Iron potentiates acetaminophen-induced oxidative stress and mitochondrial dysfunction in cultured mouse hepatocytes

Toxicological Sciences

Volumn 118, Issue 1, 2010, Pages 119-127

  Moon, Mi Sun ^a   Richie, John P ^a   Isom, Harriet C ^a,b  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b PENN STATE CANCER INSTITUTE   (United States)

Author keywords

Acetaminophen; Cell death; Hepatocyte; Iron; Mitochondrial injury; Reactive oxygen species

Indexed keywords

CD71 ANTIGEN; DEFEROXAMINE; FERRITIN; FERROCENE DERIVATIVE; HEMOSIDERIN; IRON; PARACETAMOL; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DEATH; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG POTENTIATION; GAP JUNCTION; LIVER CELL; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CELLS, CULTURED; DRUG SYNERGISM; FERROUS COMPOUNDS; HEPATOCYTES; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MITOCHONDRIA, LIVER; MITOCHONDRIAL MEMBRANES; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

HEPATITIS C VIRUS;

EID: 77958490216     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq230     Document Type: Article

References (32)

1. Bacon, B. R., Tavill, A. S., Brittenham, G. M., Park, C. H., and Recknagel, R. O. (1983). Hepatic lipid peroxidation in vivo in rats with chronic iron overload. J. Clin. Invest. 71, 429-439.
2. Bajt, M. L., Cover, C., Lemasters, J. J., and Jaeschke, H. (2006). Nuclear translocation of endonuclease G and apoptosis-inducing factor during acetaminophen-induced liver cell injury. Toxicol. Sci. 94, 217-225.
3. 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.
4. Britton, R. S., Bacon, B. R., and Recknagel, R. O. (1987). Lipid peroxidation and associated hepatic organelle dysfunction in iron overload. Chem. Phys. Lipids 45, 207-239.
5. Cable, E. E., Connor, J. R., and Isom, H. C. (1998). Accumulation of iron by primary rat hepatocytes in long-term culture: changes in nuclear shape mediated by non-transferrin-bound forms of iron. Am. J. Pathol. 152, 781-792.
6. Cable, E. E., and Isom, H. C. (1999). Metabolism of 3,5,5-trimethylhexanoylferrocene by rat liver: release of iron from 3,5,5-trimethylhexanoyl-ferrocene by a microsomal, phenobarbital-inducible cytochrome P-450. Drug Metab. Dispos. 27, 255-260.
7. Dullmann, J., Wulfhekel, U., Nielsen, P., and Heinrich, H. C. (1992). Iron overload of the liver by trimethylhexanoylferrocene in rats. Acta Anat. (Basel) 143, 96-108.
8. Eaton, J. W., and Qian, M. (2002). Molecular bases of cellular iron toxicity. Free Radic. Biol. Med. 32, 833-840.
9. El-Fouly, M. H., Trosko, J. E., and Chang, C. C. (1987). Scrape-loading and dye transfer. A rapid and simple technique to study gap junctional intercellular communication. Exp. Cell Res. 168, 422-430.
10. Feder, J. N., Penny, D. M., Irrinki, A., Lee, V. K., Lebron, J. A., Watson, N., Tsuchihashi, Z., Sigal, E., Bjorkman, P. J., and Schatzman, R. C. (1998). The hemochromatosis gene product complexes with the transferrin receptor and lowers its affinity for ligand binding. Proc. Natl. Acad. Sci. U.S.A. 95, 1472-1477.
11. Houglum, K., Filip, M., Witztum, J. L., and Chojkier, M. (1990). Malondialdehyde and 4-hydroxynonenal protein adducts in plasma and liver of rats with iron overload. J. Clin. Invest. 86, 1991-1998.
12. Isom, H. C., McDevitt, E. I., and Moon, M. S. (2009). Elevated hepatic iron: a confounding factor in chronic hepatitis C. Biochim. Biophys. Acta 1790, 650-662.
13. Ito, Y., Suzuki, Y., Ogonuki, H., Hiraishi, H., Razandi, M., Terano, A., Harada, T., and Ivey, K. J. (1994). Role of iron and glutathione redox cycle in acetaminophen-induced cytotoxicity to cultured rat hepatocytes. Dig. Dis. Sci. 39, 1257-1264.
