Vitamin E hydroquinone is an endogenous regulator of ferroptosis via redox control of 15-lipoxygenase

PLoS ONE

Volumn 13, Issue 8, 2018, Pages

  Hinman, Andrew ^a   Holst, Charles R ^a   Latham, Joey C ^a   Bruegger, Joel J ^a   Ulas, Gözde ^a   McCusker, Kevin P ^a   Amagata, Akiko ^a   Davis, Dana ^a   Hoff, Kevin G ^a   Kahn Kirby, Amanda H ^a   Kim, Virna ^a   Kosaka, Yuko ^a   Lee, Edgar ^a   Malone, Stephanie A ^a   Mei, Janet J ^a   Richards, Steve James ^a   Rivera, Veronica ^a   Miller, Guy ^a   Trimmer, Jeffrey K ^a   Shrader, William D ^a  

^a BioElectron Technology Corporation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA TOCOPHEROL DERIVATIVE; ALPHA TOCOPHEROL HYDROQUINONE; ARACHIDONATE 15 LIPOXYGENASE; FERRIC ION; FERROUS ION; UNCLASSIFIED DRUG; ALPHA TOCOPHEROL; ALPHA-TOCOPHEROL QUINOL; IRON; VITAMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FERROPTOSIS; LIPID OXIDATION; MALE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; RAT; VITAMIN METABOLISM; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; CELL LINE; CELL PROTECTION; DRUG EFFECT; LIPID PEROXIDATION; METABOLISM;

ALPHA-TOCOPHEROL; ANIMALS; APOPTOSIS; ARACHIDONATE 15-LIPOXYGENASE; CELL LINE; CYTOPROTECTION; IRON; LIPID PEROXIDATION; MICE; VITAMINS;

EID: 85053676186     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0201369     Document Type: Article

References (49)

