potla, R., Chwae, Y. J., Sepuri, N. B., Zhang, Q., Koeck, T., et al. (2009). Function of mitochondrial Stat3 in cellular respiration. Science, 323(5915), 793–797.PubMedPubMedCentralCrossRef Wegrzyn, J., Potla, R., Chwae, Y. J., Sepuri, N. B., Zhang, Q., Koeck, T., et al. (2009). Function of mitochondrial Stat3 in cellular respiration. Science, 323(5915), 793–797.PubMedPubMedCentralCrossRef
Zurück zum Zitat Westlund, K. N., Denney, R. M., Rose, R. M., & Abell, C. W. (1988). Localization of distinct monoamine oxidase A and monoamine oxidase B cell populations in human brainstem. Neuroscience, 25(2), 439–456.PubMedCrossRef Westlund, K. N., Denney, R. M., Rose, R. M., & Abell, C. W. (1988). Localization of distinct monoamine oxidase A and monoamine oxidase B cell populations in human brainstem. Neuroscience, 25(2), 439–456.PubMedCrossRef
Zurück zum Zitat Wilkins, H. M., Harris, J. L., Carl, S. M., Lezi, E., Lu, J., Eva Selfridge, J., et al. (2014). Oxaloacetate activates brain mitochondrial biogenesis, enhances the insulin pathway, reduces inflammation and stimulates neurogenesis. Human Molecular Genetics, 23(24), 6528–6541.PubMedPubMedCentralCrossRef Wilkins, H. M., Harris, J. L., Carl, S. M., Lezi, E., Lu, J., Eva Selfridge, J., et al. (2014). Oxaloacetate activates brain mitochondrial biogenesis, enhances the insulin pathway, reduces inflammation and stimulates neurogenesis. Human Molecular Genetics, 23(24), 6528–6541.PubMedPubMedCentralCrossRef
Zurück zum Zitat Wilkins, H. M., Koppel, S., Carl, S. M., Ramanujan, S., Weidling, I., Michaelis, M. L., et al. (2016). Oxaloacetate enhances neuronal cell bioenergetic fluxes and infrastructure. Journal of Neurochemistry, 137(1), 76–87.PubMedPubMedCentralCrossRef Wilkins, H. M., Koppel, S., Carl, S. M., Ramanujan, S., Weidling, I., Michaelis, M. L., et al. (2016). Oxaloacetate enhances neuronal cell bioenergetic fluxes and infrastructure. Journal of Neurochemistry, 137(1), 76–87.PubMedPubMedCentralCrossRef
Zurück zum Zitat Wisniewski, J. R., Zougman, A., Nagaraj, N., & Mann, M. (2009). Universal sample preparation method for proteome analysis. Nature Methods, 6(5), 359–362.PubMedCrossRef Wisniewski, J. R., Zougman, A., Nagaraj, N., & Mann, M. (2009). Universal sample preparation method for proteome analysis. Nature Methods, 6(5), 359–362.PubMedCrossRef
Zurück zum Zitat Xilouri, M., Brekk, O. R., & Stefanis, L. (2013). Alpha-synuclein and protein degradation systems: A reciprocal relationship. Molecular Neurobiology, 47(2), 537–551.PubMedCrossRef Xilouri, M., Brekk, O. R., & Stefanis, L. (2013). Alpha-synuclein and protein degradation systems: A reciprocal relationship. Molecular Neurobiology, 47(2), 537–551.PubMedCrossRef
Zurück zum Zitat Xun, Z., Lee, D. Y., Lim, J., Canaria, C. A., Barnebey, A., Yanonne, S. M., et al. (2012). Retinoic acid-induced differentiation increases the rate of oxygen consumption and enhances the spare respiratory capacity of mitochondria in SH-SY5Y cells. Mechanisms of Ageing and Development, 133(4), 176–185.PubMedPubMedCentralCrossRef Xun, Z., Lee, D. Y., Lim, J., Canaria, C. A., Barnebey, A., Yanonne, S. M., et al. (2012). Retinoic acid-induced differentiation increases the rate of oxygen consumption and enhances the spare respiratory capacity of mitochondria in SH-SY5Y cells. Mechanisms of Ageing and Development, 133(4), 176–185.PubMedPubMedCentralCrossRef
Zurück zum Zitat Yi, X., & Kabanov, A. V. (2013). Brain delivery of proteins via their fatty acid and block copolymer modifications. Journal of Drug Targeting, 21(10), 940–955.PubMedPubMedCentralCrossRef Yi, X., & Kabanov, A. V. (2013). Brain delivery of proteins via their fatty acid and block copolymer modifications. Journal of Drug Targeting, 21(10), 940–955.PubMedPubMedCentralCrossRef
