New Probucol Analogues Inhibit Ferroptosis, Improve Mitochondrial Parameters, and Induce Glutathione Peroxidase in HT22 Cells.
Animals
Antioxidants
/ metabolism
Cell Death
/ drug effects
Ferroptosis
/ drug effects
Glutathione
/ metabolism
Glutathione Peroxidase
/ drug effects
Mice
Mitochondria
/ drug effects
Neuroprotection
/ drug effects
Neuroprotective Agents
/ pharmacology
Oxidative Stress
/ drug effects
Probucol
/ pharmacology
Reactive Oxygen Species
/ metabolism
Antioxidant
Ferroptosis
Glutathione peroxidase
HT22
Oxytosis
Probucol
Journal
Molecular neurobiology
ISSN: 1559-1182
Titre abrégé: Mol Neurobiol
Pays: United States
ID NLM: 8900963
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
02
02
2020
accepted:
26
05
2020
pubmed:
10
6
2020
medline:
8
6
2021
entrez:
10
6
2020
Statut:
ppublish
Résumé
Probucol, a hypocholesterolemic compound, is neuroprotective in several models of neurodegenerative diseases but has serious adverse effects in vivo. We now describe the design and synthesis of two new probucol analogues that protect against glutamate-induced oxidative cell death, also known as ferroptosis, in cultured mouse hippocampal (HT22) cells and in primary cortical neurons, while probucol did not show any protective effect. Treatment with both compounds did not affect glutathione depletion but still significantly decreased glutamate-induced production of oxidants, mitochondrial superoxide generation, and mitochondrial hyperpolarization in HT22 cells. Both compounds increase glutathione peroxidase (GPx) 1 levels and GPx activity, also exhibiting protection against RSL3, a GPx4 inactivator. These two compounds are therefore potent activators of GPx activity making further studies of their neuroprotective activity in vivo worthwhile.
Identifiants
pubmed: 32514861
doi: 10.1007/s12035-020-01956-9
pii: 10.1007/s12035-020-01956-9
doi:
Substances chimiques
Antioxidants
0
Neuroprotective Agents
0
Reactive Oxygen Species
0
Glutathione Peroxidase
EC 1.11.1.9
Glutathione
GAN16C9B8O
Probucol
P3CTH044XJ
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3273-3290Subventions
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 404666/2018-3 and 302952/2018-7
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
ID : 88881.134820/2016-01
Références
Yamashita S, Matsuzawa Y (2009) Where are we with probucol: a new life for an old drug? Atherosclerosis 207(1):16–23. https://doi.org/10.1016/j.atherosclerosis.2009.04.002
doi: 10.1016/j.atherosclerosis.2009.04.002
pubmed: 19457483
Yamashita S, Masuda D, Matsuzawa Y (2015) Did we abandon probucol too soon? Curr Opin Lipidol 26(4):304–316. https://doi.org/10.1097/mol.0000000000000199
doi: 10.1097/mol.0000000000000199
pubmed: 26125504
Colle D, Hartwig JM, Antunes Soares FA, Farina M (2012) Probucol modulates oxidative stress and excitotoxicity in Huntington’s disease models in vitro. Brain Res Bull 87(4–5):397–405. https://doi.org/10.1016/j.brainresbull.2012.01.003
doi: 10.1016/j.brainresbull.2012.01.003
pubmed: 22245028
Colle D, Santos DB, Moreira ELG, Hartwig JM, dos Santos AA, Zimmermann LT, Hort MA, Farina M (2013) Probucol increases striatal glutathione peroxidase activity and protects against 3-nitropropionic acid-induced pro-oxidative damage in rats. PLoS One 8(6):e67658. https://doi.org/10.1371/journal.pone.0067658
