Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Review Article

Enlightening the Mechanism of Ferroptosis in Epileptic Heart

Author(s): Enes Akyüz, Qamar Hakeem Saleem, Çiğdem Sari, Jerónimo Auzmendi and Alberto Lazarowski*

Volume 31, Issue 8, 2024

Published on: 04 April, 2023

Page: [952 - 969] Pages: 18

DOI: 10.2174/0929867330666230223103524

Price: $65

Abstract

Epilepsy is a chronic neurological degenerative disease with a high incidence, affecting all age groups. Refractory Epilepsy (RE) occurs in approximately 30-40% of cases with a higher risk of sudden unexpected death in epilepsy (SUDEP). Recent studies have shown that spontaneous seizures developed in epilepsy can be related to an increase in oxidative stress and reactive oxygen derivatives (ROS) production. Increasing ROS concentration causes lipid peroxidation, protein oxidation, destruction of nuclear genetic material, enzyme inhibition, and cell death by a mechanism known as “ferroptosis” (Fts). Inactivation of glutathione peroxidase 4 (GPX4) induces Fts, while oxidative stress is linked with increased intracellular free iron (Fe+2) concentration. Fts is also a non-apoptotic programmed cell death mechanism, where a hypoxia-inducible factor 1 alpha (HIF-1α) dependent hypoxic stress-like condition appears to occur with accumulation of iron and cytotoxic ROS in affected cells. Assuming convulsive crises as hypoxic stress, repetitive convulsive/hypoxic stress can be an effective inducer of the “epileptic heart” (EH), which is characterized by altered autonomic function and a high risk of malignant or fatal bradycardia. We previously reported that experimental recurrent seizures induce cardiomyocyte Fts associated with SUDEP. Furthermore, several genes related to Fts and hypoxia have recently been identified in acute myocardial infarction. An emerging theme from recent studies indicates that inhibition of GPX4 through modulating expression or activities of the xCT antiporter system (SLC7A11) governs cell sensitivity to oxidative stress from ferroptosis. Furthermore, during hypoxia, an increased expression of stress transcriptional factor ATF3 can promote Fts induced by erastin in a HIF-1α-dependent manner. We propose that inhibition of Fts with ROS scavengers, iron chelators, antioxidants, and transaminase inhibitors could provide a therapeutic effect in epilepsy and improve the prognosis of SUDEP risk by protecting the heart from ferroptosis.

Keywords: Refractory epilepsy, SUDEP, P-glycoprotein, ferroptosis, SLC7A11, epileptic heart.

« Previous Next »
[1]
Stafstrom, C.E.; Carmant, L. Seizures and epilepsy: An overview for neuroscientists. Cold Spring Harb. Perspect. Med., 2015, 5(6), a022426.
[http://dx.doi.org/10.1101/cshperspect.a022426] [PMID: 26033084]
[2]
Fazel, S.; Wolf, A.; Långström, N.; Newton, C.R.; Lichtenstein, P. Premature mortality in epilepsy and the role of psychiatric comorbidity: A total population study. Lancet, 2013, 382(9905), 1646-1654.
[http://dx.doi.org/10.1016/S0140-6736(13)60899-5] [PMID: 23883699]
[3]
Devinsky, O.; Vezzani, A.; O’Brien, T.J.; Jette, N.; Scheffer, I.E.; de Curtis, M.; Perucca, P. Epilepsy. Nat. Rev. Dis. Primers, 2018, 4(1), 18024.
[http://dx.doi.org/10.1038/nrdp.2018.24] [PMID: 29722352]
[4]
Hauser, W.; Hersdorffer, D. Epilepsy: Frequency, Causes and Consequences; Demos Medical Pub: New York, 1990.
[5]
Beghi, E.; Giussani, G.; Sander, J.W. The natural history and prognosis of epilepsy. Epileptic Disord., 2015, 17(3), 243-253.
[http://dx.doi.org/10.1684/epd.2015.0751] [PMID: 26234761]
[6]
Sen, A.; Jette, N.; Husain, M.; Sander, J.W. Epilepsy in older people. Lancet, 2020, 395(10225), 735-748.
[http://dx.doi.org/10.1016/S0140-6736(19)33064-8] [PMID: 32113502]
[7]
Freitas, R.M.; Vasconcelos, S.M.M.; Souza, F.C.F.; Viana, G.S.B.; Fonteles, M.M.F. Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J., 2005, 272(6), 1307-1312.
[http://dx.doi.org/10.1111/j.1742-4658.2004.04537.x] [PMID: 15752349]
[8]
McElroy, P. B.; Liang, L. P.; Day, B. J.; Patel, M. Scavenging reactive oxygen species inhibits status epilepticus-induced neuroinflammation. Exp. Neurol., 2017, 298(Pt A), 13-22.
[http://dx.doi.org/10.1016/j.expneurol.2017.08.009]
[9]
Olowe, R.; Sandouka, S.; Saadi, A.; Shekh-Ahmad, T. Approaches for reactive oxygen species and oxidative stress quantification in epilepsy. Antioxidants, 2020, 9(10), 990.
[http://dx.doi.org/10.3390/antiox9100990] [PMID: 33066477]
[10]
Parsons, A.L.M.; Bucknor, E.M.V.; Castroflorio, E.; Soares, T.R.; Oliver, P.L.; Rial, D. The interconnected mechanisms of oxidative stress and neuroinflammation in epilepsy. Antioxidants, 2022, 11(1), 157.
[http://dx.doi.org/10.3390/antiox11010157] [PMID: 35052661]
[11]
Freitas, R.M. Investigation of oxidative stress involvement in hippocampus in epilepsy model induced by pilocarpine. Neurosci. Lett., 2009, 462(3), 225-229.
[http://dx.doi.org/10.1016/j.neulet.2009.07.037] [PMID: 19616071]
[12]
Chen, S.; Chen, Y.; Zhang, Y.; Kuang, X.; Liu, Y.; Guo, M.; Ma, L.; Zhang, D.; Li, Q. Iron metabolism and ferroptosis in epilepsy. Front. Neurosci., 2020, 14, 601193.
[http://dx.doi.org/10.3389/fnins.2020.601193] [PMID: 33424539]
[13]
Dixon, S.J.; Lemberg, K.M.; Lamprecht, M.R.; Skouta, R.; Zaitsev, E.M.; Gleason, C.E.; Patel, D.N.; Bauer, A.J.; Cantley, A.M.; Yang, W.S.; Morrison, B., III; Stockwell, B.R. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell, 2012, 149(5), 1060-1072.
[http://dx.doi.org/10.1016/j.cell.2012.03.042] [PMID: 22632970]
[14]
Cai, Y.; Yang, Z. Ferroptosis and its role in epilepsy. Front. Cell. Neurosci., 2021, 15, 696889.
[http://dx.doi.org/10.3389/fncel.2021.696889] [PMID: 34335189]
[15]
Stockwell, B.R.; Friedmann Angeli, J.P.; Bayir, H.; Bush, A.I.; Conrad, M.; Dixon, S.J.; Fulda, S.; Gascón, S.; Hatzios, S.K.; Kagan, V.E.; Noel, K.; Jiang, X.; Linkermann, A.; Murphy, M.E.; Overholtzer, M.; Oyagi, A.; Pagnussat, G.C.; Park, J.; Ran, Q.; Rosenfeld, C.S.; Salnikow, K.; Tang, D.; Torti, F.M.; Torti, S.V.; Toyokuni, S.; Woerpel, K.A.; Zhang, D.D. Ferroptosis: A regulated cell death nexus linking metabolism, redox biology, and disease. Cell, 2017, 171(2), 273-285.
