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Fernanda Rafaela Jardim, Fhelipe Jolner Souza de Almeida, Matheus Dargesso Luckachaki, Marcos Roberto de Oliveira. Effects of sulforaphane on brain mitochondria: mechanistic view and future directions[J]. Journal of Zhejiang University Science B, 2020, 21(4): 263-279.
@article{title="Effects of sulforaphane on brain mitochondria: mechanistic view and future directions",
author="Fernanda Rafaela Jardim, Fhelipe Jolner Souza de Almeida, Matheus Dargesso Luckachaki, Marcos Roberto de Oliveira",
journal="Journal of Zhejiang University Science B",
volume="21",
number="4",
pages="263-279",
year="2020",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B1900614"
}
%0 Journal Article
%T Effects of sulforaphane on brain mitochondria: mechanistic view and future directions
%A Fernanda Rafaela Jardim
%A Fhelipe Jolner Souza de Almeida
%A Matheus Dargesso Luckachaki
%A Marcos Roberto de Oliveira
%J Journal of Zhejiang University SCIENCE B
%V 21
%N 4
%P 263-279
%@ 1673-1581
%D 2020
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B1900614
TY - JOUR
T1 - Effects of sulforaphane on brain mitochondria: mechanistic view and future directions
A1 - Fernanda Rafaela Jardim
A1 - Fhelipe Jolner Souza de Almeida
A1 - Matheus Dargesso Luckachaki
A1 - Marcos Roberto de Oliveira
J0 - Journal of Zhejiang University Science B
VL - 21
IS - 4
SP - 263
EP - 279
%@ 1673-1581
Y1 - 2020
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B1900614
Abstract: The organosulfur compound sulforaphane (SFN; C6H11NOS2) is a potent cytoprotective agent promoting antioxidant, anti-inflammatory, antiglycative, and antimicrobial effects in in vitro and in vivo experimental models. mitochondria are the major site of adenosine triphosphate (ATP) production due to the work of the oxidative phosphorylation (OXPHOS) system. They are also the main site of reactive oxygen species (ROS) production in nucleated human cells. mitochondrial impairment is central in several human diseases, including neurodegeneration and metabolic disorders. In this paper, we describe and discuss the effects and mechanisms of action by which SFN modulates mitochondrial function and dynamics in mammalian cells. mitochondria-related pro-apoptotic effects promoted by SFN in tumor cells are also discussed. SFN may be considered a cytoprotective agent, at least in part, because of the effects this organosulfur agent induces in mitochondria. Nonetheless, there are certain points that should be addressed in further experiments, indicated here as future directions, which may help researchers in this field of research.
[1]Akram M, 2014. Citric acid cycle and role of its intermediates in metabolism. Cell Biochem Biophys, 68(3):475-478.
[2]Alonso JR, Cardellach F, López S, et al., 2003. Carbon monoxide specifically inhibits cytochrome c oxidase of human mitochondrial respiratory chain. Pharmacol Toxicol, 93(3):142-146.
[3]Angeloni C, Malaguti M, Hrelia S, 2015a. Antiglycative activity of sulforaphane: a new avenue to counteract neurodegeneration? Neural Regen Res, 10(11):1750-1751.
[4]Angeloni C, Malaguti M, Rizzo B, et al., 2015b. Neuroprotective effect of sulforaphane against methylglyoxal cytotoxicity. Chem Res Toxicol, 28(6):1234-1245.
[5]Aoyama K, Nakaki T, 2013. Impaired glutathione synthesis in neurodegeneration. Int J Mol Sci, 14(10):21021-21044.
[6]Bai J, Cederbaum AI, 2001. Mitochondrial catalase and oxidative injury. Biol Signals Recept, 10(3-4):189-199.
[7]Bakala H, Hamelin M, Mary J, et al., 2012. Catalase, a target of glycation damage in rat liver mitochondria with aging. Biochim Biophys Acta, 1822(10):1527-1534.