doi: 10.1371/journal.pone.0067658
pubmed: 23799154
pmcid: 3683065
Santos DB, Peres KC, Ribeiro RP, Colle D, AAd S, ELG M, DOG S, Figueiredo CP et al (2012) Probucol, a lipid-lowering drug, prevents cognitive and hippocampal synaptic impairments induced by amyloid β peptide in mice. Exp Neurol 233(2):767–775. https://doi.org/10.1016/j.expneurol.2011.11.036
doi: 10.1016/j.expneurol.2011.11.036
pubmed: 22173317
Santos DB, Colle D, Moreira ELG, Peres KC, Ribeiro RP, dos Santos AA, de Oliveira J, Hort MA et al (2015) Probucol mitigates streptozotocin-induced cognitive and biochemical changes in mice. Neuroscience 284:590–600. https://doi.org/10.1016/j.neuroscience.2014.10.019
doi: 10.1016/j.neuroscience.2014.10.019
pubmed: 25453776
Ribeiro RP, Moreira ELG, Santos DB, Colle D, dos Santos AA, Peres KC, Figueiredo CP, Farina M (2013) Probucol affords neuroprotection in a 6-OHDA mouse model of Parkinson’s disease. Neurochem Res 38(3):660–668. https://doi.org/10.1007/s11064-012-0965-0
doi: 10.1007/s11064-012-0965-0
pubmed: 23334712
Farina M, Campos F, Vendrell I, Berenguer J, Barzi M, Pons S, Suñol C (2009) Probucol increases glutathione peroxidase-1 activity and displays long-lasting protection against methylmercury toxicity in cerebellar granule cells. Toxicol Sci 112(2):416–426. https://doi.org/10.1093/toxsci/kfp219
doi: 10.1093/toxsci/kfp219
pubmed: 19770487
Stocker R (2009) Molecular mechanisms underlying the antiatherosclerotic and antidiabetic effects of probucol, succinobucol, and other probucol analogues. Curr Opin Lipidol 20(3):227–235. https://doi.org/10.1097/MOL.0b013e32832aee68
doi: 10.1097/MOL.0b013e32832aee68
pubmed: 19373083
Tardif J-C, Grégoire J, Schwartz L, Title L, Laramée L, Reeves F, Lespérance J, Bourassa MG et al (2003) Effects of AGI-1067 and probucol after percutaneous coronary interventions. Circulation 107(4):552–558. https://doi.org/10.1161/01.CIR.0000047525.58618.3C
doi: 10.1161/01.CIR.0000047525.58618.3C
pubmed: 12566365
Colle D, Santos DB, Hartwig JM, Godoi M, Engel DF, de Bem AF, Braga AL, Farina M (2016) Succinobucol, a lipid-lowering drug, protects against 3-nitropropionic acid-induced mitochondrial dysfunction and oxidative stress in SH-SY5Y cells via upregulation of glutathione levels and glutamate cysteine ligase activity. Mol Neurobiol 53(2):1280–1295. https://doi.org/10.1007/s12035-014-9086-x
doi: 10.1007/s12035-014-9086-x
pubmed: 25619973
Santos DB, Colle D, Moreira ELG, Hort MA, Godoi M, Le Douaron G, Braga AL, Assreuy J et al (2017) Succinobucol, a non-statin hypocholesterolemic drug, prevents premotor symptoms and nigrostriatal neurodegeneration in an experimental model of Parkinson’s disease. Mol Neurobiol 54(2):1513–1530. https://doi.org/10.1007/s12035-016-9747-z
doi: 10.1007/s12035-016-9747-z
pubmed: 26852411
Davis JB, Maher P (1994) Protein kinase C activation inhibits glutamate-induced cytotoxicity in a neuronal cell line. Brain Res 652(1):169–173. https://doi.org/10.1016/0006-8993(94)90334-4
doi: 10.1016/0006-8993(94)90334-4
pubmed: 7953717
Albrecht P, Henke N, Tien M-LT, Issberner A, Bouchachia I, Maher P, Lewerenz J, Methner A (2013) Extracellular cyclic GMP and its derivatives GMP and guanosine protect from oxidative glutamate toxicity. Neurochem Int 62(5):610–619. https://doi.org/10.1016/j.neuint.2013.01.019
doi: 10.1016/j.neuint.2013.01.019
