Intracellular signaling mechanisms of acetaminophen-induced liver cell death

Toxicological Sciences

Volumn 89, Issue 1, 2006, Pages 31-41

  Jaeschke, Hartmut ^a,b   Bajt, Mary Lynn ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Acetaminophen hepatotoxicity; Apoptosis; Covalent binding; DNA fragmentation; Endonucleases; Oncotic necrosis; Oxidant stress; Peroxynitrite; Reactive metabolites

Indexed keywords

ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; CALCIUM ION; CALPAIN; DNA FRAGMENT; ENDONUCLEASE; GLUTATHIONE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; PARACETAMOL; PEROXYNITRITE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; PROTEINASE;

ALKYLATION; APOPTOSIS; CALCIUM HOMEOSTASIS; CELL DEATH; CELL MEMBRANE POTENTIAL; CELL REGENERATION; CHROMATIN CONDENSATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DEGRADATION; DRUG OVERDOSE; GENOMICS; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL DAMAGE; LIVER FAILURE; LIVER TOXICITY; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; APOPTOSIS; CELL DEATH; DNA FRAGMENTATION; HEPATOCYTES; LIVER; NECROSIS; PEROXYNITROUS ACID; SIGNAL TRANSDUCTION;

EID: 29544448331     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfi336     Document Type: Review

References (119)

1. Adams, M. L., Pierce, R. H., Vail, M. E., White, C. C., Tonge, R. P., Kavanagh, T. J., Fausto, N., Nelson, S. D., and Bruschi, S. A. (2001). Enhanced acetaminophen hepatotoxicity in transgenic mice overexpressing BCL-2. Mol. Pharmacol. 60, 907-915.
2. Adamson, G. M., and Harman, A. W. (1993). Oxidative stress in cultured hepatocytes exposed to acetaminophen. Biochem. Pharmacol. 45, 2289-2294.
3. Akerman, P., Cote, P., Yang, S. Q., McClain, C., Nelson, S., Bagby, G. J., and Diehl, A. M. (1992). Antibodies to tumor necrosis factor-alpha inhibit liver regeneration after partial hepatectomy. Am. J. Physiol. 263, G579-G585.
4. Bajt, M. L., Lawson, J. A., Vonderfecht, S. L., Gujral, J. S., and Jaeschke, H. (2000). Protection against Fas receptor-mediated apoptosis in hepatocytes and nonparenchymal cells by a caspase-8 inhibitor in vivo: Evidence for a postmitochondrial processing of caspase-8. Toxicol. Sci. 58, 109-117.
5. Bajt, M. L., Knight, T. R., Farhood, A., and Jaeschke, H. (2003). Scavenging peroxynitrite with glutathione promotes regeneration and enhances survival during acetaminophen-induced liver injury in mice. J. Pharmacol. Exp. Ther. 307, 67-73.
6. 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.
7. Bajt, M. L., Lemasters, J. J., and Jaeschke, H. (2005). Role of mitochondrial Bax translocation in acetaminophen-induced hepatic necrosis (abstract). Toxicol. Sci. 84(Suppl. 1), 215.
8. Birge, R. B., Bartolone, J. B., Nishanian, E. V., Bruno, M. K., Mangold, J. B., Cohen, S. D., and Khairallah, E. A. (1988). Dissociation of covalent binding from the oxidative effects of acetaminophen. Studies using dimethylated acetaminophen derivatives. Biochem. Pharmacol. 37, 3383-3393.
9. Boulares, A. H., Zoltoski, A. J., Stoica, B. A., Cuvillier, O., and Smulson, M. E. (2002). Acetaminophen induces a caspase-dependent and Bcl-XL sensitive apoptosis in human hepatoma cells and lymphocytes. Pharmacol. Toxicol. 90, 38-50.