[http://dx.doi.org/10.1016/j.cell.2017.09.021] [PMID: 28985560]
[16]
Galluzzi, L.; Vitale, I.; Aaronson, S.A.; Abrams, J.M.; Adam, D.; Agostinis, P.; Alnemri, E.S.; Altucci, L.; Amelio, I.; Andrews, D.W.; Annicchiarico-Petruzzelli, M.; Antonov, A.V.; Arama, E.; Baehrecke, E.H.; Barlev, N.A.; Bazan, N.G.; Bernassola, F.; Bertrand, M.J.M.; Bianchi, K.; Blagosklonny, M.V.; Blomgren, K.; Borner, C.; Boya, P.; Brenner, C.; Campanella, M.; Candi, E.; Carmona-Gutierrez, D.; Cecconi, F.; Chan, F.K.M.; Chandel, N.S.; Cheng, E.H.; Chipuk, J.E.; Cidlowski, J.A.; Ciechanover, A.; Cohen, G.M.; Conrad, M.; Cubillos-Ruiz, J.R.; Czabotar, P.E.; D’Angiolella, V.; Dawson, T.M.; Dawson, V.L.; De Laurenzi, V.; De Maria, R.; Debatin, K.M.; DeBerardinis, R.J.; Deshmukh, M.; Di Daniele, N.; Di Virgilio, F.; Dixit, V.M.; Dixon, S.J.; Duckett, C.S.; Dynlacht, B.D.; El-Deiry, W.S.; Elrod, J.W.; Fimia, G.M.; Fulda, S.; García-Sáez, A.J.; Garg, A.D.; Garrido, C.; Gavathiotis, E.; Golstein, P.; Gottlieb, E.; Green, D.R.; Greene, L.A.; Gronemeyer, H.; Gross, A.; Hajnoczky, G.; Hardwick, J.M.; Harris, I.S.; Hengartner, M.O.; Hetz, C.; Ichijo, H.; Jäättelä, M.; Joseph, B.; Jost, P.J.; Juin, P.P.; Kaiser, W.J.; Karin, M.; Kaufmann, T.; Kepp, O.; Kimchi, A.; Kitsis, R.N.; Klionsky, D.J.; Knight, R.A.; Kumar, S.; Lee, S.W.; Lemasters, J.J.; Levine, B.; Linkermann, A.; Lipton, S.A.; Lockshin, R.A.; López-Otín, C.; Lowe, S.W.; Luedde, T.; Lugli, E.; MacFarlane, M.; Madeo, F.; Malewicz, M.; Malorni, W.; Manic, G.; Marine, J.C.; Martin, S.J.; Martinou, J.C.; Medema, J.P.; Mehlen, P.; Meier, P.; Melino, S.; Miao, E.A.; Molkentin, J.D.; Moll, U.M.; Muñoz-Pinedo, C.; Nagata, S.; Nuñez, G.; Oberst, A.; Oren, M.; Overholtzer, M.; Pagano, M.; Panaretakis, T.; Pasparakis, M.; Penninger, J.M.; Pereira, D.M.; Pervaiz, S.; Peter, M.E.; Piacentini, M.; Pinton, P.; Prehn, J.H.M.; Puthalakath, H.; Rabinovich, G.A.; Rehm, M.; Rizzuto, R.; Rodrigues, C.M.P.; Rubinsztein, D.C.; Rudel, T.; Ryan, K.M.; Sayan, E.; Scorrano, L.; Shao, F.; Shi, Y.; Silke, J.; Simon, H.U.; Sistigu, A.; Stockwell, B.R.; Strasser, A.; Szabadkai, G.; Tait, S.W.G.; Tang, D.; Tavernarakis, N.; Thorburn, A.; Tsujimoto, Y.; Turk, B.; Vanden Berghe, T.; Vandenabeele, P.; Vander Heiden, M.G.; Villunger, A.; Virgin, H.W.; Vousden, K.H.; Vucic, D.; Wagner, E.F.; Walczak, H.; Wallach, D.; Wang, Y.; Wells, J.A.; Wood, W.; Yuan, J.; Zakeri, Z.; Zhivotovsky, B.; Zitvogel, L.; Melino, G.; Kroemer, G. Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death 2018. Cell Death Differ., 2018, 25(3), 486-541.
[http://dx.doi.org/10.1038/s41418-017-0012-4] [PMID: 29362479]
[17]
Yang, W.S.; Kim, K.J.; Gaschler, M.M.; Patel, M.; Shchepinov, M.S.; Stockwell, B.R. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc. Natl. Acad. Sci. USA, 2016, 113(34), E4966-E4975.
[http://dx.doi.org/10.1073/pnas.1603244113] [PMID: 27506793]
[18]
Chen, X.; Li, W.; Ren, J.; Huang, D.; He, W.; Song, Y.; Yang, C.; Li, W.; Zheng, X.; Chen, P.; Han, J. Translocation of mixed lineage kinase domain-like protein to plasma membrane leads to necrotic cell death. Cell Res., 2014, 24(1), 105-121.
[http://dx.doi.org/10.1038/cr.2013.171] [PMID: 24366341]
[19]
Matsuda, T.; Zhai, P.; Sciarretta, S.; Zhang, Y.; Jeong, J.I.; Ikeda, S.; Park, J.; Hsu, C.P.; Tian, B.; Pan, D.; Sadoshima, J.; Del Re, D.P. NF2 activates hippo signaling and promotes ischemia/reperfusion injury in the heart. Circ. Res., 2016, 119(5), 596-606.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.308586] [PMID: 27402866]
[20]
Ursini, F.; Maiorino, M.; Valente, M.; Ferri, L.; Gregolin, C. Purification from pig liver of a protein which protects liposomes and biomembranes from peroxidative degradation and exhibits glutathione peroxidase activity on phosphatidylcholine hydroperoxides. Biochim. Biophys. Acta Lipids Lipid Metab., 1982, 710(2), 197-211.
[http://dx.doi.org/10.1016/0005-2760(82)90150-3] [PMID: 7066358]
[21]
Mori, A.; Hiramatsu, M.; Yokoi, I.; Edamatsu, R. Biochemical pathogenesis of post-traumatic epilepsy. Pavlov. J. Biol. Sci., 1990, 25(2), 54-62.
[http://dx.doi.org/10.1007/BF02964604] [PMID: 2122401]
[22]
Gianazza, E.; Brioschi, M.; Fernandez, A.M.; Banfi, C. Lipoxidation in cardiovascular diseases. Redox Biol., 2019, 23, 101119.
[http://dx.doi.org/10.1016/j.redox.2019.101119] [PMID: 30833142]
[23]
Farzipour, S.; Shaghaghi, Z.; Motieian, S.; Alvandi, M.; Yazdi, A.; Asadzadeh, B.; Abbasi, S. Ferroptosis inhibitors as potential new therapeutic targets for cardiovascular disease. Mini Rev. Med. Chem., 2022, 22(17), 2271-2286.
[http://dx.doi.org/10.2174/1389557522666220218123404] [PMID: 35184711]
[24]
Akyuz, E.; Doganyigit, Z.; Eroglu, E.; Moscovicz, F.; Merelli, A.; Lazarowski, A.; Auzmendi, J. Myocardial iron overload in an experimental model of sudden unexpected death in epilepsy. Front. Neurol., 2021, 12, 609236.
[http://dx.doi.org/10.3389/fneur.2021.609236] [PMID: 33643194]
[25]
Pang, T.D.; Nearing, B.D.; Krishnamurthy, K.B.; Olin, B.; Schachter, S.C.; Verrier, R.L. Cardiac electrical instability in newly diagnosed/chronic epilepsy tracked by holter and ECG patch. Neurology, 2019, 93(10), 450-458.
[http://dx.doi.org/10.1212/WNL.0000000000008077] [PMID: 31477610]
[26]
Verrier, R.L.; Pang, T.D.; Nearing, B.D.; Schachter, S.C. The epileptic heart: Concept and clinical evidence. Epilepsy Behav., 2020, 105, 106946.
[http://dx.doi.org/10.1016/j.yebeh.2020.106946] [PMID: 32109857]
[27]
Verrier, R.L.; Pang, T.D.; Nearing, B.D.; Schachter, S.C.; Prolonged, Q.T. Prolonged QT interval predicts all-cause mortality in epilepsy patients: Diagnostic and therapeutic implications. Heart Rhythm, 2022, 19(4), 585-587.
[http://dx.doi.org/10.1016/j.hrthm.2022.01.015] [PMID: 35033664]
[28]
Gatto, E.M.; Zurrú, C.M.; González, M.A.; Prolonged, Q.T. Prolonged QT syndrome presenting as epilepsy. Neurology, 1996, 46(4), 1188.
[http://dx.doi.org/10.1212/WNL.46.4.1188] [PMID: 8780130]
[29]
Tigaran, S.; Mølgaard, H.; McClelland, R.; Dam, M.; Jaffe, A.S. Evidence of cardiac ischemia during seizures in drug refractory epilepsy patients. Neurology, 2003, 60(3), 492-495.
[http://dx.doi.org/10.1212/01.WNL.0000042090.13247.48] [PMID: 12578934]
[30]
Auzmendi, J.; Salgueiro, J.; Canellas, C.; Zubillaga, M.; Men, P.; Alicia, R.; Merelli, A.; Buchholz, B.; Ricardo, G.; Ramos, A.J.; Lazarowski, A.L. Pilocarpine-induced status epilepticus (SE) induces functional and histological p-glycoprotein overexpression in cardiomyocytes, heart dysfunction and high ratio of sudden death in rats. Pharmaceuticals, 2018, 11(1), 21.
[31]
Tang, D.; Kroemer, G. Ferroptosis. Curr. Biol., 2020, 30(21), R1292-R1297.