pubmed: 23357478
Lewerenz J, Sato H, Albrecht P, Henke N, Noack R, Methner A, Maher P (2012) Mutation of ATF4 mediates resistance of neuronal cell lines against oxidative stress by inducing xCT expression. Cell Death Differ 19(5):847–858 http://www.nature.com/cdd/journal/v19/n5/suppinfo/cdd2011165s1.html
doi: 10.1038/cdd.2011.165
pubmed: 22095285
Maher P, van Leyen K, Dey PN, Honrath B, Dolga A, Methner A (2018) The role of Ca2+ in cell death caused by oxidative glutamate toxicity and ferroptosis. Cell Calcium 70:47–55. https://doi.org/10.1016/j.ceca.2017.05.007
doi: 10.1016/j.ceca.2017.05.007
pubmed: 28545724
Henke N, Albrecht P, Bouchachia I, Ryazantseva M, Knoll K, Lewerenz J, Kaznacheyeva E, Maher P et al (2013) The plasma membrane channel ORAI1 mediates detrimental calcium influx caused by endogenous oxidative stress. Cell Death Dis 4:e470
doi: 10.1038/cddis.2012.216
pubmed: 23348584
pmcid: 3564003
Dixon Scott J, Lemberg Kathryn M, Lamprecht Michael R, Skouta R, Zaitsev Eleina M, Gleason Caroline E, Patel Darpan N, Bauer Andras J et al (2012) Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149(5):1060–1072. https://doi.org/10.1016/j.cell.2012.03.042
doi: 10.1016/j.cell.2012.03.042
pubmed: 22632970
pmcid: 3367386
Albrecht P, Lewerenz J, Dittmer S, Noack R, Maher P, Methner A (2010) Mechanisms of oxidative glutamate toxicity: the glutamate/cystine antiporter system xc¯ as a neuroprotective drug target. CNS Neurol Disord Drug Targets 9(3):373–382. https://doi.org/10.2174/187152710791292567
doi: 10.2174/187152710791292567
pubmed: 20053169
Li J, Cao F, H-l Y, Z-j H, Lin Z-t, Mao N, Sun B, Wang G (2020) Ferroptosis: past, present and future. Cell Death Dis 11(2):88. https://doi.org/10.1038/s41419-020-2298-2
doi: 10.1038/s41419-020-2298-2
pubmed: 32015325
pmcid: 6997353
Lewerenz J, Ates G, Methner A, Conrad M, Maher P (2018) Oxytosis/FErroptosis—(re-) emerging roles for oxidative stress-dependent non-apoptotic cell death in diseases of the central nervous system. Front Neurosci 12:214. https://doi.org/10.3389/fnins.2018.00214
doi: 10.3389/fnins.2018.00214
pubmed: 29731704
pmcid: 5920049
Friedmann Angeli JP, Miyamoto S, Schulze A (2019) Ferroptosis: the greasy side of cell death. Chem Res Toxicol 32(3):362–369. https://doi.org/10.1021/acs.chemrestox.8b00349
doi: 10.1021/acs.chemrestox.8b00349
pubmed: 30653290
Mao X-Y, Zhou H-H, Li X, Liu Z-Q (2016) Huperzine a alleviates oxidative glutamate toxicity in hippocampal HT22 cells via activating BDNF/TrkB-dependent PI3K/Akt/mTOR signaling pathway. Cell Mol Neurobiol 36(6):915–925. https://doi.org/10.1007/s10571-015-0276-5
doi: 10.1007/s10571-015-0276-5
pubmed: 26440805
Kumari S, Mehta SL, Milledge GZ, Huang X, Li H, Li PA (2016) Ubisol-Q10 prevents glutamate-induced cell death by blocking mitochondrial fragmentation and permeability transition pore opening. Int J Biol Sci 12(6):688–700. https://doi.org/10.7150/ijbs.13589
doi: 10.7150/ijbs.13589
pubmed: 27194946
pmcid: 4870712
Jin ML, Park SY, Kim YH, Oh J-I, Lee SJ, Park G (2014) The neuroprotective effects of cordycepin inhibit glutamate-induced oxidative and ER stress-associated apoptosis in hippocampal HT22 cells. NeuroToxicology 41:102–111. https://doi.org/10.1016/j.neuro.2014.01.005
doi: 10.1016/j.neuro.2014.01.005
pubmed: 24486958