10. Bourdi, M., Masubuchi, Y., Reilly, T. P., Amouzadeh, H. R., Martin, J. L., George, J. W., Shah, A. G., and Pohl, L. R. (2002). Protection against acetaminophen-induced liver injury and lethality by interleukin 10: Role of inducible nitric oxide synthase. Hepatology 35, 289-298.
11. Burcham, P. C., and Harman, A. W. (1991). Acetaminophen toxicity results in site-specific mitochondrial damage in isolated mouse hepatocytes. J. Biol. Chem. 266, 5049-5054.
12. Chanda, S., Mangipudy, R. S., Warbritton, A., Bucci, T. J., and Mehendale, H. M. (1995). Stimulated hepatic tissue repair underlies heteroprotection by thioacetamide against acetaminophen-induced lethality. Hepatology 21, 477-486.
13. Chao, D. T., and Korsmeyer, S. J. (1998). BCL-2 family: Regulators of cell death. Annu. Rev. Immunol. 16, 395-419.
14. Chen, C., Hennig, G. E., and Manautou, J. E. (2003). Hepatobiliary excretion of acetaminophen glutathione conjugate and its derivatives in transport-deficient (TR-) hyperbilirubinemic rats. Drug Metab. Dispos. 31, 798-804.
15. Cohen, S. D., Pumford, N. R., Khairallah, E. A., Boekelheide, K., Pohl, L. R., Amouzadeh, H. R., and Hinson, J. A. (1997). Selective protein covalent binding and target organ toxicity. Toxicol. Appl. Pharmacol. 143, 1-12.
16. Chiu, H., Gardner, C. R., Dambach, D. M., Durham, S. K., Brittingham, J. A., Laskin, J. D., and Laskin, D. L. (2003). Role of tumor necrosis factor receptor 1 (p55) in hepatocyte proliferation during acetaminophen-induced toxicity in mice. Toxicol. Appl. Pharmacol. 193, 218-227.
17. Corcoran, G. B., Bauer, J. A., and Lau, T. W. (1988). Immediate rise in intracellular calcium and glycogen phosphorylase a activities upon acetaminophen covalent binding leading to hepatotoxicity in mice. Toxicology 50, 157-167.
18. Corcoran, G. B., Racz, W. J., Smith, C. V., and Mitchell, J. R. (1985). Effects of N-acetylcysteine on acetaminophen covalent binding and hepatic necrosis in mice. J. Pharmacol. Exp. Ther. 232, 864-872.
19. Cover, C., Fickert, P., Knight, T. R., Fuchsbichler, A., Farhood, A., Trauner, M., and Jaeschke, H. (2005a). Pathophysiological role of poly(ADP-ribose) polymerase (PARP) activation during acetaminophen-induced liver cell necrosis in mice. Toxicol. Sci. 84, 201-208.
20. Cover, C., Mansouri, A., Knight, T. R., Bajt, M. L., Lemasters, J. J., Pessayre, D., and Jaeschke, H. (2005b). Peroxynitrite-induced mitochondrial and endonuclease-mediated nuclear DNA damage in acetaminophen hepatotoxicity. J. Pharmacol. Exp. Ther. 315, doi:10.1124/ jpet.105.088898.
21. Cressman, D. E., Greenbaum, L. E., DeAngelis, R. A., Ciliberto, G., Furth, E. E., Poli, V., and Taub, R. (1996). Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274, 1379-1383.
22. Denicola, A., and Radi, R. (2005). Peroxynitrite and drug-dependent toxicity. Toxicology 208, 273-288.
23. Donnelly, P. J., Walker, R. M., and Racz, W. J. (1994). Inhibition of mitochondrial respiration in vivo is an early event in acetaminophen-induced hepatotoxicity. Arch. Toxicol. 68, 110-118.
24. El-Hassan, H., Anwar, K., Macanas-Pirard, P., Crabtree, M., Chow, S. C., Johnson, V. L., Lee, P. C., Hinton, R. H., Price, S. C., and Kass, G. E. (2003). Involvement of mitochondria in acetaminophen-induced apoptosis and hepatic injury: Roles of cytochrome c, Bax, Bid, and caspases. Toxicol. Appl. Pharmacol. 191, 118-129.