[8]Bandy B, Davison AJ, 1987. Interactions between metals, ligands, and oxygen in the autoxidation of 6-hydroxydopamine: mechanisms by which metal chelation enhances inhibition by superoxide dismutase. Arch Biochem Biophys, 259(2):305-315.
[9]Baxter PS, Hardingham GE, 2016. Adaptive regulation of the brain’s antioxidant defences by neurons and astrocytes. Free Radic Biol Med, 100:147-152.
[10]Bazinet RP, Layé S, 2014. Polyunsaturated fatty acids and their metabolites in brain function and disease. Nat Rev Neurosci, 15(12):771-785.
[11]Beal MF, Ferrante RJ, Swartz KJ, et al., 1991. Chronic quinolinic acid lesions in rats closely resemble Huntington’s disease. J Neurosci, 11(6):1649-1659.
[12]Bedard K, Krause KH, 2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev, 87(1):245-313.
[13]Bergantin E, Quarta C, Nanni C, et al., 2014. Sulforaphane induces apoptosis in rhabdomyosarcoma and restores TRAIL-sensitivity in the aggressive alveolar subtype leading to tumor elimination in mice. Cancer Biol Ther, 15(9):1219-1225.
[14]Bi MJ, Li Q, Guo DD, et al., 2017. Sulphoraphane improves neuronal mitochondrial function in brain tissue in acute carbon monoxide poisoning rats. Basic Clin Pharmacol Toxicol, 120(6):541-549.
[15]Bigot A, Tchan MC, Thoreau B, et al., 2017. Liver involvement in urea cycle disorders: a review of the literature. J Inherit Metab Dis, 40(6):757-769.
[16]Bijangi-Vishehsaraei K, Reza Saadatzadeh M, Wang HY, et al., 2017. Sulforaphane suppresses the growth of glioblastoma cells, glioblastoma stem cell-like spheroids, and tumor xenografts through multiple cell signaling pathways. J Neurosurg, 127(6):1219-1230.
[17]Bleier L, Dröse S, 2013. Superoxide generation by complex III: from mechanistic rationales to functional consequences. Biochim Biophys Acta, 1827(11-12):1320-1331.
[18]Bordelon YM, Chesselet MF, Nelson D, et al., 1997. Energetic dysfunction in quinolinic acid-lesioned rat striatum. J Neurochem, 69(4):1629-1639.
[19]Brown GC, 1999. Nitric oxide and mitochondrial respiration. Biochim Biophys Acta, 1411(2-3):351-369.
[20]Brown GC, 2001. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta, 1504(1):46-57.
[21]Calcerrada P, Peluffo G, Radi R, 2011. Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr Pharm Des, 17(35):3905-3932.
[22]Campello S, Scorrano L, 2010. Mitochondrial shape changes: orchestrating cell pathophysiology. EMBO Rep, 11(9):678-684.
[23]Campello S, Strappazzon F, Cecconi F, 2014. Mitochondrial dismissal in mammals, from protein degradation to mitophagy. Biochim Biophys Acta, 1837(4):451-460.
[24]Cao ZB, Lindsay JG, Isaacs NW, 2007. Mitochondrial peroxiredoxins: structure and function. In: Flohé L, Harris JR (Eds.), Peroxiredoxin Systems: Structures and Functions. Springer, Dordrecht, p.295-315.
[25]Carrasco-Pozo C, Tan KN, Borges K, 2015. Sulforaphane is anticonvulsant and improves mitochondrial function. J Neurochem, 135(5):932-942.
[26]Carter AB, Hunninghake GW, 2000. A constitutive active MEK→ERK pathway negatively regulates NF-κB-dependent gene expression by modulating TATA-binding protein phosphorylation. J Biol Chem, 275(36):27858-27864.
[27]Chaban Y, Boekema EJ, Dudkina NV, 2014. Structures of mitochondrial oxidative phosphorylation supercomplexes and mechanisms for their stabilisation. Biochim Biophys Acta, 1837(4):418-426.