[http://dx.doi.org/10.1016/j.cub.2020.09.068] [PMID: 33142092]
[32]
Auzmendi, J.; Buchholz, B.; Salguero, J.; Cañellas, C.; Kelly, J.; Men, P.; Zubillaga, M.; Rossi, A.; Merelli, A.; Gelpi, R.; Ramos, A.; Lazarowski, A. Pilocarpine-induced status epilepticus is associated with p-glycoprotein induction in cardiomyocytes, electrocardiographic changes, and sudden death. Pharmaceuticals (Basel), 2018, 11(1), 21.
[http://dx.doi.org/10.3390/ph11010021] [PMID: 29462915]
[33]
Auzmendi, J.; Puchulu, M.B.; Rodríguez, J.C.G.; Balaszczuk, A.M.; Lazarowski, A.; Merelli, A. EPO and EPO-receptor system as potential actionable mechanism for the protection of brain and heart in refractory epilepsy and SUDEP. Curr. Pharm. Des., 2020, 26(12), 1356-1364.
[http://dx.doi.org/10.2174/1381612826666200219095548] [PMID: 32072891]
[34]
Auzmendi, J.; Lazarowski, A. Seizures induces hypoxia and hypoxia induces seizures: A perverse relationship that increases the risk of SUDEP. Neurol. Disord. Epilepsy J., 2020, 3(2), 135.
[35]
Hentze, M.W.; Muckenthaler, M.U.; Galy, B.; Camaschella, C. Two to tango: Regulation of mammalian iron metabolism. Cell, 2010, 142(1), 24-38.
[http://dx.doi.org/10.1016/j.cell.2010.06.028] [PMID: 20603012]
[36]
Fang, X.; Cai, Z.; Wang, H.; Han, D.; Cheng, Q.; Zhang, P.; Gao, F.; Yu, Y.; Song, Z.; Wu, Q.; An, P.; Huang, S.; Pan, J.; Chen, H.Z.; Chen, J.; Linkermann, A.; Min, J.; Wang, F. Loss of cardiac ferritin h facilitates cardiomyopathy via Slc7a11-mediated ferroptosis. Circ. Res., 2020, 127(4), 486-501.
[http://dx.doi.org/10.1161/CIRCRESAHA.120.316509] [PMID: 32349646]
[37]
Stockwell, B.R. A powerful cell-protection system prevents cell death by ferroptosis. Nature, 2019, 575(7784), 597-598.
[http://dx.doi.org/10.1038/d41586-019-03145-8] [PMID: 31768036]
[38]
Wagner, C.A.; Lang, F.; Bröer, S. Function and structure of heterodimeric amino acid transporters. Am. J. Physiol. Cell Physiol., 2001, 281(4), C1077-C1093.
[http://dx.doi.org/10.1152/ajpcell.2001.281.4.C1077] [PMID: 11546643]
[39]
Xie, Y.; Hou, W.; Song, X.; Yu, Y.; Huang, J.; Sun, X.; Kang, R.; Tang, D. Ferroptosis: Process and function. Cell Death Differ., 2016, 23(3), 369-379.
[http://dx.doi.org/10.1038/cdd.2015.158] [PMID: 26794443]
[40]
Hai, T.; Hartman, M.G. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: Activating transcription factor proteins and homeostasis. Gene, 2001, 273(1), 1-11.
[http://dx.doi.org/10.1016/S0378-1119(01)00551-0] [PMID: 11483355]
[41]
Tang, Y.; Pacary, E.; Fréret, T.; Divoux, D.; Petit, E.; Schumann-Bard, P.; Bernaudin, M. Effect of hypoxic preconditioning on brain genomic response before and following ischemia in the adult mouse: Identification of potential neuroprotective candidates for stroke. Neurobiol. Dis., 2006, 21(1), 18-28.
[http://dx.doi.org/10.1016/j.nbd.2005.06.002] [PMID: 16040250]
[42]
Wang, L.; Liu, Y.; Du, T.; Yang, H.; Lei, L.; Guo, M.; Ding, H.F.; Zhang, J.; Wang, H.; Chen, X.; Yan, C. ATF3 promotes erastin-induced ferroptosis by suppressing system Xc–. Cell Death Differ., 2020, 27(2), 662-675.
[http://dx.doi.org/10.1038/s41418-019-0380-z] [PMID: 31273299]
[43]
Wu, X.; Li, Y.; Zhang, S.; Zhou, X. Ferroptosis as a novel therapeutic target for cardiovascular disease. Theranostics, 2021, 11(7), 3052-3059.
[http://dx.doi.org/10.7150/thno.54113] [PMID: 33537073]
[44]
Ursini, F.; Maiorino, M. Lipid peroxidation and ferroptosis: The role of GSH and GPx4. Free Radic. Biol. Med., 2020, 152, 175-185.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.02.027] [PMID: 32165281]
[45]
Baluchnejadmojarad, T.; Roghani, M. Coenzyme q10 ameliorates neurodegeneration, mossy fiber sprouting, and oxidative stress in intrahippocampal kainate model of temporal lobe epilepsy in rat. J. Mol. Neurosci., 2013, 49(1), 194-201.
[http://dx.doi.org/10.1007/s12031-012-9886-2] [PMID: 23008120]
[46]
Zou, X.; Jiang, S.; Wu, Z.; Shi, Y.; Cai, S.; Zhu, R.; Chen, L. Effectiveness of deferoxamine on ferric chloride-induced epilepsy in rats. Brain Res., 2017, 1658, 25-30.
[http://dx.doi.org/10.1016/j.brainres.2017.01.001] [PMID: 28063856]
[47]
Ye, Q.; Zeng, C.; Luo, C.; Wu, Y. Ferrostatin-1 mitigates cognitive impairment of epileptic rats by inhibiting P38 MAPK activation. Epilepsy Behav., 2020, 103(Pt A), 106670.
[http://dx.doi.org/10.1016/j.yebeh.2019.106670]
[48]
Aisen, P.; Enns, C.; Wessling-Resnick, M. Chemistry and biology of eukaryotic iron metabolism. Int. J. Biochem. Cell Biol., 2001, 33(10), 940-959.
[http://dx.doi.org/10.1016/S1357-2725(01)00063-2] [PMID: 11470229]
[49]
Lieu, P.T.; Heiskala, M.; Peterson, P.A.; Yang, Y. The roles of iron in health and disease. Mol. Aspects Med., 2001, 22(1-2), 1-87.
[http://dx.doi.org/10.1016/S0098-2997(00)00006-6] [PMID: 11207374]
[50]
Gulec, S.; Anderson, G.J.; Collins, J.F. Mechanistic and regulatory aspects of intestinal iron absorption. Am. J. Physiol. Gastrointest. Liver Physiol., 2014, 307(4), G397-G409.
[http://dx.doi.org/10.1152/ajpgi.00348.2013] [PMID: 24994858]
[51]
Li, J.; Cao, F.; Yin, H.; Huang, Z.; Lin, Z.; Mao, N.; Sun, B.; Wang, G. Ferroptosis: past, present and future. Cell Death Dis., 2020, 11(2), 88.
[http://dx.doi.org/10.1038/s41419-020-2298-2] [PMID: 32015325]
[52]
San Martin, C.D.; Garri, C.; Pizarro, F.; Walter, T.; Theil, E.C.; Núñez, M.T. Caco-2 intestinal epithelial cells absorb soybean ferritin by mu2 (AP2)-dependent endocytosis. J. Nutr., 2008, 138(4), 659-666.
[http://dx.doi.org/10.1093/jn/138.4.659] [PMID: 18356317]
[53]
Morgan, E.H.; Oates, P.S. Mechanisms and regulation of intestinal iron absorption. Blood Cells Mol. Dis., 2002, 29(3), 384-399.
[http://dx.doi.org/10.1006/bcmd.2002.0578] [PMID: 12547229]
[54]
Courville, P.; Chaloupka, R.; Cellier, M.F.M. Recent progress in structure–function analyses of Nramp proton-dependent metal-ion transporters membrane proteins in health and disease. Biochem. Cell Biol., 2006, 84(6), 960-978.
[http://dx.doi.org/10.1139/o06-193] [PMID: 17215883]
[55]
Shawki, A.; Engevik, M.A.; Kim, R.S.; Knight, P.B.; Baik, R.A.; Anthony, S.R.; Worrell, R.T.; Shull, G.E.; Mackenzie, B. Intestinal brush-border Na+/H+ exchanger-3 drives H+-coupled iron absorption in the mouse. Am. J. Physiol. Gastrointest. Liver Physiol., 2016, 311(3), G423-G430.