25. Fausto, N. (2000). Liver regeneration. J. Hepatol. 32(1 Suppl.), 19-31.
26. Ferret, P. J., Hammoud, R., Tulliez, M., Tran, A., Trebeden, H., Jaffray, P., Malassagne, B., Calmus, Y., Weill, B., and Batteux, F. (2001). Detoxification of reactive oxygen species by a nonpeptidyl mimic of superoxide dismutase cures acetaminophen-induced acute liver failure in the mouse. Hepatology 33, 1173-1180.
27. Francavilla, A., Azzarone, A., Carrieri, G., Cillo, U., Van Thiel, D., Subbottin, V., and Starzl, T. E. (1993). Administration of hepatic stimulatory substance alone or with other liver growth factors does not ameliorate acetaminophen-induced liver failure. Hepatology 17, 429-433.
28. Fu, Y., Cheng, W. H., Porres, J. M., Ross, D. A., and Lei, X. G. (1999). Knockout of cellular glutathione peroxidase gene renders mice susceptible to diquat-induced oxidative stress. Free Radic. Biol. Med. 27, 605-611.
29. Gardner, C. R., Heck, D. E., Yang, C. S., Thomas, P. E., Zhang, X. J., DeGeorge, G. L., Laskin, J. D., and Laskin, D. L. (1998). Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology 27, 748-754.
30. Gardner, C. R., Laskin, J. D., Dambach, D. M., Sacco, M., Durham, S. K., Bruno, M. K., Cohen, S. D., Gordon, M. K., Gerecke, D. R., Zhou, P., et al. (2002). Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: Potential role of tumor necrosis factor-alpha and interleukin-10. Toxicol. Appl. Pharmacol. 184, 27-36.
31. Gonzalez, F. J. (2005). Role of cytochromes P450 in chemical toxicity and oxidative stress: Studies with CYP2E1. Mutat. Res. 569, 101-110.
32. Gujral, J. S., Hinson, J. A., Farhood, A., and Jaeschke, H. (2004). NADPH oxidase-derived oxidant stress is critical for neutrophil cytotoxicity during endotoxemia. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G243-G252.
33. Gujral, J. S., Knight, T. R., Farhood, A., Bajt, M. L., and Jaeschke, H. (2002). Mode of cell death after acetaminophen overdose in mice: Apoptosis or oncotic necrosis? Toxicol. Sci. 67, 322-328.
34. Gupta, S., Rogers, L. K., Taylor, S. K., and Smith, C. V. (1997). Inhibition of carbamyl phosphate synthetase-I and glutamine synthetase by hepatotoxic doses of acetaminophen in mice. Toxicol. Appl. Pharmacol. 146, 317-327.
35. Ha, H. C., and Snyder, S. H (1999). Poly(ADP-ribose) polymerase is a mediator of necrotic cell death by ATP depletion. Proc. Natl. Acad. Sci. U.S.A. 96, 13978-13982.
36. Halliwell, B. (2003). Oxidative stress in cell culture: An under-appreciated problem? FEBS Lett. 540, 3-6.
37. Halmes, N. C., Hinson, J. A., Martin, B. M., and Pumford, N. R. (1996). Glutamate dehydrogenase covalently binds to a reactive metabolite of acetaminophen. Chem. Res. Toxicol. 9, 541-546.
38. He, L., and Lemasters, J. J. (2002). Regulated and unregulated mitochondrial permeability transition pores: A new paradigm of pore structure and function? FEBS Lett. 512, 1-7.
39. Hill, M. M., Adrain, C., and Martin, S. J. (2003). Portrait of a killer: The mitochondrial apoptosome emerges from the shadows. Mol. Interv. 3, 19-26.
