Acetaminophen-induced hepatotoxicity and protein nitration in neuronal nitric-oxide synthase knockout mice

Journal of Pharmacology and Experimental Therapeutics

Volumn 340, Issue 1, 2012, Pages 134-142

  Agarwal, Rakhee ^a   Hennings, Leah ^a   Rafferty, Tonya M ^a   Letzig, Lynda G ^a   McCullough, Sandra ^a   James, Laura P ^a   MacMillan Crow, Lee Ann ^a   Hinson, Jack A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYNONENAL; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GLUTATHIONE; MANGANESE SUPEROXIDE DISMUTASE; NEURONAL NITRIC OXIDE SYNTHASE; PARACETAMOL;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; COVALENT BOND; DRUG PROTEIN BINDING; ENZYME ACTIVITY; HISTOPATHOLOGY; LIVER TOXICITY; MALE; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; WILD TYPE;

ACETAMINOPHEN; ALANINE TRANSAMINASE; ANALGESICS, NON-NARCOTIC; ANIMALS; ASPARTATE AMINOTRANSFERASES; BLOTTING, WESTERN; CYSTEINE; CYTOPLASM; DRUG-INDUCED LIVER INJURY; LIVER; MALE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; NITRATES; NITRIC OXIDE SYNTHASE TYPE I; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

EID: 84055219018     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.184192     Document Type: Article

References (41)