[http://dx.doi.org/10.1152/ajpgi.00167.2016] [PMID: 27390324]
[56]
McKie, A.T.; Barrow, D.; Latunde-Dada, G.O.; Rolfs, A.; Sager, G.; Mudaly, E.; Mudaly, M.; Richardson, C.; Barlow, D.; Bomford, A.; Peters, T.J.; Raja, K.B.; Shirali, S.; Hediger, M.A.; Farzaneh, F.; Simpson, R.J. An iron-regulated ferric reductase associated with the absorption of dietary iron. Science, 2001, 291(5509), 1755-1759.
[http://dx.doi.org/10.1126/science.1057206] [PMID: 11230685]
[57]
Schlottmann, F.; Vera-Aviles, M.; Latunde-Dada, G.O. Duodenal cytochrome b (Cybrd1) ferric reductase functional studies in cells. Metallomics, 2017, 9(10), 1389-1393.
[http://dx.doi.org/10.1039/C7MT00254H] [PMID: 28937159]
[58]
Chiabrando, D.; Vinchi, F.; Fiorito, V.; Mercurio, S.; Tolosano, E. Heme in pathophysiology: A matter of scavenging, metabolism and trafficking across cell membranes. Front. Pharmacol., 2014, 5, 61.
[http://dx.doi.org/10.3389/fphar.2014.00061] [PMID: 24782769]
[59]
Parmley, R.T.; Barton, J.C.; Conrad, M.E.; Austin, R.L.; Holland, R.M. Ultrastructural cytochemistry and radioautography of hemoglobin-iron absorption. Exp. Mol. Pathol., 1981, 34(2), 131-144.
[http://dx.doi.org/10.1016/0014-4800(81)90070-8] [PMID: 7202683]
[60]
Le Blanc, S.; Garrick, M.D.; Arredondo, M. Heme carrier protein 1 transports heme and is involved in heme-Fe metabolism. Am. J. Physiol. Cell Physiol., 2012, 302(12), C1780-C1785.
[http://dx.doi.org/10.1152/ajpcell.00080.2012] [PMID: 22496243]
[61]
Shayeghi, M.; Latunde-Dada, G.O.; Oakhill, J.S.; Laftah, A.H.; Takeuchi, K.; Halliday, N.; Khan, Y.; Warley, A.; McCann, F.E.; Hider, R.C.; Frazer, D.M.; Anderson, G.J.; Vulpe, C.D.; Simpson, R.J.; McKie, A.T. Identification of an intestinal heme transporter. Cell, 2005, 122(5), 789-801.
[http://dx.doi.org/10.1016/j.cell.2005.06.025] [PMID: 16143108]
[62]
Hooda, J.; Shah, A.; Zhang, L. Heme, an essential nutrient from dietary proteins, critically impacts diverse physiological and pathological processes. Nutrients, 2014, 6(3), 1080-1102.
[http://dx.doi.org/10.3390/nu6031080] [PMID: 24633395]
[63]
Yang, X.; Chen-Barrett, Y.; Arosio, P.; Chasteen, N.D. Reaction paths of iron oxidation and hydrolysis in horse spleen and recombinant human ferritins. Biochemistry, 1998, 37(27), 9743-9750.
[http://dx.doi.org/10.1021/bi973128a] [PMID: 9657687]
[64]
Liu, X.B.; Yang, F.; Haile, D.J. Functional consequences of ferroportin 1 mutations. Blood Cells Mol. Dis., 2005, 35(1), 33-46.
[http://dx.doi.org/10.1016/j.bcmd.2005.04.005] [PMID: 15935710]
[65]
Qiu, A.; Jansen, M.; Sakaris, A.; Min, S.H.; Chattopadhyay, S.; Tsai, E.; Sandoval, C.; Zhao, R.; Akabas, M.H.; Goldman, I.D. Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption. Cell, 2006, 127(5), 917-928.
[http://dx.doi.org/10.1016/j.cell.2006.09.041] [PMID: 17129779]
[66]
Vulpe, C.D.; Kuo, Y.M.; Murphy, T.L.; Cowley, L.; Askwith, C.; Libina, N.; Gitschier, J.; Anderson, G.J. Hephaestin, a ceruloplasmin homologue implicated in intestinal iron transport, is defective in the SLA mouse. Nat. Genet., 1999, 21(2), 195-199.
[http://dx.doi.org/10.1038/5979] [PMID: 9988272]
[67]
Daher, R.; Manceau, H.; Karim, Z. Iron metabolism and the role of the iron-regulating hormone hepcidin in health and disease. Presse Med., 2017, 46(12), e272-e278.
[http://dx.doi.org/10.1016/j.lpm.2017.10.006] [PMID: 29129410]
[68]
Yeh, K.; Yeh, M.; Mims, L.; Glass, J. Iron feeding induces ferroportin 1 and hephaestin migration and interaction in rat duodenal epithelium. Am. J. Physiol. Gastrointest. Liver Physiol., 2009, 296(1), G55-G65.
[http://dx.doi.org/10.1152/ajpgi.90298.2008] [PMID: 18974313]
[69]
Knutson, M.D. Iron-sensing proteins that regulate hepcidin and enteric iron absorption. Annu. Rev. Nutr., 2010, 30(1), 149-171.
[http://dx.doi.org/10.1146/annurev.nutr.012809.104801] [PMID: 20415583]
[70]
Kawabata, H. Transferrin and transferrin receptors update. Free Radic. Biol. Med., 2019, 133, 46-54.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.06.037] [PMID: 29969719]
[71]
Gammella, E.; Buratti, P.; Cairo, G.; Recalcati, S. The transferrin receptor: The cellular iron gate. Metallomics, 2017, 9(10), 1367-1375.
[http://dx.doi.org/10.1039/C7MT00143F] [PMID: 28671201]
[72]
El Hout, M.; Dos Santos, L.; Hamaï, A.; Mehrpour, M. A promising new approach to cancer therapy: Targeting iron metabolism in cancer stem cells. Semin. Cancer Biol., 2018, 53, 125-138.
[http://dx.doi.org/10.1016/j.semcancer.2018.07.009] [PMID: 30071257]
[73]
Feng, H.; Schorpp, K.; Jin, J.; Yozwiak, C.E.; Hoffstrom, B.G.; Decker, A.M.; Rajbhandari, P.; Stokes, M.E.; Bender, H.G.; Csuka, J.M.; Upadhyayula, P.S.; Canoll, P.; Uchida, K.; Soni, R.K.; Hadian, K.; Stockwell, B.R. Transferrin receptor is a specific ferroptosis marker. Cell Rep., 2020, 30(10), 3411-3423.e7.
[http://dx.doi.org/10.1016/j.celrep.2020.02.049] [PMID: 32160546]
[74]
Yan, H.; Zou, T.; Tuo, Q.; Xu, S.; Li, H.; Belaidi, A.A.; Lei, P. Ferroptosis: Mechanisms and links with diseases. Signal Transduct. Target. Ther., 2021, 6(1), 49.
[http://dx.doi.org/10.1038/s41392-020-00428-9] [PMID: 33536413]
[75]
Gao, M.; Monian, P.; Quadri, N.; Ramasamy, R.; Jiang, X. Glutaminolysis and transferrin regulate ferroptosis. Mol. Cell, 2015, 59(2), 298-308.
[http://dx.doi.org/10.1016/j.molcel.2015.06.011] [PMID: 26166707]
[76]
Sun, X.; Ou, Z.; Xie, M.; Kang, R.; Fan, Y.; Niu, X.; Wang, H.; Cao, L.; Tang, D. HSPB1 as a novel regulator of ferroptotic cancer cell death. Oncogene, 2015, 34(45), 5617-5625.
[http://dx.doi.org/10.1038/onc.2015.32] [PMID: 25728673]
[77]
Wang, Z.; Ding, Y.; Wang, X.; Lu, S.; Wang, C.; He, C.; Wang, L.; Piao, M.; Chi, G.; Luo, Y.; Ge, P. Pseudolaric acid B triggers ferroptosis in glioma cells via activation of Nox4 and inhibition of xCT. Cancer Lett., 2018, 428, 21-33.
[http://dx.doi.org/10.1016/j.canlet.2018.04.021] [PMID: 29702192]
[78]
Gao, G.; Li, J.; Zhang, Y.; Chang, Y.Z. Cellular iron metabolism and regulation. Adv. Exp. Med. Biol., 2019, 1173, 21-32.
[http://dx.doi.org/10.1007/978-981-13-9589-5_2] [PMID: 31456203]
[79]
Fuhrmann, D.C.; Mondorf, A.; Beifuß, J.; Jung, M.; Brüne, B. Hypoxia inhibits ferritinophagy, increases mitochondrial ferritin, and protects from ferroptosis. Redox Biol., 2020, 36, 101670.
