Iron loading exerts synergistic action via a different mechanistic pathway from that of acetaminophen-induced hepatic injury in mice

References

• Reuben A, Tillman H, Fontana RJ, et al. Outcomes in adults with acute liver failure between 1998 and 2013: an observational cohort study. Ann Intern Med. 2016;164(11):724.
   PubMed Web of Science ®Google Scholar
• Jayashree M, Singhi S. Changing trends and predictors of outcome in patients with acute poisoning admitted to the intensive care. J Trop Pediatr. 2011;57(5):340–346.
   PubMed Web of Science ®Google Scholar
• Watkins PB, Kaplowitz N, Slattery JT, et al. Aminotransferase elevations in healthy adults receiving 4 grams of acetaminophen daily: a randomized controlled trial. JAMA. 2006;296(1):87–93.
   PubMed Web of Science ®Google Scholar
• Mayoral W, Lewis JH, Zimmerman H. Drug-induced liver disease. Curr Opin Gastroenterol. 1999;15(3):208–216.
   PubMed Web of Science ®Google Scholar
• Davis DC, Potter WZ, Jollow DJ, et al. Species differences in hepatic glutathione depletion, covalent binding and hepatic necrosis after acetaminophen. Life Sci. 1974;14(11):2099–2109.
   PubMed Web of Science ®Google Scholar
• Dai G, He L, Chou N, et al. Acetaminophen metabolism does not contribute to gender difference in its hepatotoxicity in mouse. Toxicol Sci. 2006;92(1):33–41.
   PubMed Web of Science ®Google Scholar
• Lee SS, Buters JT, Pineau T, et al. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J Biol Chem. 1996;271(20):12063–12067.
   PubMed Web of Science ®Google Scholar
• Gregus Z, Madhu C, Klaassen CD. Species variation in toxication and detoxication of acetaminophen in vivo: a comparative study of biliary and urinary excretion of acetaminophen metabolites. J Pharmacol Exp Ther. 1988;244(1):91–99.
   PubMed Web of Science ®Google Scholar
• Hinson JA, Roberts DW, James LP. Mechanisms of acetaminophen-induced liver necrosis. Handb Exp Pharmacol. 2010;196:369–405.
   PubMedGoogle Scholar
• Masubuchi Y, Nakayama J, Watanabe Y. Sex difference in susceptibility to acetaminophen hepatotoxicity is reversed by buthionine sulfoximine. Toxicology. 2011;287(1-3):54–60.
   PubMed Web of Science ®Google Scholar
• McGill MR, Sharpe MR, Williams CD, et al. The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation. J Clin Invest. 2012;122(4):1574–1583.
   PubMed Web of Science ®Google Scholar
• Jaeschke H, Ramachandran A, Chao X, et al. Emerging and established modes of cell death during acetaminophen-induced liver injury. Arch Toxicol. 2019;93(12):3491–3502.
   PubMed Web of Science ®Google Scholar
• Kon K, Kim JS, Uchiyama A, et al. Lysosomal iron mobilization and induction of the mitochondrial permeability transition in acetaminophen-induced toxicity to mouse hepatocytes. Toxicol Sci. 2010;117(1):101–108.
   PubMed Web of Science ®Google Scholar
• Hu J, Kholmukhamedov A, Lindsey CC, et al. Translocation of iron from lysosomes to mitochondria during acetaminophen-induced hepatocellular injury: Protection by starch-desferal and minocycline. Free Radic Biol Med. 2016;97:418–426.
   PubMed Web of Science ®Google Scholar
• Hu J, Lemasters JJ. Suppression of iron mobilization from lysosomes to mitochondria attenuates liver injury after acetaminophen overdose in vivo in mice: protection by minocycline. Toxicol Appl Pharmacol. 2020;392:114930.
   PubMed Web of Science ®Google Scholar
• Sakaida I, Kayano K, Wasaki S, et al. Protection against acetaminophen-induced liver injury in vivo by an iron chelator, deferoxamine. Scand J Gastroenterol. 1995;30(1):61–67.
   PubMed Web of Science ®Google Scholar
• Schnellmann JG, Pumford NR, Kusewitt DF, et al. Deferoxamine delays the development of the hepatotoxicity of acetaminophen in mice. Toxicol Lett. 1999;106(1):79–88.
   PubMed Web of Science ®Google Scholar
• Gibson JD, Pumford NR, Samokyszyn VM, et al. Mechanism of acetaminophen-induced hepatotoxicity: covalent binding versus oxidative stress. Chem Res Toxicol. 1996;9(3):580–585.