1. Stockwell BR, Friedmann Angeli JP, Bayir H, Bush AI, Conrad M, Dixon SJ, et al. Ferroptosis: A Regulated Cell Death Nexus Linking Metabolism, Redox Biology, and Disease. Cell. 2017; 171: 273-285. https://doi.org/10.1016/j.cell.2017.09.021 PMID: 28985560
2. Wenzel SE, Tyurina YY, Zhao J, St Croix CM, Dar HH, Mao G, et al. PEBP1 Wardens Ferroptosis by Enabling Lipoxygenase Generation of Lipid Death Signals. Cell. 2017; 171: 628-641.e26. https://doi.org/10.1016/j.cell.2017.09.044 PMID: 29053969
3. Drefs M, Thomas MN, Guba M, Angele MK, Werner J, Conrad M, et al. Modulation of Glutathione Hemostasis by Inhibition of 12/15-Lipoxygenase Prevents ROS-Mediated Cell Death after Hepatic Ischemia and Reperfusion. Oxid Med Cell Longev. 2017; 2017: 8325754. https://doi.org/10.1155/2017/8325754 PMID: 28811867
4. Do Van B, Gouel F, Jonneaux A, Timmerman K, Gelé P, Pétrault M, et al. Ferroptosis, a newly characterized form of cell death in Parkinson's disease that is regulated by PKC. Neurobiol Dis. Elsevier Inc.; 2016; 94: 169-178. https://doi.org/10.1016/j.nbd.2016.05.011 PMID: 27189756
5. Do Van B, Gouel F, Jonneaux A, Timmerman K, Gelé P, Pétrault M, et al. Ferroptosis, a newly characterized form of cell death in Parkinson's disease that is regulated by PKC. Neurobiol Dis. Elsevier B.V.; 2016; 94: 169-78. https://doi.org/10.1016/j.nbd.2016.05.011 PMID: 27189756
6. Kagan VE, Mao G, Qu F, Angeli JPF, Doll S, Croix CS, et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol. 2016; 13: 81-90. https://doi.org/10.1038/nchembio.2238 PMID: 27842066
7. Angeli JPF, Shah R, Pratt DA, Conrad M. Ferroptosis Inhibition: Mechanisms and Opportunities. Trends Pharmacol Sci. Elsevier Ltd; 2017; 38: 489-498. https://doi.org/10.1016/j.tips.2017.02.005 PMID: 28363764
8. Shah R, Shchepinov MS, Pratt DA. Resolving the Role of Lipoxygenases in the Initiation and Execution of Ferroptosis. ACS Cent Sci. 2018; acscentsci.7b00589. https://doi.org/10.1021/acscentsci.7b00589 PMID: 29632885
9. Yang WS, Stockwell BR. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem Biol. 2008; 15: 234-45. https://doi.org/10.1016/j.chembiol.2008.02.010 PMID: 18355723
10. Shrader WD, Amagata A, Barnes A, Hinman A, Jankowski O, Lee E, et al. Towards a modern definition of vitamin E-evidence for a quinone hypothesis. Bioorg Med Chem Lett. Elsevier Ltd; 2012; 22: 391-5. https://doi.org/10.1016/j.bmcl.2011.10.117 PMID: 22137789
11. Shrader WD, Amagata A, Barnes A, Enns GM, Hinman A, Jankowski O, et al. α-Tocotrienol quinone modulates oxidative stress response and the biochemistry of aging. Bioorg Med Chem Lett. Elsevier Ltd; 2011; 21: 3693-8. https://doi.org/10.1016/j.bmcl.2011.04.085 PMID: 21600768
12. Enns GMGM, Kinsman SLSL, Perlman SLSL, Spicer KMKM, Abdenur JEJE, Cohen BHBH, et al. Initial experience in the treatment of inherited mitochondrial disease with EPI-743. Mol Genet Metab. Elsevier Inc.; 2012; 105: 91-102. https://doi.org/10.1016/j.ymgme.2011.10.009 PMID: 22115768
13. Lynch DR, Willi SM, Wilson RB, Cotticelli MGG, Brigatti KW, Deutsch EC, et al. A0001 in Friedreich ataxia: biochemical characterization and effects in a clinical trial. Mov Disord. 2012; 27: 1026-33. https://doi.org/10.1002/mds.25058 PMID: 22744651
14. Martinelli D, Catteruccia M, Piemonte F, Pastore A, Tozzi G, Dionisi-Vici C, et al. EPI-743 reverses the progression of the pediatric mitochondrial disease-genetically defined Leigh Syndrome. Mol Genet Metab. Elsevier Inc.; 2012; 107: 383-8. https://doi.org/10.1016/j.ymgme.2012.09.007 PMID: 23010433
15. Khanna S, Roy S, Ryu H, Bahadduri P, Swaan PW, Ratan RR, et al. Molecular Basis of Vitamin E Action: Tocotrienol modulates 12-lipoxygenase, a key mediator of glutamate-induced neurodegeneration. J Biol Chem. 2003; 278: 43508-43515. https://doi.org/10.1074/jbc.M307075200 PMID: 12917400
16. Seiler A, Schneider M, Förster H, Roth S, Wirth EK, Culmsee C, et al. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 2008; 8: 237-48. https://doi.org/10.1016/j.cmet.2008.07.005 PMID: 18762024