[http://dx.doi.org/10.1016/j.redox.2020.101670] [PMID: 32810738]
[80]
Kim, S.E.; Zhang, L.; Ma, K.; Riegman, M.; Chen, F.; Ingold, I.; Conrad, M.; Turker, M.Z.; Gao, M.; Jiang, X.; Monette, S.; Pauliah, M.; Gonen, M.; Zanzonico, P.; Quinn, T.; Wiesner, U.; Bradbury, M.S.; Overholtzer, M. Ultrasmall nanoparticles induce ferroptosis in nutrient-deprived cancer cells and suppress tumour growth. Nat. Nanotechnol., 2016, 11(11), 977-985.
[http://dx.doi.org/10.1038/nnano.2016.164] [PMID: 27668796]
[81]
Basuli, D.; Tesfay, L.; Deng, Z.; Paul, B.; Yamamoto, Y.; Ning, G.; Xian, W.; McKeon, F.; Lynch, M.; Crum, C.P.; Hegde, P.; Brewer, M.; Wang, X.; Miller, L.D.; Dyment, N.; Torti, F.M.; Torti, S.V. Iron addiction: A novel therapeutic target in ovarian cancer. Oncogene, 2017, 36(29), 4089-4099.
[http://dx.doi.org/10.1038/onc.2017.11] [PMID: 28319068]
[82]
Adedoyin, O.; Boddu, R.; Traylor, A.; Lever, J.M.; Bolisetty, S.; George, J.F.; Agarwal, A. Heme oxygenase-1 mitigates ferroptosis in renal proximal tubule cells. Am. J. Physiol. Renal Physiol., 2018, 314(5), F702-F714.
[http://dx.doi.org/10.1152/ajprenal.00044.2017] [PMID: 28515173]
[83]
Doll, S.; Conrad, M. Iron and ferroptosis: A still ill-defined liaison. IUBMB Life, 2017, 69(6), 423-434.
[http://dx.doi.org/10.1002/iub.1616] [PMID: 28276141]
[84]
Ferreira, C.A.; Ni, D.; Rosenkrans, Z.T.; Cai, W. Scavenging of reactive oxygen and nitrogen species with nanomaterials. Nano Res., 2018, 11(10), 4955-4984.
[http://dx.doi.org/10.1007/s12274-018-2092-y] [PMID: 30450165]
[85]
Dröge, W. Free radicals in the physiological control of cell function. Physiol. Rev., 2002, 82(1), 47-95.
[http://dx.doi.org/10.1152/physrev.00018.2001] [PMID: 11773609]
[86]
Bystrom, L.M.; Guzman, M.L.; Rivella, S. Iron and reactive oxygen species: Friends or foes of cancer cells? Antioxid. Redox Signal., 2014, 20(12), 1917-1924.
[http://dx.doi.org/10.1089/ars.2012.5014] [PMID: 23198911]
[87]
Nita, M.; Grzybowski, A. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxid. Med. Cell. Longev., 2016, 2016, 3164734.
[http://dx.doi.org/10.1155/2016/3164734] [PMID: 26881021]
[88]
Shahidi, F.; Zhong, Y. Novel antioxidants in food quality preservation and health promotion. Eur. J. Lipid Sci. Technol., 2010, 112(9), 930-940.
[http://dx.doi.org/10.1002/ejlt.201000044]
[89]
Amer, J.; Ghoti, H.; Rachmilewitz, E.; Koren, A.; Levin, C.; Fibach, E. Red blood cells, platelets and polymorphonuclear neutrophils of patients with sickle cell disease exhibit oxidative stress that can be ameliorated by antioxidants. Br. J. Haematol., 2006, 132(1), 108-113.
[http://dx.doi.org/10.1111/j.1365-2141.2005.05834.x] [PMID: 16371026]
[90]
Sakellariou, G.K.; Jackson, M.J.; Vasilaki, A. Redefining the major contributors to superoxide production in contracting skeletal muscle. The role of NAD(P)H oxidases. Free Radic. Res., 2014, 48(1), 12-29.
[http://dx.doi.org/10.3109/10715762.2013.830718] [PMID: 23915064]
[91]
Guerriero, G.; Trocchia, S.; Abdel-Gawad, F.K.; Ciarcia, G. Roles of reactive oxygen species in the spermatogenesis regulation. Front. Endocrinol. (Lausanne), 2014, 5, 56.
[http://dx.doi.org/10.3389/fendo.2014.00056] [PMID: 24795696]
[92]
Izyumov, D.S.; Domnina, L.V.; Nepryakhina, O.K.; Avetisyan, A.V.; Golyshev, S.A.; Ivanova, O.Y.; Korotetskaya, M.V.; Lyamzaev, K.G.; Pletjushkina, O.Y.; Popova, E.N.; Chernyak, B.V. Mitochondria as source of reactive oxygen species under oxidative stress. Study with novel mitochondria-targeted antioxidants - the “Skulachev-ion” derivatives. Biochemistry (Mosc.), 2010, 75(2), 123-129.
[http://dx.doi.org/10.1134/S000629791002001X] [PMID: 20367598]
[93]
Lassègue, B.; San Martín, A.; Griendling, K.K. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ. Res., 2012, 110(10), 1364-1390.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.243972] [PMID: 22581922]
[94]
D’Autréaux, B.; Toledano, M.B. ROS as signalling molecules: Mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol., 2007, 8(10), 813-824.
[http://dx.doi.org/10.1038/nrm2256] [PMID: 17848967]
[95]
Auten, R.L.; Davis, J.M. Oxygen toxicity and reactive oxygen species: The devil is in the details. Pediatr. Res., 2009, 66(2), 121-127.
[http://dx.doi.org/10.1203/PDR.0b013e3181a9eafb] [PMID: 19390491]
[96]
Wen, X.; Wu, J.; Wang, F.; Liu, B.; Huang, C.; Wei, Y. Deconvoluting the role of reactive oxygen species and autophagy in human diseases. Free Radic. Biol. Med., 2013, 65, 402-410.
[http://dx.doi.org/10.1016/j.freeradbiomed.2013.07.013] [PMID: 23872397]
[97]
Yang, W.S.; Stockwell, B.R. Ferroptosis: Death by lipid peroxidation. Trends Cell Biol., 2016, 26(3), 165-176.
[http://dx.doi.org/10.1016/j.tcb.2015.10.014] [PMID: 26653790]
[98]
Conrad, M.; Pratt, D.A. The chemical basis of ferroptosis. Nat. Chem. Biol., 2019, 15(12), 1137-1147.
[http://dx.doi.org/10.1038/s41589-019-0408-1] [PMID: 31740834]
[99]
Wenzel, S.E.; Tyurina, Y.Y.; Zhao, J.; St Croix, C.M.; Dar, H.H.; Mao, G.; Tyurin, V.A.; Anthonymuthu, T.S.; Kapralov, A.A.; Amoscato, A.A.; Mikulska-Ruminska, K.; Shrivastava, I.H.; Kenny, E.M.; Yang, Q.; Rosenbaum, J.C.; Sparvero, L.J.; Emlet, D.R.; Wen, X.; Minami, Y.; Qu, F.; Watkins, S.C.; Holman, T.R.; VanDemark, A.P.; Kellum, J.A.; Bahar, I.; Bayır, H.; Kagan, V.E. PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell, 2017, 171(3), 628-641.e26.
[http://dx.doi.org/10.1016/j.cell.2017.09.044] [PMID: 29053969]
[100]
Yin, H.; Xu, L.; Porter, N.A. Free radical lipid peroxidation: Mechanisms and analysis. Chem. Rev., 2011, 111(10), 5944-5972.
[http://dx.doi.org/10.1021/cr200084z] [PMID: 21861450]
[101]
Lee, J.Y.; Kim, W.K.; Bae, K.H.; Lee, S.C.; Lee, E.W. Lipid metabolism and ferroptosis. Biology (Basel), 2021, 10(3), 184.
[http://dx.doi.org/10.3390/biology10030184] [PMID: 33801564]
[102]
Kagan, V.E.; Mao, G.; Qu, F.; Angeli, J.P.F.; Doll, S.; Croix, C.S.; Dar, H.H.; Liu, B.; Tyurin, V.A.; Ritov, V.B.; Kapralov, A.A.; Amoscato, A.A.; Jiang, J.; Anthonymuthu, T.; Mohammadyani, D.; Yang, Q.; Proneth, B.; Klein-Seetharaman, J.; Watkins, S.; Bahar, I.; Greenberger, J.; Mallampalli, R.K.; Stockwell, B.R.; Tyurina, Y.Y.; Conrad, M.; Bayır, H. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat. Chem. Biol., 2017, 13(1), 81-90.
[http://dx.doi.org/10.1038/nchembio.2238] [PMID: 27842066]
[103]
Panaroni, C.; Fulzele, K.; Soucy, R.; Siu, K.T.; Mukaihara, K.; Huang, C.; Chattopadhyay, S.; Raje, N. Arachidonic acid induces ferroptosis-mediated cell-death in multiple myeloma. Blood, 2018, 132(Suppl. 1), 4498-4498.