   PubMed Web of Science ®Google Scholar
• Ackerman Z, Skarzinski G, Link G, et al. The effects of chronic iron overload in rats with acute acetaminophen overdose. Toxicol Pathol. 2018;46(5):597–607.
   PubMed Web of Science ®Google Scholar
• Dixon MF, Dixon B, Aparicio SR, et al. Experimental paracetamol-induced hepatic necrosis: a light- and electron-microscope, and histochemical study. J Pathol. 1975;116(1):17–29.
   PubMed Web of Science ®Google Scholar
• Lőrincz T, Jemnitz K, Kardon T, et al. Ferroptosis is involved in acetaminophen induced cell death. Pathol Oncol Res. 2015;21(4):1115–1121.
   PubMed Web of Science ®Google Scholar
• Yamada N, Karasawa T, Kimura H, et al. Ferroptosis driven by radical oxidation of n-6 polyunsaturated fatty acids mediates acetaminophen-induced acute liver failure. Cell Death Dis. 2020;11(2):144.
   PubMed Web of Science ®Google Scholar
• Tran T, Lee WM. DILI: New Insights into Diagnosis and Management. Curr Hepat Rep. 2013;12(1):53–58.
   PubMedGoogle Scholar
• Corcoran GB, Racz WJ, Smith CV, et al. Effects of N-acetylcysteine on acetaminophen covalent binding and hepatic necrosis in mice. J Pharmacol Exp Ther. 1985;232(3):864–872.
   PubMed Web of Science ®Google Scholar
• Corcoran GB, Wong BK. Role of glutathione in prevention of acetaminophen-induced hepatotoxicity by N-acetyl-L-cysteine in vivo: studies with N-acetyl-D-cysteine in mice. J Pharmacol Exp Ther. 1986;238(1):54–61.
   PubMed Web of Science ®Google Scholar
• Mitra A, Kulkarni AP, Ravikumar VC, et al. Effect of ascorbic acid esters on hepatic glutathione levels in mice treated with a hepatotoxic dose of acetaminophen. J Biochem Toxicol. 1991;6(2):93–100.
   PubMedGoogle Scholar
• Linster CL, Van Schaftingen E. Vitamin C. Biosynthesis, recycling and degradation in mammals. Febs J. 2007;274(1):1–22.
   PubMed Web of Science ®Google Scholar
• Gabbay KH, Bohren KM, Morello R, et al. Ascorbate synthesis pathway: dual role of ascorbate in bone homeostasis. J Biol Chem. 2010;285(25):19510–19520.
   PubMed Web of Science ®Google Scholar
• Takahashi M, Miyata S, Fujii J, et al. In vivo role of aldehyde reductase. Biochim Biophys Acta. 2012;1820(11):1787–1796.
   PubMed Web of Science ®Google Scholar
• Kurahashi T, Lee J, Nabeshima A, et al. Ascorbic acid prevents acetaminophen-induced hepatotoxicity in mice by ameliorating glutathione recovery and autophagy. Arch Biochem Biophys. 2016;604:36–46.
   PubMed Web of Science ®Google Scholar
• Traber MG, Stevens JF. Vitamins C and E: beneficial effects from a mechanistic perspective. Free Radic Biol Med. 2011;51(5):1000–1013.
   PubMed Web of Science ®Google Scholar
• Lane DJ, Richardson DR. The active role of vitamin C in mammalian iron metabolism: much more than just enhanced iron absorption! Free Radic Biol Med. 2014;75:69–83.
   PubMed Web of Science ®Google Scholar
• Kang ES, Lee J, Homma T, et al. xCT deficiency aggravates acetaminophen-induced hepatotoxicity under inhibition of the transsulfuration pathway. Free Radic Res. 2017;51(1):80–90.
   PubMed Web of Science ®Google Scholar
• Matsuoka Y, Yamato M, Yamasaki T, et al. Rapid and convenient detection of ascorbic acid using a fluorescent nitroxide switch. Free Radic Biol Med. 2012;53(11):2112–2118.
   PubMed Web of Science ®Google Scholar
• Riemer J, Hoepken HH, Czerwinska H, et al. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Anal Biochem. 2004;331(2):370–375.
   PubMed Web of Science ®Google Scholar
• Kobayashi S, Lee J, Takao T, et al. Increased ophthalmic acid production is supported by amino acid catabolism under fasting conditions in mice. Biochem Biophys Res Commun. 2017;491(3):649–655.