Quispe RL, Canto RFS, Jaramillo ML, Barbosa FAR, Braga AL, de Bem AF, Farina M (2018) Design, synthesis, and in vitro evaluation of a novel probucol derivative: protective activity in neuronal cells through GPx upregulation. Mol Neurobiol 55(10):7619–7634. https://doi.org/10.1007/s12035-018-0939-6
doi: 10.1007/s12035-018-0939-6
pubmed: 29430618
Steinbeck JA, Henke N, Opatz J, Gruszczynska-Biegala J, Schneider L, Theiss S, Hamacher N, Steinfarz B et al (2011) Store-operated calcium entry modulates neuronal network activity in a model of chronic epilepsy. Exp Neurol 232(2):185–194. https://doi.org/10.1016/j.expneurol.2011.08.022
doi: 10.1016/j.expneurol.2011.08.022
pubmed: 21906591
Ellman GL (1959) Tissue sulfhydryl groups, Arch Biochem Biophys. 82(1):70–77. https://doi.org/10.1016/0003-9861(59)90090-6
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193(1):265–275
pubmed: 14907713
Chazotte B (2011) Labeling mitochondria with JC-1. Cold Spring Harb Protoc 2011(9):pdb.prot065490. https://doi.org/10.1101/pdb.prot065490
doi: 10.1101/pdb.prot065490
pubmed: 21880824
Oppermann S, Schrader FC, Elsässer K, Dolga AM, Kraus AL, Doti N, Wegscheid-Gerlach C, Schlitzer M et al (2014) Novel <em>N</em>-phenyl–substituted thiazolidinediones protect neural cells against glutamate- and tBid-induced toxicity. J Pharmacol Exp Ther 350(2):273–289. https://doi.org/10.1124/jpet.114.213777
doi: 10.1124/jpet.114.213777
pubmed: 24849923
Lopes MW, Lopes SC, Costa AP, Gonçalves FM, Rieger DK, Peres TV, Eyng H, Prediger RD et al (2015) Region-specific alterations of AMPA receptor phosphorylation and signaling pathways in the pilocarpine model of epilepsy. Neurochem Int 87:22–33. https://doi.org/10.1016/j.neuint.2015.05.003
doi: 10.1016/j.neuint.2015.05.003
pubmed: 25983036
Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83(2):346–356. https://doi.org/10.1016/0003-2697(77)90043-4
doi: 10.1016/0003-2697(77)90043-4
pubmed: 603028
Bjerrum OJ, Heegaard NHH (1988) CRC handbook of immunoblotting of proteins. CRC Press, Cleveland
Wendel A (1981) [44] Glutathione peroxidase. In: Methods in enzymology, vol 77. Academic Press, pp 325-333. https://doi.org/10.1016/S0076-6879(81)77046-0
Panee J, Stoytcheva ZR, Liu W, Berry MJ (2007) Selenoprotein H is a redox-sensing high mobility group family DNA-binding protein that up-regulates genes involved in glutathione synthesis and phase II detoxification. J Biol Chem 282(33):23759–23765. https://doi.org/10.1074/jbc.M702267200
doi: 10.1074/jbc.M702267200
pubmed: 17526492
Mao SJT, Yates MT, Jackson RL (1994) [51] Antioxidant activity and serum levels of probucol and probucal metabolites. In: Methods in enzymology, vol 234. Academic Press, pp 505-513. https://doi.org/10.1016/0076-6879(94)34122-2
Pinacho Crisóstomo FR, Carrillo R, León LG, Martín T, Padrón JM, Martín VS (2006) Molecular simplification in bioactive molecules: formal synthesis of (+)-muconin. J Organomet Chem 71(6):2339–2345. https://doi.org/10.1021/jo0524674
doi: 10.1021/jo0524674
Patani GA, LaVoie EJ (1996) Bioisosterism: a rational approach in drug design. Chem Rev 96(8):3147–3176. https://doi.org/10.1021/cr950066q
doi: 10.1021/cr950066q
pubmed: 11848856
Kwong FY, Buchwald SL (2002) A general, efficient, and inexpensive catalyst system for the coupling of aryl iodides and thiols. Org Lett 4(20):3517–3520. https://doi.org/10.1021/ol0266673