40. Hinson, J. A., Bucci, T. J., Irwin, L. K., Michael, S. L., and Mayeux, P. R. (2002). Effect of inhibitors of nitric oxide synthase on acetaminophen-induced hepatotoxicity in mice. Nitric Oxide 6, 160-167.
41. Hinson, J. A., Pike, S. L., Pumford, N. R., and Mayeux, P. R. (1998). Nitrotyrosine-protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice. Chem. Res. Toxicol. 11, 604-607.
42. Haouzi, D., Cohen, I., Vieira, H. L., Poncet, D., Boya, P., Castedo, M., Vadrot, N., Belzacq, A. S., Fau, D., Brenner, C., et al. (2002). Mitochondrial permeability transition as a novel principle of hepatorenal toxicity in vivo. Apoptosis 7, 395-405.
43. Jaeschke, H. (1990). Glutathione disuffide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: The protective effect of allopurinol. J. Pharmacol. Exp. Ther. 255, 935-941.
44. Jaeschke, H. (2005). Role of inflammation in the mechanism of acetaminophen hepatotoxicity. Exp. Opin. Drug Metab. Toxicol. 1, 389-397.
45. Jaeschke, H., Cover, C., and Bajt, M. L. (2005). Role of caspases in acetaminophen-induced liver injury. Life Sci. (In press).
46. Jaeschke, H., Farhood, A., Cai, S. X., Tseng, B. Y., and Bajt, M. L. (2000). Protection against TNF-induced liver parenchymal cell apoptosis during endotoxemia by a novel caspase inhibitor in mice. Toxicol. Appl. Pharmacol. 169, 77-83.
47. Jaeschke, H., Fisher, M. A., Lawson, J. A., Simmons, C. A., Farhood, A., and Jones, D. A. (1998). Activation of caspase 3 (CPP32)-like proteases is essential for TNF-alpha-induced hepatic parenchymal cell apoptosis and neutrophil-mediated necrosis in a murine endotoxin shock model. J. Immunol. 160, 3480-3486.
48. 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.
49. Jaeschke, H., Gujral, J. S., and Bajt, M. L. (2004). Apoptosis and necrosis in liver disease. Liver Int. 24, 85-99.
50. Jaeschke, H., Ho Y.-S., Fisher, M. A., Lawson, J. A., and Farhood, A. (1999). Glutathione peroxidase deficient mice are more susceptible to neutrophil-mediated hepatic parenchymal cell injury during endotoxemia: Importance of an intracellular oxidant stress. Hepatology 29, 443-450.
51. 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.
52. Jaeschke, H., and Lemasters, J. J. (2003). Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125, 1246-1257.
53. Jahr, S., Hentze, H., Englisch, S., Hardt, D., Fackelmayer, F. O., Hesch, R. D., and Knippers, R. (2001). DNA fragments in the blood plasma of cancer patients: Quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 61, 1659-1665.
54. James, L. P., Lamps, L. W., McCullough, S., and Hinson, J. A. (2003a). Interleukin 6 and hepatocyte regeneration in acetaminophen toxicity in the mouse. Biochem. Biophys. Res. Common. 309, 857-863.
55. James, L. P., McCullough, S. S., Knight, T. R., Jaeschke, H., and Hinson, J. A. (2003b). Acetaminophen toxicity in mice lacking NADPH oxidase activity: Role of peroxynitrite formation and mitochondrial oxidant stress. Free Radic. Res. 37, 1289-1297.
56. James, L. P., McCullough, S. S., Lamps, L. W., and Hinson, J. A. (2003c). Effect of N-acetylcysteine on acetaminophen toxicity in mice: Relationship to reactive nitrogen and cytokine formation. Toxicol. Sci. 75, 458-467.
57. Jollow, D. J., Mitchell, J. R., Potter, W. Z., Davis, D. C., Gillette, J. R., and Brodie, B. B. (1973). Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo. J. Pharmacol. Exp. Ther. 187, 195-202.