   PubMed Web of Science ®Google Scholar
• Kobayashi S, Tokairin Y, Miyakoshi T, et al. Quantitative analysis of γ-glutamylpeptides by liquid chromatography-mass spectrometry and application for γ-glutamyltransferase assays. Anal Biochem. 2019;578:13–22.
   PubMed Web of Science ®Google Scholar
• Takahashi M, Fujii J, Teshima T, et al. Identity of a major 3-deoxyglucosone-reducing enzyme with aldehyde reductase in rat liver established by amino acid sequencing and cDNA expression. Gene. 1993;127:249–253.
   PubMed Web of Science ®Google Scholar
• Toyokuni S, Ito F, Yamashita K, et al. Iron and thiol redox signaling in cancer: an exquisite balance to escape ferroptosis. Free Radic Biol Med. 2017;108:610–626.
   PubMed Web of Science ®Google Scholar
• Soga T, Baran R, Suematsu M, et al. Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. J Biol Chem. 2006;281(24):16768–16776.
   PubMed Web of Science ®Google Scholar
• Walker RM, Racz WJ, McElligott TF. Acetaminophen-induced hepatotoxic congestion in mice. Hepatology. 1985;5(2):233–240.
   PubMed Web of Science ®Google Scholar
• Moon MS, Kang BH, Krzeminski J, et al. 3,5,5-trimethyl-hexanoyl-ferrocene diet protects mice from moderate transient acetaminophen-induced hepatotoxicity. Toxicol Sci. 2011;124(2):348–358.
   PubMed Web of Science ®Google Scholar
• Tamai S, Iguchi T, Niino N, et al. A monkey model of acetaminophen-induced hepatotoxicity; phenotypic similarity to human. J Toxicol Sci. 2017;42(1):73–84.
   PubMed Web of Science ®Google Scholar
• Yamada N, Komada T, Ohno N, et al. Acetaminophen-induced hepatotoxicity: different mechanisms of acetaminophen-induced ferroptosis and mitochondrial damage. Arch Toxicol. 2020;94(6):2255–2257.
   PubMed Web of Science ®Google Scholar
• Du J, Cullen JJ, Buettner GR. Ascorbic acid: chemistry, biology and the treatment of cancer. Biochim Biophys Acta. 2012;1826(2):443–457.
   PubMed Web of Science ®Google Scholar
• Malhi H, Gores GJ, Lemasters JJ. Apoptosis and necrosis in the liver: a tale of two deaths? Hepatology. 2006;43(2 Suppl 1):S31–S44.
   PubMed Web of Science ®Google Scholar
• Du K, Ramachandran A, Jaeschke H. Oxidative stress during acetaminophen hepatotoxicity: Sources, pathophysiological role and therapeutic potential. Redox Biol. 2016;10:148–156.
   PubMed Web of Science ®Google Scholar
• Dixon SJ, Lemberg KM, Lamprecht MR, et al. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell. 2012;149(5):1060–1072.
   PubMed Web of Science ®Google Scholar
• Wang H, An P, Xie E, et al. Characterization of ferroptosis in murine models of hemochromatosis. Hepatology. 2017;66(2):449–465.
   PubMed Web of Science ®Google Scholar
• Tang HM, Tang HL. Cell recovery by reversal of ferroptosis. Biol Open. 2019;8(6):bio043182.
   PubMed Web of Science ®Google Scholar
• Peterson FJ, Lindemann NJ, Duquette PH, Holtzman JL. Potentiation of acute acetaminophen lethality by selenium and vitamin E deficiency in mice. J Nutr. 1992;122(1):74–81.
   PubMed Web of Science ®Google Scholar
• Amimoto T, Matsura T, Koyama SY, et al. Acetaminophen-induced hepatic injury in mice: the role of lipid peroxidation and effects of pretreatment with coenzyme Q10 and alpha-tocopherol. Free Radic Biol Med. 1995;19(2):169–176.
   PubMed Web of Science ®Google Scholar
• Bersuker K, Hendricks J, Li Z, et al. The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis. Nature. 2019;575(7784):688–692.
   PubMed Web of Science ®Google Scholar
• Doll S, Freitas FP, Shah R, et al. FSP1 is a glutathione-independent ferroptosis suppressor. Nature. 2019;575(7784):693–698.
   PubMed Web of Science ®Google Scholar
• Knight TR, Fariss MW, Farhood A, et al. Role of lipid peroxidation as a mechanism of liver injury after acetaminophen overdose in mice. Toxicol Sci. 2003;76(1):229–236.
   PubMed Web of Science ®Google Scholar