doi: 10.1021/ol0266673
pubmed: 12323058
Murphy TH, Miyamoto M, Sastre A, Schnaar RL, Coyle JT (1989) Glutamate toxicity in a neuronal cell line involves inhibition of cystine transport leading to oxidative stress. Neuron 2(6):1547–1558. https://doi.org/10.1016/0896-6273(89)90043-3
doi: 10.1016/0896-6273(89)90043-3
pubmed: 2576375
Cooper AJL, Ta F (1998) Role of astrocytes in maintaining cerebral glutathione homeostasis and in protecting the brain against xenobiotics and oxidative stress. The role of glutathione in the nervous system, Washington, pp 91–115
Fukui M, Song JH, Choi JY, Choi HJ, Zhu BT (2009) Mechanism of glutamate-induced neurotoxicity in HT22 mouse hippocampal cells. Eur J Pharmacol 617(1–3):1–11. https://doi.org/10.1016/j.ejphar.2009.06.059
doi: 10.1016/j.ejphar.2009.06.059
pubmed: 19580806
Herrera F, Martin V, Garcia-Santos G, Rodriguez-Blanco J, Antolin I, Rodriguez C (2007) Melatonin prevents glutamate-induced oxytosis in the HT22 mouse hippocampal cell line through an antioxidant effect specifically targeting mitochondria. J Neurochem 100(3):736–746. https://doi.org/10.1111/j.1471-4159.2006.04228.x
doi: 10.1111/j.1471-4159.2006.04228.x
pubmed: 17263795
Pallast S, Arai K, Wang XY, Lo EH, van Leyen K (2009) 12/15-Lipoxygenase targets neuronal mitochondria under oxidative stress. J Neurochem 111(3):882–889. https://doi.org/10.1111/j.1471-4159.2009.06379.x
doi: 10.1111/j.1471-4159.2009.06379.x
pubmed: 19737346
pmcid: 2773137
Fukui M, Zhu BT (2010) Mitochondrial superoxide dismutase SOD2, but not cytosolic SOD1, plays a critical role in protection against glutamate-induced oxidative stress and cell death in HT22 neuronal cells. Free Radic Biol Med 48(6):821–830. https://doi.org/10.1016/j.freeradbiomed.2009.12.024
doi: 10.1016/j.freeradbiomed.2009.12.024
pubmed: 20060889
pmcid: 2861908
Tobaben S, Grohm J, Seiler A, Conrad M, Plesnila N, Culmsee C (2011) Bid-mediated mitochondrial damage is a key mechanism in glutamate-induced oxidative stress and AIF-dependent cell death in immortalized HT-22 hippocampal neurons. Cell Death Differ 18(2):282–292. https://doi.org/10.1038/cdd.2010.92
doi: 10.1038/cdd.2010.92
pubmed: 20689558
Pfeiffer A, Jaeckel M, Lewerenz J, Noack R, Pouya A, Schacht T, Hoffmann C, Winter J et al (2014) Mitochondrial function and energy metabolism in neuronal HT22 cells resistant to oxidative stress. Br J Pharmacol 171(8):2147–2158. https://doi.org/10.1111/bph.12549
doi: 10.1111/bph.12549
pubmed: 24319993
pmcid: 3976627
Zhang C, Yuan X-r, Li H-y, Zhao Z-j, Liao Y-w, Wang X-y, Su J, Sang S-s et al (2014) Downregualtion of dynamin-related protein 1 attenuates glutamate-induced excitotoxicity via regulating mitochondrial function in a calcium dependent manner in HT22 cells. Biochem Biophys Res Commun 443(1):138–143. https://doi.org/10.1016/j.bbrc.2013.11.072
doi: 10.1016/j.bbrc.2013.11.072
pubmed: 24284040
Sun S, Hu F, Wu J, Zhang S (2017) Cannabidiol attenuates OGD/R-induced damage by enhancing mitochondrial bioenergetics and modulating glucose metabolism via pentose-phosphate pathway in hippocampal neurons. Redox Biol 11:577–585. https://doi.org/10.1016/j.redox.2016.12.029
doi: 10.1016/j.redox.2016.12.029
pubmed: 28110213