58. Kamanaka, Y., Kawabata, A., Matsuya, H., Taga, C., Sekiguchi, F., and Kawao, N. (2003). Effect of a potent iNOS inhibitor (ONO-1714) on acetaminophen-induced hepatotoxicity in the rat. Life Sci. 74, 793-802.
59. Kim, J. S., He, L., and Lemasters, J. J. (2003). Mitochondrial permeability transition: A common pathway to necrosis and apoptosis. Biochem. Biophys. Res. Commun. 304, 463-470.
60. Kirsch, M., Lehnig, M., Korth, H. G., Sustmann, R., and de Groot, H. (2001). Inhibition of peroxynitrite-induced nitration of tyrosine by glutathione in the presence of carbon dioxide through both radical repair and peroxynitrate formation. Chemistry 7, 3313-3320.
61. Knight, T. R., Fariss, M. W., Farhood, A., and Jaeschke, H. (2003). Role of lipid peroxidation as a mechanism of liver injury after acetaminophen overdose in mice. Toxicol. Sci. 76, 229-236.
62. Knight, T. R., Ho, Y. S., Farhood, A., and Jaeschke, H. (2002). Peroxynitrite is a critical mediator of acetaminophen hepatotoxicity in murine livers: Protection by glutathione. J. Pharmacol. Exp. Ther. 303, 468-475.
63. Knight, T. R., and Jaeschke, H. (2002). Acetaminophen-induced inhibition of Fas receptor-mediated liver cell apoptosis: Mitochondrial dysfunction versus glutathione depletion. Toxicol. Appl. Pharmacol. 181, 133-141.
64. Knight, T. R., Kurtz, A., Bajt, M. L., Hinson, J. A., and Jaeschke, H. (2001). Vascular and hepatocellular peroxynitrite formation during acetaminophen-induced liver injury: Role of mitochondrial oxidant stress. Toxicol. Sci. 62, 212-220.
65. Kon, K., Kim, J. S., Jaeschke, H., and Lemasters, J. J. (2004a). Mitochondrial permeability transition in acetaminophen-induced necrotic and apoptotic cell death to cultured mouse hepatocytes. Hepatology 40, 1170-1179.
66. Kon, K., Kim, J. S., Jaeschke, H., and Lemasters, J. J. (2004b). Increase of cytosolic ferrous iron induces the mitochondrial permeability transition in acetaminophen-induced toxicity to mouse hepatocytes (abstract). Hepatology 40, 647A.
67. Lawson, J. A., Fisher, M. A., Simmons, C. A., Farhood, A., and Jaeschke, H. (1999). Inhibition of Fas receptor (CD95)-induced hepatic caspase activation and apoptosis by acetaminophen in mice. Toxicol. Appl. Pharmacol. 156, 179-186.
68. Lee, W. M. (2004). Acetaminophen and the U.S. Acute Liver Failure Study Group: Lowering the risks of hepatic failure. Hepatology 40, 6-9.
69. Limaye, P. B., Apte, U. M., Shankar, K., Bucci, T. J., Warbritton, A., and Mehendale, H. M. (2003). Calpain released from dying hepatocytes mediates progression of acute liver injury induced by model hepatotoxicants. Toxicol. Appl. Pharmacol. 191, 211-226.
70. Liu, X., Van Vleet, T., and Schnellmann, R. G. (2004). The role of calpain in oncotic cell death. Annu. Rev. Pharmacol. Toxicol. 44, 349-370.
71. Macanas-Pirard, P., Yaacob, N. S., Lee, P. C., Holder, J. C., Hinton, R. H., and Kass, G. E. (2005). Glycogen synthase kinase-3 mediates acetaminophen-induced apoptosis in human hepatoma cells. J. Pharmacol. Exp. Ther. 313, 780-789.
72. Masubuchi, Y., Suda, C., and Horie, T. (2005). Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice. J. Hepatol. 42, 110-116.
