Acetaminophen toxicity in mice lacking NADPH oxidase activity: Role of peroxynitrite formation and mitochondrial oxidant stress

Free Radical Research

Volumn 37, Issue 12, 2003, Pages 1289-1297

  James, Laura P ^a,c   McCullough, Sandra S ^a   Knight, Tamara R ^b   Jaeschke, Hartmut ^b   Hinson, Jack A ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c ARKANSAS CHILDREN S HOSPITAL   (United States)

Author keywords

Acetaminophen; Glutathione; NADPH oxidase; Nitrotyrosine; Peroxynitrite; Superoxide

Indexed keywords

3 NITROTYROSINE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; LIVER ENZYME; PARACETAMOL; PEROXYNITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; DOSE RESPONSE; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME SUBUNIT; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LIVER CELL; LIVER MITOCHONDRION; LIVER TOXICITY; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; REVIEW; TOXICITY TESTING; VASCULAR ENDOTHELIUM; WILD TYPE;

ACETAMINOPHEN; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ENDOTHELIUM, VASCULAR; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEPATOCYTES; HYDROGEN PEROXIDE; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; NADPH OXIDASE; OXIDATIVE STRESS; PEROXYNITROUS ACID; SUPEROXIDES; TYROSINE;

ANIMALIA;

EID: 0344117500     PISSN: 10715762     EISSN: None     Source Type: Journal    
DOI: 10.1080/10715760310001617776     Document Type: Review

References (33)

