Carbamazepine-induced liver injury requires CYP3A-mediated metabolism and glutathione depletion in rats

Drug Metabolism and Disposition

Volumn 43, Issue 7, 2015, Pages 958-968

  Iida, Azumi ^a   Sasaki, Eita ^a   Yano, Azusa ^a   Tsuneyama, Koichi ^b   Fukami, Tatsuki ^a   Nakajima, Miki ^a   Yokoi, Tsuyoshi ^a,c  

^a KANAZAWA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOYAMA   (Japan)

^c NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

10,11 DIHYDRO 10,11 DIHYDROXYCARBAMAZEPINE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BUTHIONINE SULFOXIMINE; CARBAMAZEPINE; CARBAMAZEPINE 10,11 OXIDE; CYTOCHROME P450 3A; DEXAMETHASONE; DRUG METABOLITE; GLUTATHIONE; KETOCONAZOLE; OXCARBAZEPINE; TROLEANDOMYCIN; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; ENZYME INHIBITOR;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CONTROLLED STUDY; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG METABOLISM; LIVER MICROSOME; LIVER NECROSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REPEATED DRUG DOSE; SINGLE DRUG DOSE; TOXIC HEPATITIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYME INDUCTION; ENZYMOLOGY; FISCHER 344 RAT; HYDROXYLATION; LIVER; METABOLISM;

RATTUS;

ALANINE TRANSAMINASE; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIFUNGAL AGENTS; BUTHIONINE SULFOXIMINE; CARBAMAZEPINE; CYTOCHROME P-450 CYP3A; DRUG-INDUCED LIVER INJURY; ENZYME INDUCTION; ENZYME INHIBITORS; GLUTATHIONE; HYDROXYLATION; KETOCONAZOLE; LIVER; MALE; MICROSOMES, LIVER; RATS; RATS, INBRED F344; TROLEANDOMYCIN;

EID: 84940384506     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.115.063370     Document Type: Article

References (50)