[http://dx.doi.org/10.1182/blood-2018-99-118482]
[104]
Dixon, S.J.; Winter, G.E.; Musavi, L.S.; Lee, E.D.; Snijder, B.; Rebsamen, M.; Superti-Furga, G.; Stockwell, B.R. Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem. Biol., 2015, 10(7), 1604-1609.
[http://dx.doi.org/10.1021/acschembio.5b00245] [PMID: 25965523]
[105]
Doll, S.; Proneth, B.; Tyurina, Y.Y.; Panzilius, E.; Kobayashi, S.; Ingold, I.; Irmler, M.; Beckers, J.; Aichler, M.; Walch, A.; Prokisch, H.; Trümbach, D.; Mao, G.; Qu, F.; Bayir, H.; Füllekrug, J.; Scheel, C.H.; Wurst, W.; Schick, J.A.; Kagan, V.E.; Angeli, J.P.F.; Conrad, M. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat. Chem. Biol., 2017, 13(1), 91-98.
[http://dx.doi.org/10.1038/nchembio.2239] [PMID: 27842070]
[106]
Skouta, R.; Dixon, S.J.; Wang, J.; Dunn, D.E.; Orman, M.; Shimada, K.; Rosenberg, P.A.; Lo, D.C.; Weinberg, J.M.; Linkermann, A.; Stockwell, B.R. Ferrostatins inhibit oxidative lipid damage and cell death in diverse disease models. J. Am. Chem. Soc., 2014, 136(12), 4551-4556.
[http://dx.doi.org/10.1021/ja411006a] [PMID: 24592866]
[107]
Friedmann Angeli, J.P.; Schneider, M.; Proneth, B.; Tyurina, Y.Y.; Tyurin, V.A.; Hammond, V.J.; Herbach, N.; Aichler, M.; Walch, A.; Eggenhofer, E.; Basavarajappa, D.; Rådmark, O.; Kobayashi, S.; Seibt, T.; Beck, H.; Neff, F.; Esposito, I.; Wanke, R.; Förster, H.; Yefremova, O.; Heinrichmeyer, M.; Bornkamm, G.W.; Geissler, E.K.; Thomas, S.B.; Stockwell, B.R.; O’Donnell, V.B.; Kagan, V.E.; Schick, J.A.; Conrad, M. Inactivation of the ferroptosis regulator Gpx4 triggers acute renal failure in mice. Nat. Cell Biol., 2014, 16(12), 1180-1191.
[http://dx.doi.org/10.1038/ncb3064] [PMID: 25402683]
[108]
Küch, E.M.; Vellaramkalayil, R.; Zhang, I.; Lehnen, D.; Brügger, B.; Stremmel, W.; Ehehalt, R.; Poppelreuther, M.; Füllekrug, J. Differentially localized acyl-CoA synthetase 4 isoenzymes mediate the metabolic channeling of fatty acids towards phosphatidylinositol. Biochim. Biophys. Acta Mol. Cell Biol. Lipids, 2014, 1841(2), 227-239.
[http://dx.doi.org/10.1016/j.bbalip.2013.10.018] [PMID: 24201376]
[109]
Lei, P.; Bai, T.; Sun, Y. Mechanisms of ferroptosis and relations with regulated cell death: A review. Front. Physiol., 2019, 10, 139.
[http://dx.doi.org/10.3389/fphys.2019.00139] [PMID: 30863316]
[110]
Kuhn, H.; Saam, J.; Eibach, S.; Holzhütter, H.G.; Ivanov, I.; Walther, M. Structural biology of mammalian lipoxygenases: Enzymatic consequences of targeted alterations of the protein structure. Biochem. Biophys. Res. Commun., 2005, 338(1), 93-101.
[http://dx.doi.org/10.1016/j.bbrc.2005.08.238] [PMID: 16168952]
[111]
Hishikawa, D.; Shindou, H.; Kobayashi, S.; Nakanishi, H.; Taguchi, R.; Shimizu, T. Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proc. Natl. Acad. Sci. USA, 2008, 105(8), 2830-2835.
[http://dx.doi.org/10.1073/pnas.0712245105] [PMID: 18287005]
[112]
Ayala, A.; Muñoz, M.F.; Argüelles, S. Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid. Med. Cell. Longev., 2014, 2014, 360438.
[http://dx.doi.org/10.1155/2014/360438] [PMID: 24999379]
[113]
Reis, A.; Spickett, C.M. Chemistry of phospholipid oxidation. Biochim. Biophys. Acta Biomembr., 2012, 1818(10), 2374-2387.
[http://dx.doi.org/10.1016/j.bbamem.2012.02.002] [PMID: 22342938]
[114]
Chen, J.J.; Galluzzi, L. Fighting resilient cancers with iron. Trends Cell Biol., 2018, 28(2), 77-78.
[http://dx.doi.org/10.1016/j.tcb.2017.11.007] [PMID: 29223642]
[115]
Xiao, Y.; Meierhofer, D. Glutathione metabolism in renal cell carcinoma progression and implications for therapies. Int. J. Mol. Sci., 2019, 20(15), 3672.
[http://dx.doi.org/10.3390/ijms20153672] [PMID: 31357507]
[116]
Pizzorno, J. Glutathione. Interg. Med., 2014, 13(1), 8-12.
[117]
Liang, C.; Zhang, X.; Yang, M.; Dong, X. Recent progress in ferroptosis inducers for cancer therapy. Adv. Mater., 2019, 31(51), 1904197.
[http://dx.doi.org/10.1002/adma.201904197] [PMID: 31595562]
[118]
Zhang, L.; Wang, L.; Ning, F-B.; Wang, T.; Liang, Y-C.; Liu, Y-L. Erythropoietin reduces hippocampus injury in neonatal rats with hypoxic ischemic brain damage via targeting matrix metalloprotein-2. Eur. Rev. Med. Pharmacol. Sci., 2017, 21(19), 4327-4333.
[PMID: 29077163]
[119]
Meister, A. Glutathione; Metabolism and function via the γ-glutamyl cycle. Life Sci., 1974, 15(2), 177-190.
[http://dx.doi.org/10.1016/0024-3205(74)90206-9] [PMID: 4620960]
[120]
Meister, A. The gamma-glutamyl cycle. Diseases associated with specific enzyme deficiencies. Ann. Intern. Med., 1974, 81(2), 247-253.
[http://dx.doi.org/10.7326/0003-4819-81-2-247] [PMID: 4152527]
[121]
Stark, A.A.; Porat, N.; Volohonsky, G.; Komlosh, A.; Bluvshtein, E.; Tubi, C.; Steinberg, P. The role of γ-glutamyl transpeptidase in the biosynthesis of glutathione. Biofactors, 2003, 17(1-4), 139-149.
[http://dx.doi.org/10.1002/biof.5520170114] [PMID: 12897436]
[122]
Bjørklund, G.; Tinkov, A.A.; Hosnedlová, B.; Kizek, R.; Ajsuvakova, O.P.; Chirumbolo, S.; Skalnaya, M.G.; Peana, M.; Dadar, M.; El-Ansary, A.; Qasem, H.; Adams, J.B.; Aaseth, J.; Skalny, A.V. The role of glutathione redox imbalance in autism spectrum disorder: A review. Free Radic. Biol. Med., 2020, 160, 149-162.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.07.017] [PMID: 32745763]
[123]
Cozza, G.; Rossetto, M.; Bosello-Travain, V.; Maiorino, M.; Roveri, A.; Toppo, S.; Zaccarin, M.; Zennaro, L.; Ursini, F. Glutathione peroxidase 4-catalyzed reduction of lipid hydroperoxides in membranes: The polar head of membrane phospholipids binds the enzyme and addresses the fatty acid hydroperoxide group toward the redox center. Free Radic. Biol. Med., 2017, 112, 1-11.
[http://dx.doi.org/10.1016/j.freeradbiomed.2017.07.010] [PMID: 28709976]
[124]
Lewerenz, J.; Hewett, S.J.; Huang, Y.; Lambros, M.; Gout, P.W.; Kalivas, P.W.; Massie, A.; Smolders, I.; Methner, A.; Pergande, M.; Smith, S.B.; Ganapathy, V.; Maher, P. The cystine/glutamate antiporter system x(c)(-) in health and disease: from molecular mechanisms to novel therapeutic opportunities. Antioxid. Redox Signal., 2013, 18(5), 522-555.
[http://dx.doi.org/10.1089/ars.2011.4391] [PMID: 22667998]
[125]
Bannai, S.; Kitamura, E. Transport interaction of L-cystine and L-glutamate in human diploid fibroblasts in culture. J. Biol. Chem., 1980, 255(6), 2372-2376.