14. Kadiiska, M. B., Burkitt, M. J., Xiang, Q. H., and Mason, R. P. (1995). Iron supplementation generates hydroxyl radical in vivo. An ESR spin-trapping investigation. J. Clin. Invest. 96, 1653-1657.
15. Kojima, T., Yamamoto, M., Tobioka, H., Mizuguchi, T., Mitaka, T., and Mochizuki, Y. (1996). Changes in cellular distribution of connexins 32 and 26 during formation of gap junctions in primary cultures of rat hepatocytes. Exp. Cell Res. 223, 314-326.
16. 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.
17. Kyle, M. E., Miccadei, S., Nakae, D., and Farber, J. L. (1987). Superoxide dismutase and catalase protect cultured hepatocytes from the cytotoxicity of acetaminophen. Biochem. Biophys. Res. Commun. 149, 889-896.
18. Larson, A. M., Polson, J., Fontana, R. J., Davern, T. J., Lalani, E., Hynan, L. S., Reisch, J. S., Schiodt, F. V., Ostapowicz, G., Shakil, A. O., et al. (2005). Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology 42, 1364-1372.
19. Loew, L. M., Carrington, W., Tuft, R. A., and Fay, F. S. (1994). Physiological cytosolic Ca2{thorn} transients evoke concurrent mitochondrial depolarizations. Proc. Natl. Acad. Sci. U.S.A. 91, 12579-12583.
20. Nelles, E., Butzler, C., Jung, D., Temme, A., Gabriel, H. D., Dahl, U., Traub, O., Stumpel, F., Jungermann, K., Zielasek, J., et al. (1996). Defective propagation of signals generated by sympathetic nerve stimulation in the liver of connexin32-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93, 9565-9570.
21. Nielsen, P., and Heinrich, H. C. (1993). Metabolism of iron from (3,5,5-trimethylhexanoyl)ferrocene in rats. A dietary model for severe iron overload. Biochem. Pharmacol. 45, 385-391.
22. Niemela, O., Parkkila, S., Britton, R. S., Brunt, E., Janney, C., and Bacon, B. (1999). Hepatic lipid peroxidation in hereditary hemochromatosis and alcoholic liver injury. J. Lab. Clin. Med. 133, 451-460.
23. 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, C1286-C1294.
24. Ostapowicz, G., Fontana, R. J., Schiodt, F. V., Larson, A., Davern, T. J., Han, S. H., McCashland, T. M., Shakil, A. O., Hay, J. E., Hynan, L., et al. (2002). Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann. Intern. Med. 137, 947-954.
25. 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.
26. Richie, J. P., Jr., Skowronski, L., Abraham, P., and Leutzinger, Y. (1996). Blood glutathione concentrations in a large-scale human study. Clin. Chem. 42, 64-70.
27. Ruch, R. J., and Klaunig, J. E. (1988). Kinetics of phenobarbital inhibition of intercellular communication in mouse hepatocytes. Cancer Res. 48, 2519-2523.
28. 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.
29. Squires, R. H., Jr., Shneider, B. L., Bucuvalas, J., Alonso, E., Sokol, R. J., Narkewicz, M. R., Dhawan, A., Rosenthal, P., Rodriguez-Baez, N., Murray, K. F., et al. (2006). Acute liver failure in children: the first 348 patients in the pediatric acute liver failure study group. J. Pediatr. 148, 652-658.
30. Stoehr, S. A., and Isom, H. C. (2003). Gap junction-mediated intercellular communication in a long-term primary mouse hepatocyte culture system. Hepatology 38, 1125-1135.
31. Temme, A., Buchmann, A., Gabriel, H. D., Nelles, E., Schwarz, M., and Willecke, K. (1997). High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr. Biol. 7, 713-716.
32. Young, I. S., Trouton, T. G., Torney, J. J., McMaster, D., Callender, M. E., and Trimble, E. R. (1994). Antioxidant status and lipid peroxidation in hereditary haemochromatosis. Free Radic. Biol. Med. 16, 393-397.