[28]Clarke JD, Hsu A, Williams DE, et al., 2011. Metabolism and tissue distribution of sulforaphane in Nrf2 knockout and wild-type mice. Pharm Res, 28(12):3171-3179.
[29]Cobley JN, Fiorello ML, Bailey DM, 2018. 13 reasons why the brain is susceptible to oxidative stress. Redox Biol, 15: 490-503.
[30]Cohen G, Heikkila RE, 1974. The generation of hydrogen peroxide, superoxide radical, and hydroxyl radical by 6-hydroxydopamine, dialuric acid, and related cytotoxic agents. J Biol Chem, 249(8):2447-2452.
[31]Corrado M, Scorrano L, Campello S, 2012. Mitochondrial dynamics in cancer and neurodegenerative and neuroinflammatory diseases. Int J Cell Biol, 2012:729290.
[32]de Armas MI, Esteves R, Viera N, et al., 2019. Rapid peroxynitrite reduction by human peroxiredoxin 3: implications for the fate of oxidants in mitochondria. Free Radic Biol Med, 130:369-378.
[33]de Oliveira MR, 2015. Vitamin A and retinoids as mitochondrial toxicants. Oxid Med Cell Longev, 2015:140267.
[34]de Oliveira MR, 2016. Fluoxetine and the mitochondria: a review of the toxicological aspects. Toxicol Lett, 258: 185-191.
[35]de Oliveira MR, Jardim FR, 2016. Cocaine and mitochondria-related signaling in the brain: a mechanistic view and future directions. Neurochem Int, 92:58-66.
[36]de Oliveira MR, Brasil FB, Fürstenau CR, 2018a. Sulforaphane attenuated the pro-inflammatory state induced by hydrogen peroxide in SH-SY5Y cells through the Nrf2/HO-1 signaling pathway. Neurotox Res, 34(2):241-249.
[37]de Oliveira MR, de Bittencourt Brasil F, Fürstenau CR, 2018b. Sulforaphane promotes mitochondrial protection in SH-SY5Y cells exposed to hydrogen peroxide by an Nrf2-dependent mechanism. Mol Neurobiol, 55(6):4777-4787.
[38]Deponte M, 2013. Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta, 1830(5):3217-3266.
[39]di Domenico F, Tramutola A, Butterfield DA, 2017. Role of 4-hydroxy-2-nonenal (HNE) in the pathogenesis of alzheimer disease and other selected age-related neurodegenerative disorders. Free Radic Biol Med, 111:253-261.
[40]Esposito LA, Kokoszka JE, Waymire KG, et al., 2000. Mitochondrial oxidative stress in mice lacking the glutathione peroxidase-1 gene. Free Radic Biol Med, 28(5):754-766.
[41]Fahey JW, Holtzclaw WD, Wehage SL, et al., 2015. Sulforaphane bioavailability from glucoraphanin-rich broccoli: control by active endogenous myrosinase. PLoS ONE, 10(11):e0140963.
[42]Fernández-Checa JC, Kaplowitz N, García-Ruiz C, et al., 1997. GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am J Physiol, 273(1 Pt 1):G7-G17.
[43]Fernández-Checa JC, García-Ruiz C, Colell A, et al., 1998. Oxidative stress: role of mitochondria and protection by glutathione. BioFactors, 8(1-2):7-11.
[44]Franklin CC, Backos DS, Mohar I, et al., 2009. Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med, 30(1-2):86-98.
[45]Gerich JE, Meyer C, Woerle HJ, et al., 2001. Renal gluconeogenesis: its importance in human glucose homeostasis. Diabetes Care, 24(2):382-391.
[46]Ghezzi P, 2013. Protein glutathionylation in health and disease. Biochim Biophys Acta, 1830(5):3165-3172.
[47]Greco T, Fiskum G, 2010. Brain mitochondria from rats treated with sulforaphane are resistant to redox-regulated permeability transition. J Bioenerg Biomembr, 42(6):491-497.