Zhang YM, Bhavnani BR (2006) Glutamate-induced apoptosis in neuronal cells is mediated via caspase-dependent and independent mechanisms involving calpain and caspase-3 proteases as well as apoptosis inducing factor (AIF) and this process is inhibited by equine estrogens. BMC Neurosci 7:49. https://doi.org/10.1186/1471-2202-7-49
doi: 10.1186/1471-2202-7-49
pubmed: 16776830
pmcid: 1526740
Liu Y, Schubert DR (2009) The specificity of neuroprotection by antioxidants. J Biomed Sci 16(1):98. https://doi.org/10.1186/1423-0127-16-98
doi: 10.1186/1423-0127-16-98
pubmed: 19891782
pmcid: 2779189
Kumari S, Mehta SL, Li PA (2012) Glutamate induces mitochondrial dynamic imbalance and autophagy activation: preventive effects of selenium. PLoS One 7(6):e39382. https://doi.org/10.1371/journal.pone.0039382
doi: 10.1371/journal.pone.0039382
pubmed: 22724008
pmcid: 3378533
Grohm J, Plesnila N, Culmsee C (2010) Bid mediates fission, membrane permeabilization and peri-nuclear accumulation of mitochondria as a prerequisite for oxidative neuronal cell death. Brain Behav Immun 24(5):831–838. https://doi.org/10.1016/j.bbi.2009.11.015
doi: 10.1016/j.bbi.2009.11.015
pubmed: 19961923
Murphy Michael P (2009) How mitochondria produce reactive oxygen species. Biochem J 417(1):1–13. https://doi.org/10.1042/bj20081386
doi: 10.1042/bj20081386
pubmed: 19061483
Westermann B (2010) Mitochondrial fusion and fission in cell life and death. Nat Rev Mol Cell Biol 11:872–884. https://doi.org/10.1038/nrm3013
doi: 10.1038/nrm3013
pubmed: 21102612
Bertram R, Gram Pedersen M, Luciani DS, Sherman A (2006) A simplified model for mitochondrial ATP production. J Theor Biol 243(4):575–586. https://doi.org/10.1016/j.jtbi.2006.07.019
doi: 10.1016/j.jtbi.2006.07.019
pubmed: 16945388
Hatefi Y (1985) The mitochondrial electron transport and oxidative phosphorylation system. Annu Rev Biochem 54(1):1015–1069. https://doi.org/10.1146/annurev.bi.54.070185.005055
doi: 10.1146/annurev.bi.54.070185.005055
pubmed: 2862839
Wang K, Yin XM, Chao DT, Milliman CL, Korsmeyer SJ (1996) BID: a novel BH3 domain-only death agonist. Genes Dev 10(22):2859–2869. https://doi.org/10.1101/gad.10.22.2859
doi: 10.1101/gad.10.22.2859
pubmed: 8918887
Gross A, Yin X-M, Wang K, Wei MC, Jockel J, Milliman C, Erdjument-Bromage H, Tempst P et al (1999) Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 274(2):1156–1163. https://doi.org/10.1074/jbc.274.2.1156
doi: 10.1074/jbc.274.2.1156
pubmed: 9873064
Eskes R, Desagher S, Antonsson B, Martinou J-C (2000) Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol 20(3):929–935. https://doi.org/10.1128/mcb.20.3.929-935.2000
doi: 10.1128/mcb.20.3.929-935.2000
pubmed: 10629050
pmcid: 85210
Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, Thompson CB, Korsmeyer SJ (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 14(16):2060–2071. https://doi.org/10.1101/gad.14.16.2060
doi: 10.1101/gad.14.16.2060
pubmed: 10950869
pmcid: 316859
Neitemeier S, Jelinek A, Laino V, Hoffmann L, Eisenbach I, Eying R, Ganjam GK, Dolga AM et al (2017) BID links ferroptosis to mitochondrial cell death pathways. Redox Biol 12:558–570. https://doi.org/10.1016/j.redox.2017.03.007
doi: 10.1016/j.redox.2017.03.007
pubmed: 28384611
pmcid: 5382034
Feng H, Stockwell BR (2018) Unsolved mysteries: how does lipid peroxidation cause ferroptosis? PLoS Biol 16(5):e2006203. https://doi.org/10.1371/journal.pbio.2006203
doi: 10.1371/journal.pbio.2006203