17. Chen L, Hambright WS, Na R, Ran Q. Ablation of the Ferroptosis Inhibitor Glutathione Peroxidase 4 in Neurons Results in Rapid Motor Neuron Degeneration and Paralysis. J Biol Chem. 2015; 290: 28097-106. https://doi.org/10.1074/jbc.M115.680090 PMID: 26400084
18. Carlson BA, Tobe R, Yefremova E, Tsuji PA, Hoffmann VJ, Schweizer U, et al. Glutathione peroxidase 4 and vitamin E cooperatively prevent hepatocellular degeneration. Redox Biol. 2016; 9: 22-31. https://doi.org/10.1016/j.redox.2016.05.003 PMID: 27262435
19. Matsushita M, Freigang S, Schneider C, Conrad M, Bornkamm GW, Kopf M. T cell lipid peroxidation induces ferroptosis and prevents immunity to infection. J Exp Med. 2015; 212: 555-568. https://doi.org/10.1084/jem.20140857 PMID: 25824823
20. Ruan Q, Lesort M, MacDonald ME, Johnson GVW. Striatal cells from mutant huntingtin knock-in mice are selectively vulnerable to mitochondrial complex II inhibitor-induced cell death through a non-apoptotic pathway. Hum Mol Genet. 2004; 13: 669-81. https://doi.org/10.1093/hmg/ddh082 PMID: 14962977
21. Wu JH, Croft KD. Vitamin E metabolism. Mol Aspects Med. 2007; 28: 437-52. https://doi.org/10.1016/j. mam.2006.12.007 PMID: 17306359
22. Schmölz L, Birringer M, Lorkowski S, Wallert M. Complexity of vitamin E metabolism. World J Biol Chem. 2016; 7: 14-43. https://doi.org/10.4331/wjbc.v7.i1.14 PMID: 26981194
23. Galli F, Polidori MC, Stahl W, Mecocci P, Kelly FJ. Vitamin E biotransformation in humans. Vitam Horm. 2007; 76: 263-80. https://doi.org/10.1016/S0083-6729(07)76009-0 PMID: 17628177
24. Angeli JPF, Proneth B, Hammond VJ, Tyurina YY, Tyurin VA, O'Donnell VB, et al. Inactivation of the Ferroptosis Regulator Gpx4 Triggers Acute Renal Failure in a Therapeutically Relevant Mechanism. Free Radic Biol Med. Elsevier; 2014; 76: S77-S78. https://doi.org/10.1016/j.freeradbiomed.2014.10.276
25. Shimada K, Skouta R, Kaplan A, Yang WS, Hayano M, Dixon SJ, et al. Global survey of cell death mechanisms reveals metabolic regulation of ferroptosis. Nat Chem Biol. Nature Publishing Group; 2016; 1-10. https://doi.org/10.1038/nchembio.2079 PMID: 27159577
26. Yang WS, Kim KJ, Gaschler MM, Patel M, Shchepinov MS, Stockwell BR. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc Natl Acad Sci U S A. 2016; 113: E4966-75. https://doi.org/10.1073/pnas.1603244113 PMID: 27506793
27. Hughes PE, Tove SB. Synthesis of alpha-tocopherolquinone by the rat and its reduction by mitochondria. J Biol Chem. 1980; 255: 7095-7. Available: http://www.ncbi.nlm.nih.gov/pubmed/7391070 PMID: 7391070
28. Kaneko K, Kiyose C, Ueda T, Ichikawa H, Igarashi O. Studies of the metabolism of alpha-tocopherol stereoisomers in rats using [5-methyl-(14)C]SRR- and RRR-alpha-tocopherol. J Lipid Res. 2000; 41: 357-67. Available: http://www.ncbi.nlm.nih.gov/pubmed/10706583 PMID: 10706583
29. Csallany AS, Draper HH, Shah SN. Conversion of d-α-tocopherol-C14 to tocopheryl-p-quinone in vivo. Arch Biochem Biophys. 1962; 98: 142-145. https://doi.org/10.1016/0003-9861(62)90159-5 PMID: 13882501
30. Plack PA, Bieri JG. Metabolic products of α-tocopherol in the livers of rats given intraperitoneal injections of [14C]-α-tocopherol. Biochim Biophys Acta-Spec Sect Lipids Relat Subj. 1964; 84: 729-738. https://doi.org/10.1016/0926-6542(64)90031-9
31. Jain SK, Levine SN. Elevated lipid peroxidation and vitamin e-quinone levels in heart ventricles of streptozotocin-treated diabetic rats. Free Radic Biol Med. 1995; 18: 337-341. https://doi.org/10.1016/0891-5849(94)00114-Y PMID: 7744318
32. Kiyose C, Kaneko K, Muramatsu R, Ueda T, Igarashi O. Simultaneous determination of RRR- and SRR-alpha-tocopherols and their quinones in rat plasma and tissues by using chiral high-performance liquid chromatography. Lipids. 1999; 34: 415-22. Available: http://www.ncbi.nlm.nih.gov/pubmed/10443975 PMID: 10443975