[48]Green DR, Galluzzi L, Kroemer G, 2014. Metabolic control of cell death. Science, 345(6203):1250256.
[49]Grivennikova VG, Vinogradov AD, 2006. Generation of superoxide by the mitochondrial Complex I. Biochim Biophys Acta, 1757(5-6):553-561.
[50]Gustafsson CM, Falkenberg M, Larsson NG, 2016. Maintenance and expression of mammalian mitochondrial DNA. Annu Rev Biochem, 85:133-160.
[51]Hanlon N, Coldham N, Gielbert A, et al., 2008. Absolute bioavailability and dose-dependent pharmacokinetic behaviour of dietary doses of the chemopreventive isothiocyanate sulforaphane in rat. Br J Nutr, 99(3):559-564.
[52]Heikkila RE, Cohen G, 1973. 6-Hydroxydopamine: evidence for superoxide radical as an oxidative intermediate. Science, 181(4098):456-457.
[53]Herrmann JM, Riemer J, 2010. The intermembrane space of mitochondria. Antioxid Redox Signal, 13(9):1341-1358.
[54]Houghton CA, Fassett RG, Coombes JS, 2016. Sulforaphane and other nutrigenomic Nrf2 activators: can the clinician’s expectation be matched by the reality? Oxid Med Cell Longev, 2016:7857186.
[55]Huang J, Philbert MA, 1995. Distribution of glutathione and glutathione-related enzyme systems in mitochondria and cytosol of cultured cerebellar astrocytes and granule cells. Brain Res, 680(1-2):16-22.
[56]Huang TY, Chang WC, Wang MY, et al., 2012. Effect of sulforaphane on growth inhibition in human brain malignant glioma GBM 8401 cells by means of mitochondrial- and MEK/ERK-mediated apoptosis pathway. Cell Biochem Biophys, 63(3):247-259.
[57]Hunt JV, Dean RT, Wolff SP, 1988. Hydroxyl radical production and autoxidative glycosylation. Glucose autoxidation as the cause of protein damage in the experimental glycation model of diabetes mellitus and ageing. Biochem J, 256(1):205-212.
[58]Jardim FR, de Rossi FT, Nascimento MX, et al., 2018. Resveratrol and brain mitochondria: a review. Mol Neurobiol, 55(3):2085-2101.
[59]Jiang BB, Xu SQ, Hou XY, et al., 2004. Temporal control of NF-κB activation by ERK differentially regulates interleukin-1β-induced gene expression. J Biol Chem, 279(2):1323-1329.
[60]Jiang H, Shang X, Wu HT, et al., 2010. Combination treatment with resveratrol and sulforaphane induces apoptosis in human U251 Glioma cells. Neurochem Res, 35(1):152-161.
[61]Jin HS, Suh HW, Kim SJ, et al., 2017. Mitochondrial control of innate immunity and inflammation. Immune Netw, 17(2):77-88.
[62]Karmakar S, Weinberg MS, Banik NL, et al., 2006. Activation of multiple molecular mechanisms for apoptosis in human malignant glioblastoma T98G and U87MG cells treated with sulforaphane. Neuroscience, 141(3):1265-1280.
[63]Keum YS, Khor TO, Lin W, et al., 2009. Pharmacokinetics and pharmacodynamics of broccoli sprouts on the suppression of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) mice: implication of induction of Nrf2, HO-1 and apoptosis and the suppression of Akt-dependent kinase pathway. Pharm Res, 26(10):2324-2331.
[64]Kloster MM, Naderi EH, Carlsen H, et al., 2011. Hyperactivation of NF-κB via the MEK signaling is indispensable for the inhibitory effect of cAMP on DNA damage-induced cell death. Mol Cancer, 10:45.
[65]Krysko DV, Agostinis P, Krysko O, et al., 2011. Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol, 32(4):157-164.