Zurück zum Zitat Youdim, M. B., & Weinstock, M. (2004). Therapeutic applications of selective and non-selective inhibitors of monoamine oxidase A and B that do not cause significant tyramine potentiation. Neurotoxicology, 25(1–2), 243–250.PubMedCrossRef Youdim, M. B., & Weinstock, M. (2004). Therapeutic applications of selective and non-selective inhibitors of monoamine oxidase A and B that do not cause significant tyramine potentiation. Neurotoxicology, 25(1–2), 243–250.PubMedCrossRef
Zurück zum Zitat Yuan, Y., Sun, J., Zhao, M., Hu, J., Wang, X., Du, G., et al. (2010). Overexpression of alpha-synuclein down-regulates BDNF expression. Cellular and Molecular Neurobiology, 30(6), 939–946.PubMedCrossRef Yuan, Y., Sun, J., Zhao, M., Hu, J., Wang, X., Du, G., et al. (2010). Overexpression of alpha-synuclein down-regulates BDNF expression. Cellular and Molecular Neurobiology, 30(6), 939–946.PubMedCrossRef
Zurück zum Zitat Zaleska, M. M., & Floyd, R. A. (1985). Regional lipid peroxidation in rat brain in vitro: Possible role of endogenous iron. Neurochemical Research, 10(3), 397–410.PubMedCrossRef Zaleska, M. M., & Floyd, R. A. (1985). Regional lipid peroxidation in rat brain in vitro: Possible role of endogenous iron. Neurochemical Research, 10(3), 397–410.PubMedCrossRef
Zurück zum Zitat Zarranz, J. J., Alegre, J., Gomez-Esteban, J. C., Lezcano, E., Ros, R., Ampuero, I., et al. (2004). The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Annals of Neurology, 55(2), 164–173.PubMedCrossRef Zarranz, J. J., Alegre, J., Gomez-Esteban, J. C., Lezcano, E., Ros, R., Ampuero, I., et al. (2004). The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Annals of Neurology, 55(2), 164–173.PubMedCrossRef
Zurück zum Zitat Zhou, G., Miura, Y., Shoji, H., Yamada, S., & Matsuishi, T. (2001). Platelet monoamine oxidase B and plasma beta-phenylethylamine in Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 70(2), 229–231.PubMedPubMedCentralCrossRef Zhou, G., Miura, Y., Shoji, H., Yamada, S., & Matsuishi, T. (2001). Platelet monoamine oxidase B and plasma beta-phenylethylamine in Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 70(2), 229–231.PubMedPubMedCentralCrossRef
Zurück zum Zitat Zhou, H. Y., Zheng, G. T., & Zhang, S. S. (1996). Effects of l-malate, an inhibitor of glutamate decarboxylase, on learning and memory in mice. Yao Xue Xue Bao, 31(12), 897–900.PubMed Zhou, H. Y., Zheng, G. T., & Zhang, S. S. (1996). Effects of l-malate, an inhibitor of glutamate decarboxylase, on learning and memory in mice. Yao Xue Xue Bao, 31(12), 897–900.PubMed
Zurück zum Zitat Zhu, M., Li, J., & Fink, A. L. (2003). The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. Journal of Biological Chemistry, 278(41), 40186–40197.PubMedCrossRef Zhu, M., Li, J., & Fink, A. L. (2003). The association of alpha-synuclein with membranes affects bilayer structure, stability, and fibril formation. Journal of Biological Chemistry, 278(41), 40186–40197.PubMedCrossRef
Metadaten
Titel
Individual Amino Acid Supplementation Can Improve Energy Metabolism and Decrease ROS Production in Neuronal Cells Overexpressing Alpha-Synuclein
verfasst von
Vedad Delic
Jeddidiah W. D. Griffin
Sandra Zivkovic
Yumeng Zhang
Tam-Anh Phan
Henry Gong
Dale Chaput
Christian Reynes
Vinh B. Dinh
Josean Cruz
Eni Cvitkovic
Devon Placides
Ernide Frederic
Hamed Mirzaei
Stanley M. Stevens Jr.
Umesh Jinwal
Daniel C. Lee
Patrick C. Bradshaw
Publikationsdatum
15.06.2017
Verlag
Springer US
Erschienen in
NeuroMolecular Medicine / Ausgabe 2-3/2017
Print ISSN: 1535-1084
Elektronische ISSN: 1559-1174
DOI
https://doi.org/10.1007/s12017-017-8448-8

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