33. Upston JM, Witting PK, Brown AJ, Stocker R, Keaney JF. Effect of vitamin E on aortic lipid oxidation and intimal proliferation after arterial injury in cholesterol-fed rabbits. Free Radic Biol Med. 2001; 31: 1245-53. https://doi.org/10.1016/S0891-5849(01)00721-3 PMID: 11705703
34. Terentis AC, Thomas SR, Burr JA, Liebler DC, Stocker R. Vitamin E oxidation in human atherosclerotic lesions. Circ Res. 2002; 90: 333-9. https://doi.org/10.1161/hh0302.104454 PMID: 11861423
35. Mottier P, Gremaud E, Guy P a, Turesky RJ. Comparison of gas chromatography-mass spectrometry and liquid chromatography-tandem mass spectrometry methods to quantify alpha-tocopherol and alpha-tocopherolquinone levels in human plasma. Anal Biochem. 2002; 301: 128-35. https://doi.org/10.1006/abio.2001.5486 PMID: 11811977
36. Shichiri M, Yoshida Y, Ishida N, Hagihara Y, Iwahashi H, Tamai H, et al. α-Tocopherol suppresses lipid peroxidation and behavioral and cognitive impairments in the Ts65Dn mouse model of Down syndrome. Free Radic Biol Med. Elsevier Inc.; 2011; 50: 1801-11. https://doi.org/10.1016/j.freeradbiomed.2011. 03.023 PMID: 21447382
37. Hinman AW. Methods of analyzing p-hydroquinone levels and ratios. WIPO-World Intellectual Property Organization;WO2018/081644 A1, 2018. p. 90.
38. Siegel D, Bolton EM, Burr JA, Liebler DC, Ross D. The reduction of alpha-tocopherolquinone by human NAD(P)H: quinone oxidoreductase: the role of alpha-tocopherolhydroquinone as a cellular antioxidant. Mol Pharmacol. 1997; 52: 300-5. Available: http://www.ncbi.nlm.nih.gov/pubmed/9271353 PMID: 9271353
39. Hayashi T, Kanetoshi A, Nakamura M, Tamura M, Shirahama H. Reduction of alpha-tocopherolquinone to alpha-tocopherolhydroquinone in rat hepatocytes. Biochem Pharmacol. 1992; 44: 489-93. Available: http://www.ncbi.nlm.nih.gov/pubmed/1510699 PMID: 1510699
40. Traber MG, Atkinson J. Vitamin E, antioxidant and nothing more. Free Radic Biol Med. 2007; 43: 4-15. https://doi.org/10.1016/j.freeradbiomed.2007.03.024 PMID: 17561088
41. Cao G, Alessio HM, Cutler RG. Oxygen-radical absorbance capacity assay for antioxidants. Free Radic Biol Med. 1993; 14: 303-11. https://doi.org/10.1016/0891-5849(93)90027-R PMID: 8458588
42. Shah R, Margison K, Pratt DA. The Potency of Diarylamine Radical-Trapping Antioxidants as Inhibitors of Ferroptosis Underscores the Role of Autoxidation in the Mechanism of Cell Death. ACS Chem Biol. 2017; 12: 2538-2545. https://doi.org/10.1021/acschembio.7b00730 PMID: 28837769
43. Doll S, Proneth B, Tyurina YY, Panzilius E, Kobayashi S, Ingold I, et al. ACSL4 dictates ferroptosis sensitivity by shaping cellular lipid composition. Nat Chem Biol. 2016; 13: 91-98. https://doi.org/10.1038/nchembio.2239 PMID: 27842070
44. Kemal C, Louis-Flamberg P, Krupinski-Olsen R, Shorter AL. Reductive Inactivation of Soybean Lipoxygenase 1 by Catechols: A Possible Mechanism for Regulation of Lipoxygenase Activity. Biochemistry. 1987; 26: 7064-7072. https://doi.org/10.1021/bi00396a031 PMID: 3122826
45. Nelson MJ, Batt DG, Thompson JS, Wright SW. Reduction of the active-site iron by potent inhibitors of lipoxygenases. J Biol Chem. 1991; 266: 8225-9. Available: http://www.ncbi.nlm.nih.gov/pubmed/1850741 PMID: 1850741
46. Evans HM, Emerson OH, Emerson GA, Smith LI, Ungnade HE, Prichard WW, et al. The chemistry of Vitamin E. XII. Specificity and relationship between chemical structure and Vitamin E activity. J Org Chem. 1939; 04: 376-388. https://doi.org/10.1021/jo01216a003
47. Emmerson OH, Emmerson GA, Evans HM. The vitamin E activity of alpha-tocoquinone. J Biol Chem. 1939; 131: 409-412.
48. Lebold KM, Traber MG. Interactions between α-tocopherol, polyunsaturated fatty acids, and lipoxygenases during embryogenesis. Free Radic Biol Med. Elsevier; 2014; 66: 13-9. https://doi.org/10.1016/j.freeradbiomed.2013.07.039 PMID: 23920314
49. Yant LJ, Ran Q, Rao L, Van Remmen H, Shibatani T, Belter JG, et al. The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med. 2003; 34: 496-502. https://doi.org/10.1016/S0891-5849(02)01360-6 PMID: 12566075