1. Ahmed SN and Siddiqi ZA (2006) Antiepileptic drugs and liver disease. Seizure 15:156-164.
2. Allameh A, Vansoun EY, and Zarghi A (1997) Role of glutathione conjugation in protection of weanling rat liver against acetaminophen-induced hepatotoxicity. Mech Ageing Dev 95:71-79.
3. Beghi E and Perucca E (1995) The management of epilepsy in the 1990s. Acquisitions, uncertainties and priorities for future research. Drugs 49:680-694.
4. Björnsson E (2008) Hepatotoxicity associated with antiepileptic drugs. Acta Neurol Scand 118: 281-290.
5. Björnsson E and Olsson R (2005) Outcome and prognostic markers in severe drug-induced liver disease. Hepatology 42:481-489.
6. Bollard ME, Keun HC, Beckonert O, Ebbels T.M., Antti H., Nicholls AW, Shockcor JP, Cantor GH, Stevens G, and Lindon JC, et al. (2005) Comparative metabonomics of differential hy-drazine toxicity in the rat and mouse. Toxicol Appl Pharmacol 204:135-151.
7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
8. Bühler R., Lindros KO, Nordling A, Johansson I., and Ingelman-Sundberg M (1992) Zonation of cytochrome P450 isozyme expression and induction in rat liver. Eur J Biochem 204:407-412.
9. Clayton NP, Yoshizawa K, Kissling G.E., Burka LT, Chan PC, and Nyska A (2007) Immuno-histochemical analysis of expressions of hepatic cytochrome P450 in F344 rats following oral treatment with kava extract. Exp Toxicol Pathol 58:223-236.
10. Crincoli CM, Patel NN, Tchao R, and Harvison PJ (2008) Role of biotransformation in 3-(3,5-dichlorophenyl)-2,4-thiazolidinedione-induced hepatotoxicity in Fischer 344 rats. Toxicology 250:100-108.
11. Emoto C, Yamazaki H, Yamasaki S., Shimada N, Nakajima M, and Yokoi T (2000) Characterization of cytochrome P450 enzymes involved in drug oxidations in mouse intestinal microsomes. Xenobiotica 30:943-953.
12. Fox A, Gentry C, Patel S., Kesingland A, and Bevan S (2003) Comparative activity of the anti-convulsants oxcarbazepine, carbamazepine, lamotrigine and gabapentin in a model of neuropathic pain in the rat and guinea-pig. Pain 105:355-362.
13. Gao W, Mizukawa Y, Nakatsu N., Minowa Y, Yamada H, Ohno Y., and Urushidani T (2010) Mechanism-based biomarker gene sets for glutathione depletion-related hepatotoxicity in rats. Toxicol Appl Pharmacol 247:211-221.
14. Gardner I, Wakazono H, Bergin P., de Waziers I, Beaune P, Kenna J.G., and Caldwell J (1997) Cytochrome P450 mediated bioactivation of methyleugenol to 1'-hydroxymethyleugenol in Fischer 344 rat and human liver microsomes. Carcinogenesis 18:1775-1783.
15. Griffith OW and Meister A (1979) Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S-n-butyl homocysteine sulfoximine). J Biol Chem 254:7558-7560.
16. Harstad EB and Klaassen CD (2002) Analysis of strain difference in sensitivity to cadmium-induced hepatotoxicity in Fischer 344 and Sprague-Dawley rats. Toxicol Sci 67:329-340.
17. Higuchi S, Yano A, Takai S., Tsuneyama K, Fukami T, Nakajima M., and Yokoi T (2012) Metabolic activation and inflammation reactions involved in carbamazepine-induced liver injury. Toxicol Sci 130:4-16.
18. Ju C and Uetrecht JP (1999) Detection of 2-hydroxyiminostilbene in the urine of patients taking carbamazepine and its oxidation to a reactive iminoquinone intermediate. J Pharmacol Exp Ther 288:51-56.
19. Kaplowitz N (2005) Idiosyncratic drug hepatotoxicity. Nat Rev Drug Discov 4:489-499.
20. Kerr BM, Thummel KE, Wurden C.J., Klein SM, Kroetz DL, Gonzalez FJ, and Levy RH (1994) Human liver carbamazepine metabolism. Role of CYP3A4 and CYP2C8 in 10,11-epoxide formation. Biochem Pharmacol 47:1969-1979.
21. Kobayashi K, Urashima K, Shimada N., and Chiba K (2003) Selectivities of human cytochrome P450 inhibitors toward rat P450 isoforms: study with cDNA-expressed systems of the rat. Drug Metab Dispos 31:833-836.
22. Kobayashi M, Higuchi S, Ide M., Nishikawa S, Fukami T, Nakajima M., and Yokoi T (2012a) Th2 cytokine-mediated methimazole-induced acute liver injury in mice. J Appl Toxicol 32: 823-833.
23. Kobayashi Y, Fukami T, Nakajima A., Watanabe A, Nakajima M, and Yokoi T (2012b) Species differences in tissue distribution and enzyme activities of arylacetamide deacetylase in human, rat, and mouse. Drug Metab Dispos 40:671-679.
24. Kostrubsky VE, Szakacs JG, Jeffery E.H., Wood SG, Bement WJ, Wrighton SA, Sinclair P.R., and Sinclair JF (1997) Role of CYP3A in ethanol-mediated increases in acetaminophen hep-atotoxicity. Toxicol Appl Pharmacol 143:315-323.
25. Kotegawa T, Laurijssens BE, Von Moltke LL, Cotreau MM, Perloff MD, Venkatakrishnan K, Warrington J.S., Granda BW, Harmatz JS, and Greenblatt DJ (2002) In vitro, pharmacokinetic, and pharmacodynamic interactions of ketoconazole and midazolam in the rat. J Pharmacol Exp Ther 302:1228-1237.