[66]Lan FM, Pan Q, Yu HM, et al., 2015. Sulforaphane enhances temozolomide-induced apoptosis because of down-regulation of miR-21 via Wnt/β-catenin signaling in glioblastoma. J Neurochem, 134(5):811-818.
[67]Lash LH, 2006. Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem Biol Interact, 163(1-2):54-67.
[68]Lavich IC, de Freitas BS, Kist LW, et al., 2015. Sulforaphane rescues memory dysfunction and synaptic and mitochondrial alterations induced by brain iron accumulation. Neuroscience, 301:542-552.
[69]Leoncini E, Malaguti M, Angeloni C, et al., 2011. Cruciferous vegetable phytochemical sulforaphane affects phase II enzyme expression and activity in rat cardiomyocytes through modulation of Akt signaling pathway. J Food Sci, 76(7):H175-H181.
[70]Lipton SA, Choi YB, Pan ZH, et al., 1993. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature, 364(6438):626-632.
[71]Liu YL, Hyde AS, Simpson MA, et al., 2014. Emerging regulatory paradigms in glutathione metabolism. Adv Cancer Res, 122:69-101.
[72]Lu SC, 2009. Regulation of glutathione synthesis. Mol Aspects Med, 30(1-2):42-59.
[73]Lu SC, 2013. Glutathione synthesis. Biochim Biophys Acta, 1830(5):3143-3153.
[74]Luis-García ER, Limón-Pacheco JH, Serrano-García N, et al., 2017. Sulforaphane prevents quinolinic acid-induced mitochondrial dysfunction in rat striatum. J Biochem Mol Toxicol, 31(2):e21837.
[75]Ma Q, 2013. Role of Nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol, 53:401-426.
[76]Maes M, Galecki P, Chang YS, et al., 2011. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro)degenerative processes in that illness. Prog Neuro-Psychopharm Biol Psychiatry, 35(3):676-692.
[77]Magistretti PJ, Allaman I, 2015. A cellular perspective on brain energy metabolism and functional imaging. Neuron, 86(4):883-901.
[78]Mailloux RJ, Bériault R, Lemire J, et al., 2007. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist. PLoS ONE, 2(8):e690.
[79]Marí M, Morales A, Colell A, et al., 2013. Mitochondrial glutathione: features, regulation and role in disease. Biochim Biophys Acta, 1830(5):3317-3328.
[80]Miao ZW, Yu F, Ren YH, et al., 2017.
[81]Miller DM, Buettner GR, Aust SD, 1990. Transition metals as catalysts of “autoxidation” reactions. Free Radic Biol Med, 8(1):95-108.
[82]Miller DM, Singh IN, Wang JA, et al., 2013. Administration of the Nrf2-ARE activators sulforaphane and carnosic acid attenuates 4-hydroxy-2-nonenal-induced mitochondrial dysfunction ex vivo. Free Radic Biol Med, 57:1-9.
[83]Mishra J, Kumar A, 2014. Improvement of mitochondrial function by paliperidone attenuates quinolinic acid-induced behavioural and neurochemical alterations in rats: implications in Huntington’s disease. Neurotox Res, 26(4):363-381.
[84]Murphy MP, 2009. How mitochondria produce reactive oxygen species. Biochem J, 417(1):1-13.
[85]Nguyen P, Leray V, Diez M, et al., 2008. Liver lipid metabolism. J Anim Physiol Anim Nutr, 92(3):272-283.
[86]Nguyen T, Nioi P, Pickett CB, 2009. The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem, 284(20):13291-13295.
[87]Niki E, Yoshida Y, Saito Y, et al., 2005. Lipid peroxidation: mechanisms, inhibition, and biological effects. Biochem Biophys Res Commun, 338(1):668-676.
[88]O'Mealey GB, Berry WL, Plafker SM, 2017. Sulforaphane is a Nrf2-independent inhibitor of mitochondrial fission. Redox Biol, 11:103-110.
[89]Ostrom QT, Bauchet L, Davis FG, et al., 2014. The epidemiology of glioma in adults: a “state of the science” review. Neuro-Oncol, 16(7):896-913.