1. Abdelmegeed MA, Moon KH, Chen C, Gonzalez FJ, and Song BJ (2010) Role of cytochrome P450 2E1 in protein nitration and ubiquitin-mediated degradation during acetaminophen toxicity. Biochem Pharmacol 79:57-66.
2. Agarwal R, MacMillan-Crow LA, Rafferty TM, Saba H, Roberts DW, Fifer EK, James LP, and Hinson JA (2011) Acetaminophen-induced hepatotoxicity in mice occurs with inhibition of activity and nitration of mitochondrial manganese superoxide dismutase. J Pharmacol Exp Ther 337:110-116.
3. Amimoto T, Matsura T, Koyama SY, Nakanishi T, Yamada K, and Kajiyama G (1995) Acetaminophen-induced hepatic injury in mice: the role of lipid peroxidation and effects of pretreatment with coenzyme Q10 and α-tocopherol. Free Radic Biol Med 19:169-176.
4. Boobis AR, Seddon CE, Nasseri-Sina P, and Davies DS (1990) Evidence for a direct role of intracellular calcium in paracetamol toxicity. Biochem Pharmacol 39:1277-1281. (Pubitemid 20119202)
5. Boobis AR, Tee LB, Hampden CE, and Davies DS (1986) Freshly isolated hepatocytes as a model for studying the toxicity of paracetamol. Food Chem Toxicol 24:731-736. (Pubitemid 17184058)
6. Bourdi M, Eiras DP, Holt MP, Webster MR, Reilly TP, Welch KD, and Pohl LR (2007) Role of IL-6 in an IL-10 and IL-4 double knockout mouse model uniquely susceptible to acetaminophen-induced liver injury. Chem Res Toxicol 20:208-216. (Pubitemid 46408857)
7. Brookes PS (2004) Mitochondrial nitric oxide synthase. Mitochondrion 3:187-204.
8. Burke AS, MacMillan-Crow LA, and Hinson JA (2010) Reactive nitrogen species in acetaminophen-induced mitochondrial damage and toxicity in mouse hepatocytes. Chem Res Toxicol 23:1286-1292.
9. 2+ to the mitochondrial permeability transition induced by tert-butylhydroperoxide in rat hepatocytes. Hepatology 29:1523-1531.
10. Dahlin DC, Miwa GT, Lu AY, and Nelson SD (1984) N-acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen. Proc Natl Acad Sci U S A 81:1327-1331. (Pubitemid 14173462)
11. Esterbauer H (1996) Estimation of peroxidative damage. A critical review. Pathol Biol (Paris) 44:25-28.
12. Fujimoto K, Kumagai K, Ito K, Arakawa S, Ando Y, Oda S, Yamoto T, and Manabe S (2009) Sensitivity of liver injury in heterozygous Sod2 knockout mice treated with troglitazone or acetaminophen. Toxicol Pathol 37:193-200.
13. Ghafourifar P and Cadenas E (2005) Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26:190-195. (Pubitemid 40432654)
14. Grewal KK and Racz WJ (1993) Intracellular calcium disruption as a secondary event in acetaminophen-induced hepatotoxicity. Can J Physiol Pharmacol 71:26-33. (Pubitemid 23172120)
15. Hinson JA, Bucci TJ, Irwin LK, Michael SL, and Mayeux PR (2002) Effect of inhibitors of nitric oxide synthase on acetaminophen-induced hepatotoxicity in mice. Nitric Oxide 6:160-167. (Pubitemid 34848438)
16. Hinson JA, Pike SL, Pumford NR, and Mayeux PR (1998) Nitrotyrosine- protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice. Chem Res Toxicol 11:604-607. (Pubitemid 28285584)
17. Hoffmann KJ, Streeter AJ, Axworthy DB, and Baillie TA (1985) Identification of the major covalent adduct formed in vitro and in vivo between acetaminophen and mouse liver proteins. Mol Pharmacol 27:566-573. (Pubitemid 15098314)
18. Institute of Laboratory Animal Resources (1996) Guide for the Care and Use of Laboratory Animals 7th ed. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, Washington DC.
19. Jaeschke H, Knight TR, and Bajt ML (2003) The role of oxidant stress and reactive nitrogen species in acetaminophen hepatotoxicity. Toxicol Lett 144:279-288. (Pubitemid 36966712)
20. James LP, Mayeux PR, and Hinson JA (2003) Acetaminophen-induced hepatotoxicity. Drug Metab Dispos 31:1499-1506. (Pubitemid 37466918)
21. Kamiyama T, Sato C, Liu J, Tajiri K, Miyakawa H, and Marumo F (1993) Role of lipid peroxidation in acetaminophen-induced hepatotoxicity: comparison with carbon tetrachloride. Toxicol Lett 66:7-12.
22. Kaplowitz N, Shinohara M, Liu ZX, and Han D (2008) How to protect against acetaminophen: don't ask for JUNK. Gastroenterology 135:1047-1051.
23. Kon K, Kim JS, Jaeschke H, and Lemasters JJ (2004) Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 40:1170-1179. (Pubitemid 39425573)
24. MacMillan-Crow LA, Crow JP, Kerby JD, Beckman JS, and Thompson JA (1996) Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc Natl Acad Sci U S A 93:11853-11858. (Pubitemid 26347213)
25. MacMillan-Crow LA and Cruthirds DL (2001) Invited review: manganese superoxide dismutase in disease. Free Radic Res 34:325-336.
26. McCord JM and Fridovich I (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049-6055.
27. Michael SL, Mayeux PR, Bucci TJ, Warbritton AR, Irwin LK, Pumford NR, and Hinson JA (2001) Acetaminophen-induced hepatotoxicity in mice lacking inducible nitric oxide synthase activity. Nitric Oxide 5:432-441. (Pubitemid 32953593)
28. Mitchell JR, Jollow DJ, Potter WZ, Davis DC, Gillette JR, and Brodie BB (1973a) Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism. J Pharmacol Exp Ther 187:185-194.
29. Mitchell JR, Jollow DJ, Potter WZ, Gillette JR, and Brodie BB (1973) Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J Pharmacol Exp Ther 187:211-217.
30. Moore M, Thor H, Moore G, Nelson S, Moldéus P, and Orrenius S (1985) The toxicity of acetaminophen and N-acetyl-p-benzoquinone imine in isolated hepatocytes is associated with thiol depletion and increased cytosolic Ca2+. J Biol Chem 260:13035-13040. (Pubitemid 16209772)
31. Muldrew KL, James LP, Coop L, McCullough SS, Hendrickson HP, Hinson JA, and Mayeux PR (2002) Determination of acetaminophen-protein adducts in mouse liver and serum and human serum after hepatotoxic doses of acetaminophen using high-performance liquid chromatography with electrochemical detection. Drug Metab Dispos 30:446-451. (Pubitemid 34263830)
32. Ozden O, Park SH, Kim HS, Jiang H, Coleman MC, Spitz DR, and Gius D (2011) Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging 3:102-107.
33. Reid AB, Kurten RC, McCullough SS, Brock RW, and Hinson JA (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. (Pubitemid 40189547)
34. Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, Kirk M, and Freeman BA (1994) Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J Biol Chem 269:26066-26075.
35. Schöpfer F, Riobó N, Carreras MC, Alvarez B, Radi R, Boveris A, Cadenas E, and Poderoso JJ (2000) Oxidation of ubiquinol by peroxynitrite: implications for protection of mitochondria against nitrosative damage. Biochem J 349:35-42. (Pubitemid 30440162)
36. Stolz DB, Zamora R, Vodovotz Y, Loughran PA, Billiar TR, Kim YM, Simmons RL, and Watkins SC (2002) Peroxisomal localization of inducible nitric oxide synthase in hepatocytes. Hepatology 36:81-93. (Pubitemid 34700765)
37. Tirmenstein MA and Nelson SD (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. (Pubitemid 19159244)
38. Waeg G, Dimsity G, and Esterbauer H (1996) Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins. Free Radic Res 25:149-159. (Pubitemid 26345345)
39. Yoshikawa Y, Morita M, Hosomi H, Tsuneyama K, Fukami T, Nakajima M, and Yokoi T (2009) Knockdown of superoxide dismutase 2 enhances acetaminophen- induced hepatotoxicity in rat. Toxicology 264:89-95.
40. Younes M, Cornelius S, and Siegers CP (1986) Ferrous ion supported in vivo lipid peroxidation induced by paracetamol-its relation to hepatotoxicity. Res Commun Chem Pathol Pharmacol 51:89-99. (Pubitemid 16185478)
41. Zorov DB, Filburn CR, Klotz LO, Zweier JL, and Sollott SJ (2000) Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001-1014.