[http://dx.doi.org/10.1016/S0021-9258(19)85901-X] [PMID: 7358676]
[126]
Gochenauer, G.E.; Robinson, M.B. Dibutyryl-cAMP (dbcAMP) up-regulates astrocytic chloride-dependent l-[3H]glutamate transport and expression of both system xc− subunits. J. Neurochem., 2001, 78(2), 276-286.
[http://dx.doi.org/10.1046/j.1471-4159.2001.00385.x] [PMID: 11461963]
[127]
Patel, S.A.; Warren, B.A.; Rhoderick, J.F.; Bridges, R.J. Differentiation of substrate and non-substrate inhibitors of transport system xc−: an obligate exchanger of L-glutamate and L-cystine. Neuropharmacology, 2004, 46(2), 273-284.
[http://dx.doi.org/10.1016/j.neuropharm.2003.08.006] [PMID: 14680765]
[128]
Liu, L.; Liu, R.; Liu, Y.; Li, G.; Chen, Q.; Liu, X.; Ma, S. Cystine-glutamate antiporter XCT as a therapeutic target for cancer. Cell Biochem. Funct., 2021, 39(2), 174-179.
[http://dx.doi.org/10.1002/cbf.3581] [PMID: 32749001]
[129]
Yamaguchi, I.; Yoshimura, S.H.; Katoh, H. High cell density increases glioblastoma cell viability under glucose deprivation via degradation of the cystine/glutamate transporter xCT (SLC7A11). J. Biol. Chem., 2020, 295(20), 6936-6945.
[http://dx.doi.org/10.1074/jbc.RA119.012213] [PMID: 32265299]
[130]
Magtanong, L.; Ko, P.J.; Dixon, S.J. Emerging roles for lipids in non-apoptotic cell death. Cell Death Differ., 2016, 23(7), 1099-1109.
[http://dx.doi.org/10.1038/cdd.2016.25] [PMID: 26967968]
[131]
Dächert, J.; Schoeneberger, H.; Rohde, K.; Fulda, S. RSL3 and Erastin differentially regulate redox signaling to promote Smac mimetic-induced cell death. Oncotarget, 2016, 7(39), 63779-63792.
[http://dx.doi.org/10.18632/oncotarget.11687] [PMID: 27588473]
[132]
Sui, X.; Zhang, R.; Liu, S.; Duan, T.; Zhai, L.; Zhang, M.; Han, X.; Xiang, Y.; Huang, X.; Lin, H.; Xie, T. RSL3 drives ferroptosis through GPX4 inactivation and ROS production in colorectal cancer. Front. Pharmacol., 2018, 9, 1371.
[http://dx.doi.org/10.3389/fphar.2018.01371] [PMID: 30524291]
[133]
Leestma, J.E.; Walczak, T.; Hughes, J.R.; Kalelkar, M.B.; Teas, S.S. A prospective study on sudden unexpected death in epilepsy. Ann. Neurol., 1989, 26(2), 195-203.
[http://dx.doi.org/10.1002/ana.410260203] [PMID: 2774506]
[134]
Falconer, B.; Rajs, J. Post-mortem findings of cardiac lesions in epileptics: A preliminary report. Forensic Sci., 1976, 8(1), 63-71.
[http://dx.doi.org/10.1016/0300-9432(76)90048-0] [PMID: 824190]
[135]
Natelson, B.H.; Suarez, R.V.; Terrence, C.F.; Turizo, R. Patients with epilepsy who die suddenly have cardiac disease. Arch. Neurol., 1998, 55(6), 857-860.
[http://dx.doi.org/10.1001/archneur.55.6.857] [PMID: 9626779]
[136]
Fineschi, V.; Silver, M.D.; Karch, S.B.; Parolini, M.; Turillazzi, E.; Pomara, C.; Baroldi, G. Myocardial disarray: An architectural disorganization linked with adrenergic stress? Int. J. Cardiol., 2005, 99(2), 277-282.
[http://dx.doi.org/10.1016/j.ijcard.2004.01.022] [PMID: 15749187]
[137]
Zhuo, L.; Zhang, Y.; Zielke, H.R.; Levine, B.; Zhang, X.; Chang, L.; Fowler, D.; Li, L. Sudden unexpected death in epilepsy: Evaluation of forensic autopsy cases. Forensic Sci. Int., 2012, 223(1-3), 171-175.
[http://dx.doi.org/10.1016/j.forsciint.2012.08.024] [PMID: 22999232]
[138]
Goldberger, J.J.; Cain, M.E.; Hohnloser, S.H.; Kadish, A.H.; Knight, B.P.; Lauer, M.S.; Maron, B.J.; Page, R.L.; Passman, R.S.; Siscovick, D.; Stevenson, W.G.; Zipes, D.P. American Heart Association/american college of cardiology foundation/heart rhythm society scientific statement on noninvasive risk stratification techniques for identifying patients at risk for sudden cardiac death: a scientific statement from the american heart association council on clinical cardiology committee on electrocardiography and arrhythmias and council on epidemiology and prevention. Heart Rhythm, 2008, 5(10), e1-e21.
[http://dx.doi.org/10.1016/j.hrthm.2008.05.031] [PMID: 18929319]
[139]
Zack, M.; Luncheon, C. Adults with an epilepsy history, notably those 45–64 years old or at the lowest income levels, more often report heart disease than adults without an epilepsy history. Epilepsy Behav., 2018, 86, 208-210.
[http://dx.doi.org/10.1016/j.yebeh.2018.05.021] [PMID: 29908906]
[140]
Szabó, C.Á.; Akopian, M.; González, D.A.; Garza, M.A.; Carless, M.A. Cardiac biomarkers associated with epilepsy in a captive baboon pedigree. Epilepsia, 2019, 60(11), e110-e114.
[http://dx.doi.org/10.1111/epi.16359] [PMID: 31592545]
[141]
Tu, E.; Bagnall, R.D.; Duflou, J.; Semsarian, C. Post- mortem review and genetic analysis of sudden unexpected death in epilepsy (SUDEP) cases. Brain Pathol., 2011, 21(2), 201-208.
[http://dx.doi.org/10.1111/j.1750-3639.2010.00438.x] [PMID: 20875080]
[142]
Friedman, D.; Kannan, K.; Faustin, A.; Shroff, S.; Thomas, C.; Heguy, A.; Serrano, J.; Snuderl, M.; Devinsky, O. Cardiac arrhythmia and neuroexcitability gene variants in resected brain tissue from patients with sudden unexpected death in epilepsy (SUDEP). NPJ Genom. Med., 2018, 3(1), 9.
[http://dx.doi.org/10.1038/s41525-018-0048-5] [PMID: 29619247]
[143]
Bagnall, R.D.; Crompton, D.E.; Petrovski, S.; Lam, L.; Cutmore, C.; Garry, S.I.; Sadleir, L.G.; Dibbens, L.M.; Cairns, A.; Kivity, S.; Afawi, Z.; Regan, B.M.; Duflou, J.; Berkovic, S.F.; Scheffer, I.E.; Semsarian, C. Exome-based analysis of cardiac arrhythmia, respiratory control, and epilepsy genes in sudden unexpected death in epilepsy. Ann. Neurol., 2016, 79(4), 522-534.
[http://dx.doi.org/10.1002/ana.24596] [PMID: 26704558]
[144]
Tester, D.J.; Ackerman, M.J. Genetics of long QT syndrome. Methodist DeBakey Cardiovasc. J., 2014, 10(1), 29-33.
[http://dx.doi.org/10.14797/mdcj-10-1-29] [PMID: 24932360]
[145]
Auzmendi, J.; Akyuz, E.; Lazarowski, A. The role of p-glycoprotein (p-gp) and inwardly rectifying potassium (kir) channels in sudden unexpected death in Epilepsy (SUDEP). Epilepsy Behav., 2021, 121(Pt B), 106590.
[http://dx.doi.org/10.1016/j.yebeh.2019.106590]
[146]
Akyüz, E.; Üner, A.K.; Köklü, B.; Arulsamy, A.; Shaikh, M.F. Cardiorespiratory findings in epilepsy: A recent review on outcomes and pathophysiology. J. Neurosci. Res., 2021, 99(9), 2059-2073.
[http://dx.doi.org/10.1002/jnr.24861] [PMID: 34109651]
[147]
Merelli, A.; Ramos, A.J.; Lazarowski, A.; Auzmendi, J. Convulsive stress mimics brain hypoxia and promotes the P-glycoprotein (P-gp) and erythropoietin receptor overexpression. Front. Neurosci., 2019, 13, 750.