73. Mehendale, H. M. (2005). Tissue repair: An important determinant of final outcome of toxicant-induced injury. Toxicol. Pathol. 33, 41-51.
74. Meyer-Ficca, M. L., Meyer, R. G., Jacobson, E. L., and Jacobson, M. K. (2005). Poly(ADP-ribose) polymerases: Managing genome stability. Int. J. Biochem. Cell Biol. 37, 920-926.
75. Meyers, L. L., Beierschmitt, W. P., Khairallah, E. A., and Cohen, S. D. (1988). Acetaminophen-induced inhibition of mitochondrial respiration in mice. Toxicol. Appl. Pharmacol. 93, 378-387.
76. Michael, S. L., Mayeux, P. R., Bucci, T. J., Warbritton, A. R., Irwin, L. K., Pumford, N. R., and Hinson, J. A. (2001). Acetaminophen-induced hepatotoxicity in mice lacking inducible nitric oxide synthase activity. Nitric Oxide 5, 432-441.
77. Michalopoulos, G. K., and DeFrances, M. (2005). Liver regeneration. Adv. Biochem. Eng. Biotechnol. 93, 101-134.
78. Mitchell, J. R., Jollow, D. J., Potter, W. Z., Davis, D. C., Gillette, J. R., and Brodie, B. B. (1973a). Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism. J. Pharmacol. Exp. Ther. 187, 185-194.
79. Mitchell, J. R., Jollow, D. J., Potter, W. Z., Gillette, J. R., and Brodie, B. B. (1973b). Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J. Pharmacol. Exp. Ther. 187, 211-217.
80. Nagai, H., Matsumaru, K., Feng, G., and Kaplowitz, N. (2002). Reduced glutathione depletion causes necrosis and sensitization to tumor necrosis factor-alpha-induced apoptosis in cultured mouse hepatocytes. Hepatology 36, 55-64.
81. Nagata, S., Nagase, H., Kawane, K., Mukae, N., and Fukuyama, H. (2003). Degradation of chromosomal DNA during apoptosis. Cell Death Differ. 10, 108-116.
82. Nelson, S. D. (1990). Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Semin. Liver Dis. 10, 267-278.
83. Polson, J., and Lee, W. M. (2005). AASLD position paper: The management of acute liver failure. Hepatology 41, 1179-1197.
84. Pumford, N. R., Halmes, N. C., Martin, B. M., Cook, R. J., Wagner, C., and Hinson, J. A. (1997). Covalent binding of acetaminophen to N-10-formyltetrahydrofolate dehydrogenase in mice. J. Pharmacol. Exp. Ther. 280, 501-505.
85. Qiu, Y., Benet, L. Z., and Burlingame, A. L. (1998). Identification of the hepatic protein targets of reactive metabolites of acetaminophen in vivo in mice using two-dimensional gel electrophoresis and mass spectrometry. J. Biol. Chem. 273, 17940-17953.
86. 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 two-dimensional gel electrophoresis and mass spectrometry. Adv. Exp. Med. Biol. 500, 663-673.
87. Ramsay, R. R., Rashed, M. S., and Nelson, S. D. (1989). In vitro effects of acetaminophen metabolites and analogs on the respiration of mouse liver mitochondria. Arch. Biochem. Biophys. 273, 449-457.
88. Raucy, J. L., Lasker, J. M., Lieber, C. S., and Black, M. (1989). Acetaminophen activation by human liver cytochromes P450IIE1 and P450IA2. Arch. Biochem. Biophys. 271, 270-283.
89. Ray, S. D., Balasubramanian, G., Bagchi, D., and Reddy, C. S. (2001). Ca(2+)-calmodulin antagonist chlorpromazine and poly(ADP-ribose) polymerase modulators 4-aminobenzamide and nicotinamide influence hepatic expression of BCL-XL and P53 and protect against acetaminophen-induced programmed and unprogrammed cell death in mice. Free Radic. Biol. Med. 31, 277-291.