26. Lake BG, Renwick AB, Cunninghame M.E., Price RJ, Surry D, and Evans DC (1998) Comparison of the effects of some CYP3A and other enzyme inducers on replicative DNA synthesis and cytochrome P450 isoforms in rat liver. Toxicology 131:9-20.
27. Lee WM (2003) Drug-induced hepatotoxicity. N Engl J Med 349:474-485.
28. Lertratanangkoon K and Horning MG (1982) Metabolism of carbamazepine. Drug Metab Dispos 10:1-10.
29. Lillibridge JH, Amore BM, Slattery J.T., Kalhorn TF, Nelson SD, Finnell RH, and Bennett GD (1996) Protein-reactive metabolites of carbamazepine in mouse liver microsomes. Drug Metab Dispos 24:509-514.
30. Mather GG and Levy RH (2000) Anticonvulsants, in Metabolic Drug Interactions (Levy RH, Thummel KE, Trager WF, Hansten PD, and Eichelbaum M, eds) pp 217-232, Lippincott Williams & Wilkins, Philadelphia, PA.
31. Nishiya T, Mori K, Hattori C., Kai K, Kataoka H, Masubuchi N., Jindo T, and Manabe S (2008) The crucial protective role of glutathione against tienilic acid hepatotoxicity in rats. Toxicol Appl Pharmacol 232:280-291.
32. Oscarson M, Zanger UM, Rifki O.F., Klein K., Eichelbaum M, and Meyer UA (2006) Tran-scriptional profiling of genes induced in the livers of patients treated with carbamazepine. Clin Pharmacol Ther 80:440-456.
33. Park BK, Kitteringham NR, Maggs J.L., Pirmohamed M., and Williams DP (2005) The role of metabolic activation in drug-induced hepatotoxicity. Annu Rev Pharmacol Toxicol 45: 177-202.
34. Pearce RE, Vakkalagadda GR, and Leeder JS (2002) Pathways of carbamazepine bioactivation in vitro I. Characterization of human cytochromes P450 responsible for the formation of 2- and 3-hydroxylated metabolites. Drug Metab Dispos 30:1170-1179.
35. Pearce RE, Uetrecht JP, and Leeder JS (2005) Pathways of carbamazepine bioactivation in vitro: II. The role of human cytochrome P450 enzymes in the formation of 2-hydroxyiminostilbene. Drug Metab Dispos 33:1819-1826.
36. Pirmohamed M, Kitteringham NR, Breckenridge A.M., and Park BK (1992a) Detection of an autoantibody directed against human liver microsomal protein in a patient with carbamazepine hypersensitivity. Br J Clin Pharmacol 33:183-186.
37. Pirmohamed M, Kitteringham NR, Guenthner T.M., Breckenridge AM, and Park BK (1992b) An investigation of the formation of cytotoxic, protein-reactive and stable metabolites from car-bamazepine in vitro. Biochem Pharmacol 43:1675-1682.
38. Renton KW (2001) Alteration of drug biotransformation and elimination during infection and inflammation. Pharmacol Ther 92:147-163.
39. Shaw PJ, Hopfensperger MJ, Ganey P.E., and Roth RA (2007) Lipopolysaccharide and trova-floxacin coexposure in mice causes idiosyncrasy-like liver injury dependent on tumor necrosis factor-alpha. Toxicol Sci 100:259-266.
40. Shimizu S, Atsumi R, Itokawa K., Iwasaki M, Aoki T, Ono C., Izumi T, Sudo K, and Okazaki O (2009) Metabolism-dependent hepatotoxicity of amodiaquine in glutathione-depleted mice. Arch Toxicol 83:701-707.
41. Shimizu S, Atsumi R, Nakazawa T., Izumi T, Sudo K, Okazaki O., and Saji H (2011) Ticlopidine-induced hepatotoxicity in a GSH-depleted rat model. Arch Toxicol 85:347-353.
42. Steup DR, Wiersma D, McMillan D.A., and Sipes IG (1991) Pretreatment with drinking water solutions containing trichloroethylene or chloroform enhances the hepatotoxicity of carbon tetrachloride in Fischer 344 rats. Fundam Appl Toxicol 16:798-809.
43. Stine ER, Gunawardhana L, and Sipes IG (1991) The acute hepatotoxicity of the isomers of dichlorobenzene in Fischer-344 and Sprague-Dawley rats: isomer-specific and strain-specific differential toxicity. Toxicol Appl Pharmacol 109:472-481.
44. Tateishi T, Asoh M, Nakura H., Watanabe M, Tanaka M, Kumai T., and Kobayashi S (1999) Carba-mazepine induces multiple cytochrome P450 subfamilies in rats. Chem Biol Interact 117:257-268.
45. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502-522.
46. Uetrecht J (2007) Idiosyncratic drug reactions: current understanding. Annu Rev Pharmacol Toxicol 47:513-539.
47. Wang X, Lee WY, Or P.M., and Yeung JH (2010) Pharmacokinetic interaction studies of tanshinones with tolbutamide, a model CYP2C11 probe substrate, using liver microsomes, primary hepatocytes and in vivo in the rat. Phytomedicine 17:203-211.
48. Watanabe T, Sagisaka H, Arakawa S., Shibaya Y, Watanabe M, Igarashi I., Tanaka K, Totsuka S, Takasaki W., and Manabe S (2003) A novel model of continuous depletion of glutathione in mice treated with L-buthionine (S, R)-sulfoximine. J Toxicol Sci 28:455-469.
49. Zaccara G, Franciotta D, and Perucca E (2007) Idiosyncratic adverse reactions to antiepileptic drugs. Epilepsia 48:1223-1244.
50. Zou W, Devi SS, Sparkenbaugh E, Younis H.S., Roth RA, and Ganey PE (2009) Hepatotoxic interaction of sulindac with lipopolysaccharide: role of the hemostatic system. Toxicol Sci 108:184-193.