1. Roberts, D.W., Bucci, T.J., Benson, R.W., Warbritton, A.R., McRae, T.A., Pumford, N.R., et al. (1991) "Immunohistochemical localization and quantification of the 3-(cystein-S-yl)-acetaminophen protein adduct in acetaminophen hepatotoxicity", Am. J. Pathol. 138(2), 359-371.
2. Nakae, D., Yoshiji, H., Yamamoto, K., Maruyama, H., Kinugasa, T., Takashima, Y., et al. (1990) "Influence of timing of administration of liposome-encapsulated superoxide dismutase on its prevention of acetaminophen-induced liver cell necrosis in rats", Acta Pathol. Jpn. 40(8), 568-573.
3. Jaeschke, H. (1990) "Glutathione disulfide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: the protective effect of allopurinol", J. Pharmacol. Exp. Ther. 255(3), 935-941.
4. Smith, C.V. and Mitchell, J.R. (1985) "Acetaminophen hepatotoxicity in vivo is not accompanied by oxidant stress", Biochem. Biophys. Res. Commun. 133(1), 329-336.
5. Smith, C.V., Hughes, H., Lauterburg, B.H. and Mitchell, J.R. (1985) "Oxidant stress and hepatic necrosis in rats treated with diquat", J. Pharmacol. Exp. Ther. 235(1), 172-177.
6. Laskin, D.L., Gardner, C.R., Price, V.F. and Jollow, D.J. (1995) "Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen", Hepatology 21(4), 1045-1050.
7. Blazka, M.E., Germolec, D.R., Simeonove, P., Bruccoleri, A., Pennypacker, K.R. and Luster, M.I. (1995) "Acetaminophen-induced hepatotoxicity is associated with early changes in NF-kB and NF-IL6 DNA binding activity", J. Inflamm. 47(3), 138-150.
8. Goldin, R.D., Ratnayaka, I.D., Breach, C.S., Brown, I.N. and Wickramasinghe, S.N. (1996) "Role of macrophages in acetaminophen (paracetamol)-induced hepatotoxicity", J. Pathol. 179(4), 432-435.
9. Squadrito, G.L. and Pryor, W.A. (1998) "Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite, and carbon dioxide", Free Radic. Biol. Med. 25(4-5), 392-403.
10. 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(6), 604-607.
11. Hinson, J.A., Michael, S.L., Ault, S.G. and Pumford, N.R. (2000) "Western blot analysis for nitrotyrosine protein adducts in livers of saline-treated and acetaminophen-treated mice", Toxicol. Sci. 53(2), 467-473.
12. Michael, S.L., Pumford, N.R., Mayeux, P.R., Niesman, M.R. and Hinson, J.A. (1999) "Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species", Hepatology 30(1), 186-195.
13. Gorlach, A., Brandes, R.P., Nguyen, K., Amidi, M., Dehghani, F. and Busse, R. (2000) "A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall", Circ. Res. 87(1), 26-32.
14. Hsich, E., Segal, B.H., Pagano, P.J., Rey, F.E., Paigen, B., Deleonardis, J., et al. (2000) "Vascular effects following homozygous disruption of p47(phox): an essential component of NADPH oxidase", Circulation 101(11), 1234-1236.
15. Dinauer, M.C. (1993) "The respiratory burst oxidase and the molecular genetics of chronic granulomatous disease", Crit. Rev. Clin. Lab. Sci. 30(4), 329-369.
16. Curnutte, J.T. (1993) "Chronic granulomatous disease: the solving of a clinical riddle at the molecular level", Clin. Immunol. Immunopathol. 67((3 pt 2), S2-S15.
17. Pollock, J.D., Williams, D.A., Gifford, M.A., Li, L.L., Du, X., Fisherman, J., et al. (1995) "Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production", Nat. Genet. 9(2), 202-209.
18. Kirk, E.A., Dinauer, M.C., Rosen, H., Chait, A., Heinecke, J.W. and LeBoeuf, R.C. (2000) "Impaired superoxide production due to a deficiency in phagocyte NADPH oxidase fails to inhibit atherosclerosis in mice", Arterioscler. Thromb. Vasc. Biol. 20(6), 1529-1535.
19. 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(1), 211-217.
20. Knight, T.R., Kurtz, A., Bajt, M.L., Hinson, J.A. and Jaeschke, H. (2001) "Vascular and hepatocellular peroxynitrite formation during acetaminophen toxicity: role of mitochondrial oxidant stress", Toxicol. Sci. 62(2), 212-220.
21. Winwood, P.J. and Arthur, M.J. (1993) "Kupffer cells: their activation and role in animal models of liver injury and human liver disease", Semin. Liver Dis. 13(1), 50-59.
22. Badwey, J.A. and Karnovsky, M.L. (1980) "Active oxygen species and the functions of phagocytic leukocytes", Annu. Rev. Biochem. 49, 695-726.
23. Morgenstern, D.E., Gifford, M.A., Li, L.L., Doerschuk, C.M. and Dinauer, M.C. (1997) "Absence of respiratory burst in X-linked chronic granulomatous disease mice leads to abnormalities in both host defense and inflammatory response to Aspergillus fumigatus", J. Exp. Med. 185(2), 207-218.
24. Harada, H., Hines, I.N., Hoffman, J.M., Gao, B., Flores, S., McCord, J.M. and Grisham, M.B. (2002) "Role of NADPH oxidase-derived superoxide in reduced size liver ischemia and reperfusion injury in mice", Hepatology 36(4), 175A.
25. Esterline, R.L., Ray, S.D. and Ji, S. (1989) "Reversible and irreversible inhibition of hepatic mitochondrial respirtion by acetaminophen and its toxic metabolite, N-acetyl-p-benzoquinoneimine (NAPQI)", Biochem. Pharmacol. 38(14), 2387-2390.
26. Pumford, N.R., Hinson, J.A., Benson, R.W. and Roberts, D.W. (1990) "Immunoblot analysis of protein containing 3-(cystein-S-yl)acetaminophen adducts in serum and subcellular liver fractions from acetaminophen-treated mice", Toxicol. Appl. Pharmacol. 104(3), 521-532.
27. DeLeve, L.D., Wang, X., Kaplowitz, N., Shulman, H.M., Bart, J.A. and van der Hoek, A. (1997) "Sinusoidal endothelial cells as a target for acetaminophen toxicity. Direct action versus requirement for hepatocyte activation in different mouse strains", Biochem. Pharmacol. 53(9), 1339-1345.
28. Steinberg, P., Lafranconi, W.M., Wolf, C.R., Waxman, D.J., Oesch, F. and Friedberg, T. (1987) "Xenobiotic metabolising enzymes are not restricted to parenchymal cells in rat liver", Mol. Pharmacol. 32(4), 463-470.
29. Steinberg, P., Schlemper, B., Molitor, E., Platt, K.L., Seidel, A. and Oesch, F. (1990) "Rat liver endothelial and Kupffer cell-mediated mutagenicity of polycyclic aromatic hydrocarbons and aflatoxin B1", Environ. Health Perspect. 88, 71-76.
30. Deaciuc, I.V., D'Souza, N.B., Sarphie, T.G., Schmidt, J., Hill, D.B. and McClain, C.J. (1999) "Effects of exogenous superoxide anion and nitric oxide on the scavenging function and electron microscopic appearance of the sinusoidal endothelium, in the isolated, perfused rat liver", J. Hepatol. 30(2), 213-221.
31. Lawson, J.A., Farhood, A., Hopper, R.D., Bajt, M.L. and Jaeschke, H. (2000) "The hepatic inflammatory response after acetaminophen overdose: role of neutrophils", Toxicol. Sci. 54(2), 509-516.
32. Suh, Y.A., Arnold, R.S., Lassegue, B., Shi, J., Xu, X., Sorescu, D., et al. (1999) "Cell transformation by the superoxide-generating oxidase Mox 1", Nature 401(6748), 79-82.
33. Arbiser, J.L., Petros, J., Klafter, R., Govindarajan, B., McLaughlin, E.R., Brown, L.F., et al. (2002) "Reactive oxygen generated by Nox 1 triggers the angiogenic switch", Proc. Natl Acad. Sci. USA 99(2), 715-720.