pubmed: 29795546
pmcid: 5991413
Chaudiere J, Wilhelmsen EC, Tappel AL (1984) Mechanism of selenium-glutathione peroxidase and its inhibition by mercaptocarboxylic acids and other mercaptans. J Biol Chem 259(2):1043–1050
pubmed: 6693375
Cardoso BR, Hare DJ, Bush AI, Roberts BR (2016) Glutathione peroxidase 4: a new player in neurodegeneration? Mol Psychiatry 22:328–335. https://doi.org/10.1038/mp.2016.196
doi: 10.1038/mp.2016.196
pubmed: 27777421
Brigelius-Flohé R, Maiorino M (2013) Glutathione peroxidases. Biochim Biophys Acta Gen Subj 1830(5):3289–3303. https://doi.org/10.1016/j.bbagen.2012.11.020
doi: 10.1016/j.bbagen.2012.11.020
Casañas-Sánchez V, Pérez JA, Fabelo N, Herrera-Herrera AV, Fernández C, Marín R, González-Montelongo MC, Díaz M (2014) Addition of docosahexaenoic acid, but not arachidonic acid, activates glutathione and thioredoxin antioxidant systems in murine hippocampal HT22 cells: potential implications in neuroprotection. J Neurochem 131(4):470–483. https://doi.org/10.1111/jnc.12833
doi: 10.1111/jnc.12833
pubmed: 25060706
Jelinek A, Heyder L, Daude M, Plessner M, Krippner S, Grosse R, Diederich WE, Culmsee C (2018) Mitochondrial rescue prevents glutathione peroxidase-dependent ferroptosis. Free Radic Biol Med 117:45–57. https://doi.org/10.1016/j.freeradbiomed.2018.01.019
doi: 10.1016/j.freeradbiomed.2018.01.019
pubmed: 29378335
Thangaraj P (2016) In vitro antioxidant assays. In: Pharmacological assays of plant-based natural products. Springer International Publishing, Cham, pp 57–72. https://doi.org/10.1007/978-3-319-26811-8_9
Pfleger J, He M, Abdellatif M (2015) Mitochondrial complex II is a source of the reserve respiratory capacity that is regulated by metabolic sensors and promotes cell survival. Cell Death Dis 6:e1835. https://doi.org/10.1038/cddis.2015.202 https://www.nature.com/articles/cddis2015202#supplementary-information
doi: 10.1038/cddis.2015.202
pubmed: 26225774
pmcid: 4650745
Seiler A, Schneider M, Förster H, Roth S, Wirth EK, Culmsee C, Plesnila N, Kremmer E et al (2008) Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab 8(3):237–248. https://doi.org/10.1016/j.cmet.2008.07.005
doi: 10.1016/j.cmet.2008.07.005
pubmed: 18762024
Lubos E, Loscalzo J, Handy DE (2011) Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 15(7):1957–1997. https://doi.org/10.1089/ars.2010.3586
doi: 10.1089/ars.2010.3586
pubmed: 21087145
pmcid: 3159114
Sies H (1993) Ebselen, a selenoorganic compound as glutathione peroxidase mimic. Free Radic Biol Med 14(3):313–323. https://doi.org/10.1016/0891-5849(93)90028-S
doi: 10.1016/0891-5849(93)90028-S
pubmed: 8458589
Nogueira CW, Zeni G, Rocha JBT (2004) Organoselenium and organotellurium compounds: toxicology and pharmacology. Chem Rev 104(12):6255–6286. https://doi.org/10.1021/cr0406559
doi: 10.1021/cr0406559
pubmed: 15584701
Reich HJ, Hondal RJ (2016) Why nature chose selenium. ACS Chem Biol 11(4):821–841. https://doi.org/10.1021/acschembio.6b00031
doi: 10.1021/acschembio.6b00031
pubmed: 26949981
Poirier J, Miron J, Picard C, Gormley P, Théroux L, Breitner J, Dea D (2014) Apolipoprotein E and lipid homeostasis in the etiology and treatment of sporadic Alzheimer’s disease. Neurobiol Aging 35:S3–S10. https://doi.org/10.1016/j.neurobiolaging.2014.03.037
doi: 10.1016/j.neurobiolaging.2014.03.037
pubmed: 24973118
pmcid: 5140289