Lysosomal Iron mobilization and induction of the mitochondrial permeability transition in acetaminophen-induced toxicity to mouse hepatocytes

Toxicological Sciences

Volumn 117, Issue 1, 2010, Pages 101-108

  Kon, Kazuyoshi ^a,b   Kim, Jae Sung ^c   Uchiyama, Akira ^a,b   Jaeschke, Hartmut ^d   Lemasters, John J ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Acetaminophen; Cell death; Glutathione; Iron; Mitochondria

Indexed keywords

CALCEIN; DEFEROXAMINE MESYLATE; FERROUS ION; IRON CHELATE; PARACETAMOL; PROPIDIUM IODIDE; REACTIVE OXYGEN METABOLITE; RHODAMINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOLOGICAL MONITORING; CELL DAMAGE; CELL DEATH; CELL FREE SYSTEM; CELL ISOLATION; CELL KILLING; CELL PROTECTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG CYTOTOXICITY; FLUORESCENCE; FLUOROMETRY; IRON CHELATION; IRON KINETICS; LIVER CELL; LIVER TOXICITY; LYSOSOME; MALE; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; MOUSE; NONHUMAN; TARGET CELL DESTRUCTION; TOXICITY TESTING;

ACETAMINOPHEN; ANIMALS; FLUORESCEINS; FLUORESCENCE; HEPATOCYTES; IRON; IRON CHELATING AGENTS; LYSOSOMES; MALE; MICE; MICE, INBRED C3H; MICROSCOPY, CONFOCAL; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; REACTIVE OXYGEN SPECIES;

MUS;

EID: 77955899169     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq175     Document Type: Article

References (30)