[90]Papa S, Martino PL, Capitanio G, et al., 2012. The oxidative phosphorylation system in mammalian mitochondria. In: Scatena R, Bottoni P, Giardina B (Eds.), Advances in Mitochondrial Medicine. Springer, Dordrecht, p.3-37.
[91]Paupe V, Prudent J, 2018. New insights into the role of mitochondrial calcium homeostasis in cell migration. Biochem Biophys Res Commun, 500(1):75-86.
[92]Petersen MC, Vatner DF, Shulman GI, 2017. Regulation of hepatic glucose metabolism in health and disease. Nat Rev Endocrinol, 13(10):572-587.
[93]Pinton P, Brini M, Bastianutto C, et al., 1998. New light on mitochondrial calcium. BioFactors, 8(3-4):243-253.
[94]Poderoso JJ, Carreras MC, Lisdero C, et al., 1996. Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch Biochem Biophys, 328(1):85-92.
[95]Poderoso JJ, Helfenberger K, Poderoso C, 2019. The effect of nitric oxide on mitochondrial respiration. Nitric Oxide, 88: 61-72.
[96]Porcelli AM, Ghelli A, Zanna C, et al., 2005. pH difference across the outer mitochondrial membrane measured with a green fluorescent protein mutant. Biochem Biophys Res Commun, 326(4):799-804.
[97]Prasai K, 2017. Regulation of mitochondrial structure and function by protein import: a current review. Pathophysiology, 24(3):107-122.
[98]Puchalska P, Crawford PA, 2017. Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metab, 25(2):262-284.
[99]Radi R, 2013. Peroxynitrite, a stealthy biological oxidant. J Biol Chem, 288(37):26464-26472.
[100]Raffaello A, Mammucari C, Gherardi G, et al., 2016. Calcium at the center of cell signaling: interplay between endoplasmic reticulum, mitochondria, and lysosomes. Trends Biochem Sci, 41(12):1035-1049.
[101]Ramsay RR, Gravestock MB, 2003. Monoamine oxidases: to inhibit or not to inhibit. Mini Rev Med Chem, 3(2):129-136.
[102]Reis A, Spickett CM, 2012. Chemistry of phospholipid oxidation. Biochim Biophys Acta, 1818(10):2374-2387.
[103]Ren XY, Zou LL, Zhang X, et al., 2017. Redox signaling mediated by thioredoxin and glutathione systems in the central nervous system. Antioxid Redox Signal, 27(13):989-1010.
[104]Rodolfo C, Campello S, Cecconi F, 2018. Mitophagy in neurodegenerative diseases. Neurochem Int, 117:156-166.
[105]Russo M, Spagnuolo C, Russo GL, et al., 2018. Nrf2 targeting by sulforaphane: a potential therapy for cancer treatment. Crit Rev Food Sci Nutr, 58(8):1391-1405.
[106]Salim S, 2017. Oxidative stress and the central nervous system. J Pharmacol Exp Ther, 360(1):201-205.
[107]Salvi M, Battaglia V, Brunati AM, et al., 2007. Catalase takes part in rat liver mitochondria oxidative stress defense. J Biol Chem, 282(33):24407-24415.
[108]Scarpulla RC, 2006. Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem, 97(4):673-683.
[109]Scarpulla RC, 2008. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev, 88(2):611-638.
[110]Scarpulla RC, 2011. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim Biophys Acta, 1813(7):1269-1278.
[111]Schain M, Kreisl WC, 2017. Neuroinflammation in neurodegenerative disorders—a review. Curr Neurol Neurosci Rep, 17(3):25.
[112]Scialò F, Fernández-Ayala DJ, Sanz A, 2017. Role of mitochondrial reverse electron transport in ROS signaling: potential roles in health and disease. Front Physiol, 8:428.
[113]Scott I, Youle RJ, 2010. Mitochondrial fission and fusion. Essays Biochem, 47:85-98.