[http://dx.doi.org/10.3389/fnins.2019.00750] [PMID: 31379495]
[148]
Ersoy Dursun, F.; Açıksarı, G.; Özkök, S.; İncealtın, O. Evaluation of electrocardiography, echocardiography and cardiac T2* for cardiac complications in beta thalassemia major. Int. J. Cardiovasc. Imag., 2022, 38(3), 533-542.
[http://dx.doi.org/10.1007/s10554-021-02421-x] [PMID: 34623560]
[149]
Engle, M.A.; Erlandson, M.; Smith, C.H. Late cardiac complications of chronic, severe, refractory anemia with hemochromatosis. Circulation, 1964, 30(5), 698-705.
[http://dx.doi.org/10.1161/01.CIR.30.5.698] [PMID: 14226168]
[150]
Cecchetti, G.; Binda, A.; Piperno, A.; Nador, F.; Fargion, S.; Fiorelli, G. Cardiac alterations in 36 consecutive patients with idiopathic haemochromatosis: Polygraphic and echocardiographic evaluation. Eur. Heart J., 1991, 12(2), 224-230.
[http://dx.doi.org/10.1093/oxfordjournals.eurheartj.a059873] [PMID: 2044557]
[151]
Tadokoro, T.; Ikeda, M.; Ide, T.; Deguchi, H.; Ikeda, S.; Okabe, K.; Ishikita, A.; Matsushima, S.; Koumura, T.; Yamada, K.; Imai, H.; Tsutsui, H. Mitochondria-dependent ferroptosis plays a pivotal role in doxorubicin cardiotoxicity. JCI Insight, 2020, 5(9), e132747.
[http://dx.doi.org/10.1172/jci.insight.132747] [PMID: 32376803]
[152]
Fang, X.; Wang, H.; Han, D.; Xie, E.; Yang, X.; Wei, J.; Gu, S.; Gao, F.; Zhu, N.; Yin, X.; Cheng, Q.; Zhang, P.; Dai, W.; Chen, J.; Yang, F.; Yang, H.T.; Linkermann, A.; Gu, W.; Min, J.; Wang, F. Ferroptosis as a target for protection against cardiomyopathy. Proc. Natl. Acad. Sci. USA, 2019, 116(7), 2672-2680.
[http://dx.doi.org/10.1073/pnas.1821022116] [PMID: 30692261]
[153]
Conrad, M.; Proneth, B. Broken hearts: Iron overload, ferroptosis and cardiomyopathy. Cell Res., 2019, 29(4), 263-264.
[http://dx.doi.org/10.1038/s41422-019-0150-y] [PMID: 30809018]
[154]
Bai, T.; Li, M.; Liu, Y.; Qiao, Z.; Wang, Z. Inhibition of ferroptosis alleviates atherosclerosis through attenuating lipid peroxidation and endothelial dysfunction in mouse aortic endothelial cell. Free Radic. Biol. Med., 2020, 160, 92-102.
[http://dx.doi.org/10.1016/j.freeradbiomed.2020.07.026] [PMID: 32768568]
[155]
Selim, M.H.; Ratan, R.R. The role of iron neurotoxicity in ischemic stroke. Ageing Res. Rev., 2004, 3(3), 345-353.
[http://dx.doi.org/10.1016/j.arr.2004.04.001] [PMID: 15231241]
[156]
Ishimaru, H.; Ishikawa, K.; Ohe, Y.; Takahashi, A.; Tatemoto, K.; Maruyama, Y. Activation of iron handling system within the gerbil hippocampus after cerebral ischemia. Brain Res., 1996, 726(1-2), 23-30.
[157]
Pereira, A.; Brandao, P.; Auzmendi, J.; Lazarowski, A. Hemosiderin, a possible biomarker for sudep? Rev. Neurociencias, 2021, 29, 1-13.
[158]
Liu, X.J.; Lv, Y.F.; Cui, W.Z.; Li, Y.; Liu, Y.; Xue, Y.T.; Dong, F. Icariin inhibits hypoxia/reoxygenation-induced ferroptosis of cardiomyocytes via regulation of the Nrf2/HO-1 signaling pathway. FEBS Open Bio, 2021, 11(11), 2966-2976.
[http://dx.doi.org/10.1002/2211-5463.13276] [PMID: 34407320]
[159]
Pansani, A.P.; Ghazale, P.P.; dos Santos, E.G.; dos Santos Borges, K.; Gomes, K.P.; Lacerda, I.S.; Castro, C.H.; Mendes, E.P.; dos Santos, F.C.A.; Biancardi, M.F.; Nejm, M.B.; Dogini, D.B.; Rabelo, L.A.; Nunes-Souza, V.; Scorza, F.A.; Colugnati, D.B. The number and periodicity of seizures induce cardiac remodeling and changes in micro-RNA expression in rats submitted to electric amygdala kindling model of epilepsy. Epilepsy Behav., 2021, 116, 107784.
[http://dx.doi.org/10.1016/j.yebeh.2021.107784] [PMID: 33548915]
[160]
Castoldi, M.; Muckenthaler, M.U. Regulation of iron homeostasis by microRNAs. Cell. Mol. Life Sci., 2012, 69(23), 3945-3952.
[http://dx.doi.org/10.1007/s00018-012-1031-4] [PMID: 22678662]
[161]
Alsharafi, W.A.; Xiao, B.; Abuhamed, M.M.; Luo, Z. miRNAs: Biological and clinical determinants in epilepsy. Front. Mol. Neurosci., 2015, 8(OCT), 59.
[http://dx.doi.org/10.3389/fnmol.2015.00059] [PMID: 26528124]
[162]
Linkermann, A.; Skouta, R.; Himmerkus, N.; Mulay, S.R.; Dewitz, C.; De Zen, F.; Prokai, A.; Zuchtriegel, G.; Krombach, F.; Welz, P.S.; Weinlich, R.; Vanden Berghe, T.; Vandenabeele, P.; Pasparakis, M.; Bleich, M.; Weinberg, J.M.; Reichel, C.A.; Bräsen, J.H.; Kunzendorf, U.; Anders, H.J.; Stockwell, B.R.; Green, D.R.; Krautwald, S. Synchronized renal tubular cell death involves ferroptosis. Proc. Natl. Acad. Sci. USA, 2014, 111(47), 16836-16841.
[http://dx.doi.org/10.1073/pnas.1415518111] [PMID: 25385600]
[163]
Matsushita, M.; Freigang, S.; Schneider, C.; Conrad, M.; Bornkamm, G.W.; Kopf, M. T cell lipid peroxidation induces ferroptosis and prevents immunity to infection. J. Exp. Med., 2015, 212(4), 555-568.
[http://dx.doi.org/10.1084/jem.20140857] [PMID: 25824823]
[164]
Dixon, S.J.; Patel, D.N.; Welsch, M.; Skouta, R.; Lee, E.D.; Hayano, M.; Thomas, A.G.; Gleason, C.E.; Tatonetti, N.P.; Slusher, B.S.; Stockwell, B.R. Pharmacological inhibition of cystine–glutamate exchange induces endoplasmic reticulum stress and ferroptosis. eLife, 2014, 3(3), e02523.
[http://dx.doi.org/10.7554/eLife.02523] [PMID: 24844246]
[165]
Jiang, L.; Kon, N.; Li, T.; Wang, S.J.; Su, T.; Hibshoosh, H.; Baer, R.; Gu, W. Ferroptosis as a p53-mediated activity during tumour suppression. Nature, 2015, 520(7545), 57-62.
[http://dx.doi.org/10.1038/nature14344] [PMID: 25799988]
[166]
Prakash, C.; Mishra, M.; Kumar, P.; Kumar, V.; Sharma, D. Dehydroepiandrosterone alleviates oxidative stress and apoptosis in iron-induced epilepsy via activation of Nrf2/ARE signal pathway. Brain Res. Bull., 2019, 153, 181-190.
[http://dx.doi.org/10.1016/j.brainresbull.2019.08.019] [PMID: 31472186]
[167]
Kose, T.; Vera-Aviles, M.; Sharp, P.A.; Latunde-Dada, G.O. Curcumin and (−)- epigallocatechin-3-gallate protect murine min6 pancreatic beta-cells against iron toxicity and erastin-induced ferroptosis. Pharmaceuticals, 2019, 12(1), 26.
[http://dx.doi.org/10.3390/ph12010026] [PMID: 30736288]
[168]
Liu, K.; Chen, S.; Lu, R. Identification of important genes related to ferroptosis and hypoxia in acute myocardial infarction based on WGCNA. Bioengineered, 2021, 12(1), 7950-7963.
[http://dx.doi.org/10.1080/21655979.2021.1984004] [PMID: 34565282]

Rights & Permissions Print Cite
Article Metrics
32
3
© 2024 Bentham Science Publishers | Privacy Policy