1. Badr, M. Z., Belinsky, S. A., Kauffman, F. C., and Thurman, R. G. (1986). Mechanism of hepatotoxicity to periportal regions of the liver lobule due to allyl alcohol: role of oxygen and lipid peroxidation. J. Pharmacol. Exp. Ther. 238, 1138-1142.
2. Bajt, M. L., Knight, T. R., Lemasters, J. J., and Jaeschke, H. (2004). Acetaminophen-induced oxidant stress and cell injury in cultured mouse hepatocytes: protection by N-acetyl cysteine. Toxicol. Sci. 80, 343-349.
3. Breuer, W., Epsztejn, S., Millgram, P., and Cabantchik, I. Z. (1995). Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am. J. Physiol. 268(Pt 1), C1354-C1361.
4. Cohen, S. D., and Khairallah, E. A. (1997). Selective protein arylation and acetaminophen-induced hepatotoxicity. Drug Metab. Rev. 29, 59-77.
5. Fontana, R. J. (2008). Acute liver failure including acetaminophen overdose. Med. Clin. North Am. 92, 761-794. viii.
6. Gerson, R. J., Casini, A., Gilfor, D., Serroni, A., and Farber, J. L. (1985). Oxygen-mediated cell injury in the killing of cultured hepatocytes by acetaminophen. Biochem. Biophys. Res. Commun. 126, 1129-1137.
7. Gores, G. J., Nieminen, A. L., Wray, B. E., Herman, B., and Lemasters, J. J. (1989). Intracellular pH during "chemical hypoxia" in cultured rat hepatocytes. Protection by intracellular acidosis against the onset of cell death. J. Clin. Invest. 83, 386-396.
8. Hanawa, N., Shinohara, M., Saberi, B., Gaarde, W. A., Han, D., and Kaplowitz, N. (2008). Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J. Biol. Chem. 283, 13565-13577.
9. Jadot, M., Bielande, V., Beauloye, V., Wattiaux-De, C. S., and Wattiaux, R. (1990). Cytotoxicity and effect of glycyl-D-phenylalanine-2-naphthylamide on lysosomes. Biochim. Biophys. Acta 1027, 205-209.
10. Jaeschke, H., and Bajt, M. L. (2006). Intracellular signaling mechanisms of acetaminophen-induced liver cell death. Toxicol. Sci. 89, 31-41.
11. Jaeschke, H., Gores, G. J., Cederbaum, A. I., Hinson, J. A., Pessayre, D., and Lemasters, J. J. (2002). Mechanisms of hepatotoxicity. Toxicol. Sci. 65, 166-176.
12. Jaeschke, H., Knight, T. R., and Bajt, M. L. (2003). The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity. Toxicol. Lett. 144, 279-288.
13. Kon, K., Kim, J. S., Jaeschke, H., and Lemasters, J. J. (2004). Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 40, 1170-1179.
14. Kurz, T., Terman, A., and Brunk, U. T. (2007). Autophagy, ageing and apoptosis: the role of oxidative stress and lysosomal iron. Arch. Biochem. Biophys. 462, 220-230.
15. Liu, Z. D., and Hider, R. C. (2002). Design of clinically useful iron(III)-selective chelators. Med. Res. Rev. 22, 26-64.
16. Mitchell, J. R., Jollow, D. J., Potter, W. Z., Gillette, J. R., and Brodie, B. B. (1973). Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J. Pharmacol. Exp. Ther. 187, 211-217.
17. Nelson, S. D. (1990). Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Semin. Liver Dis. 10, 267-278.
18. Nieminen, A. L., Byrne, A. M., Herman, B., and Lemasters, J. J. (1997). Mitochondrial permeability transition in hepatocytes induced by t-BuOOH: NAD(P)H and reactive oxygen species. Am. J. Physiol. 272(Pt 1), C1286-C1294.
19. Nieminen, A. L., Gores, G. J., Bond, J. M., Imberti, R., Herman, B., and Lemasters, J. J. (1992). A novel cytotoxicity screening assay using a multiwell fluorescence scanner. Toxicol. Appl. Pharmacol. 115, 147-155.
20. Petrat, F., de Groot, H., Sustmann, R., and Rauen, U. (2002). The chelatable iron pool in living cells: a methodically defined quantity. Biol. Chem. 383, 489-502.
21. Qian, T., Nieminen, A. L., Herman, B., and Lemasters, J. J. (1997). Mitochondrial permeability transition in pH-dependent reperfusion injury to rat hepatocytes. Am. J. Physiol. 273(Pt 1), C1783-C1792.
22. Qiu, Y., Benet, L. Z., and Burlingame, A. L. (2001). Identification of hepatic protein targets of the reactive metabolites of the non-hepatotoxic regioisomer of acetaminophen, 3'-hydroxyacetanilide, in the mouse in vivo using twodimensional gel electrophoresis and mass spectrometry. Adv. Exp. Med. Biol. 500, 663-673.
23. Reid, A. B., Kurten, R. C., McCullough, S. S., Brock, R. W., and Hinson, J. A. (2005). Mechanisms of acetaminophen-induced hepatotoxicity: role of oxidative stress and mitochondrial permeability transition in freshly isolated mouse hepatocytes. J. Pharmacol. Exp. Ther. 312, 509-516.
24. Sakaida, I., Kayano, K., Wasaki, S., Nagatomi, A., Matsumura, Y., and Okita, K. (1995). Protection against acetaminophen-induced liver injury in vivo by an iron chelator, deferoxamine. Scand. J. Gastroenterol. 30, 61-67.
25. Schnellmann, J. G., Pumford, N. R., Kusewitt, D. F., Bucci, T. J., and Hinson, J. A. (1999). Deferoxamine delays the development of the hepatotoxicity of acetaminophen in mice. Toxicol. Lett. 106, 79-88.
26. Tirmenstein, M. A., and Nelson, S. D. (1989). Subcellular binding and effects on calcium homeostasis produced by acetaminophen and a nonhepatotoxic regioisomer, 3'-hydroxyacetanilide, in mouse liver. J. Biol. Chem. 264, 9814-9819.
27. Uchiyama, A., Kim, J. S., Kon, K., Jaeschke, H., Ikejima, K., Watanabe, S., and Lemasters, J. J. (2008). Translocation of iron from lysosomes into mitochondria is a key event during oxidative stress-induced hepatocellular injury. Hepatology 48, 1644-1654.
28. Werneburg, N. W., Guicciardi, M. E., Bronk, S. F., and Gores, G. J. (2002). Tumor necrosis factor-alpha-associated lysosomal permeabilization is cathepsin B dependent. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G947-G956.
29. Wildenthal, K., and Decker, R. S. (1980). The role of lysosomes in the heart. Adv. Myocardiol. 2, 349-358.
30. Zahrebelski, G., Nieminen, A. L., al Ghoul, K., Qian, T., Herman, B., and Lemasters, J. J. (1995). Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: a laser scanning confocal microscopic study. Hepatology 21, 1361-1372.