[114]Sies H, Berndt C, Jones DP, 2017. Oxidative stress. Annu Rev Biochem, 86:715-748.
[115]Signes A, Fernandez-Vizarra E, 2018. Assembly of mammalian oxidative phosphorylation complexes I–V and supercomplexes. Essays Biochem, 62(3):255-270.
[116]Smirnova E, Griparic L, Shurland DL, et al., 2001. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell, 12(8):2245-2256.
[117]Socała K, Nieoczym D, Kowalczuk-Vasilev E, et al., 2017. Increased seizure susceptibility and other toxicity symptoms following acute sulforaphane treatment in mice. Toxicol Appl Pharmacol, 326:43-53.
[118]Spinelli JB, Haigis MC, 2018. The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol, 20(7):745-754.
[119]Stojanovski D, Müller JM, Milenkovic D, et al., 2008. The MIA system for protein import into the mitochondrial intermembrane space. Biochim Biophys Acta, 1783(4):610-617.
[120]Sultana R, Perluigi M, Butterfield DA, 2013. Lipid peroxidation triggers neurodegeneration: a redox proteomics view into the Alzheimer disease brain. Free Radic Biol Med, 62:157-169.
[121]Sumimoto H, 2008. Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J, 275(13):3249-3277.
[122]Thornalley PJ, 1985. Monosaccharide autoxidation in health and disease. Environ Health Perspect, 64:297-307.
[123]Tracey TJ, Steyn FJ, Wolvetang EJ, et al., 2018. Neuronal lipid metabolism: multiple pathways driving functional outcomes in health and disease. Front Mol Neurosci, 11:10.
[124]Uttara B, Singh AV, Zamboni P, et al., 2009. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol, 7(1):65-74.
[125]van der Laan M, Horvath SE, Pfanner N, 2016. Mitochondrial contact site and cristae organizing system. Curr Opin Cell Biol, 41:33-42.
[126]Vermeulen M, Klöpping-Ketelaars IW, van den Berg R, et al., 2008. Bioavailability and kinetics of sulforaphane in humans after consumption of cooked versus raw broccoli. J Agric Food Chem, 56(22):10505-10509.
[127]Wang XL, Su B, Lee HG, et al., 2009. Impaired balance of mitochondrial fission and fusion in Alzheimer’s disease. J Neurosci, 29(28):9090-9103.
[128]Wang Y, Liu N, Lu BW, 2019. Mechanisms and roles of mitophagy in neurodegenerative diseases. CNS Neurosci Ther, 25(7):859-875.
[129]Watmough NJ, Frerman FE, 2010. The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochim Biophys Acta, 1797(12):1910-1916.
[130]Westermann B, 2012. Bioenergetic role of mitochondrial fusion and fission. Biochim Biophys Acta, 1817(10):1833-1838.
[131]Wilkins HM, Kirchhof D, Manning E, et al., 2013. Mitochondrial glutathione transport is a key determinant of neuronal susceptibility to oxidative and nitrosative stress. J Biol Chem, 288(7):5091-5101.
[132]Wolff SP, Dean RT, 1987. Glucose autoxidation and protein modification. The potential role of ‘autoxidative glycosylation’ in diabetes. Biochem J, 245(1):243-250.
[133]Youdim MBH, Edmondson D, Tipton KF, 2006. The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci, 7(4):295-309.
[134]Zhang J, Frerman FE, Kim JJP, 2006. Structure of electron transfer flavoprotein-ubiquinone oxidoreductase and electron transfer to the mitochondrial ubiquinone pool. Proc Natl Acad Sci USA, 103(44):16212-16217.
[135]Zhang JH, 2013. Autophagy and mitophagy in cellular damage control. Redox Biol, 1(1):19-23.
[136]Zhang Z, Li CL, Shang L, et al., 2016. Sulforaphane induces apoptosis and inhibits invasion in U251MG glioblastoma cells. SpringerPlus, 5:235.
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