90. Ray, S. D., Kamendulis, L. M., Gurule, M. W., Yorkin, R. D., and Corcoran, G. B. (1993). Ca2+ antagonists inhibit DNA fragmentation and toxic cell death induced by acetaminophen. FASEB J. 7, 453-463.
91. Ray, S. D., Mumaw, V. R., Raje, R. R., and Fariss, M. W. (1996). Protection of acetaminophen-induced hepatocellular apoptosis and necrosis by cholesteryl hemisuccinate pretreatment. J. Pharmacol. Exp. Ther. 279, 1470-1483.
92. 2+ in the nucleus during acetaminophen-induced liver injury. Toxicol. Appl. Pharmacol. 106, 346-351.
93. 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.
94. Reilly, T. P., Bourdi, M., Brady, J. N., Pise-Masison, C. A., Radonovich, M. F., George, J. W., and Pohl, L. R. (2001). Expression profiling of acetaminophen liver toxicity in mice using microarray technology. Biochem. Biophys. Res. Commun. 282, 321-328.
95. Roberts, D. W., Bucci, T. J., Benson, R. W., Warbritton, A. R., McRae, T. A., Pumford, N. R., and Hinson, J. A. (1991). Immunohistochemical localization and quantification of the 3-(cystein-S-yl)-acetaminophen protein adduct in acetaminophen hepatotoxicity. Am. J. Pathol. 138, 359-371.
96. Rogers, L. K., Moorthy, B., and Smith, C. V. (1997). Acetaminophen binds to mouse hepatic and renal DNA at human therapeutic doses. Chem. Res. Toxicol. 10, 470-476.
97. Rogers, L. K., Valentine, C. J., Szczpyka, M., and Smith, C. V. (2000). Effects of hepatotoxic doses of acetaminophen and furosemide on tissue concentrations of CoASH and CoASSG in vivo. Chem. Res. Toxicol. 13, 873-882.
98. Ruepp, S. U., Tonge, R. P., Shaw, J., Wallis, N., and Pognan, F. (2002). Genomics and proteomics analysis of acetaminophen toxicity in mouse liver. Toxicol. Sci. 65, 135-150.
99. Rumack, B. H. (2004). Acetaminophen misconceptions. Hepatology 40, 10-15.
100. Salminen, W. F., Jr., Voellmy, R., and Roberts, S. M. (1998). Effect of N-acetylcysteine on heat shock protein induction by acetaminophen in mouse liver. J. Pharmacol. Exp. Ther. 286, 519-524.
101. 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.
102. Scorrano, L., and Korsmeyer, S. J. (2003). Mechanisms of cytochrome c release by proapoptotic BCL-2 family members. Biochem. Biophys. Res. Commun. 304, 437-444.
103. Shen, W., Kamendulis, L. M., Ray, S. D., and Corcoran, G. B. (1991). Acetaminophen-induced cytotoxicity in cultured mouse hepatocytes: Correlation of nuclear Ca2+ accumulation and early DNA fragmentation with cell death. Toxicol. Appl. Pharmacol. 111, 242-254.
104. Shen, W., Kamendulis, L. M., Ray, S. D., and Corcoran, G. B. (1992). Acetaminophen-induced cytotoxicity in cultured mouse hepatocytes: Effects of Ca(2+)-endonuclease, DNA repair, and glutathione depletion inhibitors on DNA fragmentation and cell death. Toxicol. Appl. Pharmacol. 112, 32-40.
105. Slitt, A. L., Naylor, L., Hoivik, J., Manautou, J. E., Macrides, T., and Cohen, S. D. (2004). The shark bile salt 5 beta-scymnol abates acetaminophen toxicity, but not covalent binding. Toxicology 203, 109-121.
106. Smith, C. V., Hughes, H., and Mitchell, J. R. (1986). Deferoxamine does not protect against acetaminophen-induced hepatic necrosis in vivo (abstract). Fed. Proc. 45, 572.
107. Susin, S. A., Daugas, E., Ravagnan, L., Samejima, K., Zamzami, N., Loeffler, M., Costantini, P., Ferri, K. F., Irinopoulou, T., Prevost, M. C., et al. (2000). Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192, 571-580.
108. Tinel, M., Berson, A., Vadrot, N., Descatoire, V., Grodet, A., Feldmann, G., Thenot, J. P., and Pessayre, D. (2004). Subliminal Fas stimulation increases the hepatotoxicity of acetaminophen and bromobenzene in mice. Hepatology 39, 655-666.
109. 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.
110. Tirmenstein, M. A., and Nelson, S. D. (1990). Acetaminophen-induced oxidation of protein thiols. Contribution of impaired thiol-metabolizing enzymes and the breakdown of adenine nucleotides. J. Biol. Chem. 265, 3059-3065.
111. Tsokos-Kuhn, J. O., Hughes, H., Smith, C. V., and Mitchell, J. R. (1988). Alkylation of the liver plasma membrane and inhibition of the Ca2+ ATPase by acetaminophen. Biochem. Pharmacol. 37, 2125-2131.
112. van Loo, G., Schotte, P., van Gurp, M., Demol, H., Hoorelbeke, B., Gevaert, K., Rodriguez, I., Ruiz-Carrillo, A., Vandekerckhove, J., Declercq, W., et al. (2001). Endonuclease G: A mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ. 8, 1136-1142.
113. Welch, K. D., Wen, B., Goodlett, D. R., Yi, E. C., Lee, H., Reilly, T. P., Nelson, S. D., and Pohl, L. R. (2005). Proteomic identification of potential susceptibility factors in drug-induced liver disease. Chem. Res. Toxicol. 18, 924-933.
114. Wendel, A., and Jaeschke, H. (1982). Drug-induced lipid peroxidation in mice-III. Glutathione content of liver, kidney and spleen after intravenous administration of free and liposomally entrapped glutathione. Biochem. Pharmacol. 31, 3607-3611.
115. Xiong, H., Turner, K. C., Ward, E. S., Jansen, P. L., and Brouwer, K. L. (2000). Altered hepatobiliary disposition of acetaminophen glucuronide in isolated perfused livers from multidrug resistance-associated protein 2-deficient TR(-) rats. J. Pharmacol. Exp. Ther. 295, 512-518.
116. Yakovlev, A. G., Wang, G., Stoica, B. A., Boulares, H. A., Spoonde, A. Y., Yoshihara, K., and Smulson, M. E. (2000). A role of the Ca2+/ mg2+-dependent endonuclease in apoptosis and its inhibition by Poly(ADP-ribose) polymerase. J. Biol. Chem. 275, 21302-21308.
117. Yakovlev, A. G., Wang, G., Stoica, B. A., Simbulan-Rosenthal, C. M., Yoshihara, K., and Smulson, M. E. (1999). Role of DNAS1L3 in Ca2+-and Mg2+-dependent cleavage of DNA into oligonucleosomal and high molecular mass fragments. Nucleic Acids Res. 27, 1999-2005.
118. Zamek-Gliszczynski, M. J., Hoffmaster, K. A., Tian, X., Zhao, R., Polli, J. W., Humphreys, J. E., Webster, L. O., Bridges, A. S., Kalvass, J. C., and Brouwer, K. L. (2005). Multiple mechanisms are involved in the biliary excretion of acetaminophen sulfate in the rat: Role of mrp2 and bcrp1. Drug Metab. Dispos. 33, 1158-1165.
119. Zhang, H., Cook, J., Nickel, J., Yu, R., Stecker, K., Myers, K., and Dean, N. M. (2000). Reduction of liver Fas expression by an antisense oligonucleotide protects mice from fulminant hepatitis. Nat. Biotechnol. 18, 862-867.