Relationship between coumarin-induced hepatocellular toxicity and mitochondrial function in rats

Food and Chemical Toxicology

Volumn 90, Issue , 2016, Pages 1-9

  Tanaka, Yasuhiro ^a,b   Fujii, Wataru ^a   Hori, Hisako ^a   Kitagawa, Yoshinori ^a   Ozaki, Kiyokazu ^b  

^a SUNTORY LTD   (Japan)

^b SETSUNAN UNIVERSITY   (Japan)

Author keywords

Coumarin; CYP2E1; Hepatotoxicity; Mitochondria; Rat; Subcellular localization

Indexed keywords

ACONITATE HYDRATASE; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; ASPARTATE AMINOTRANSFERASE; BILIRUBIN; COUMARIN; CYTOCHROME P450 2E1; GAMMA GLUTAMYLTRANSFERASE; GLUTAMATE DEHYDROGENASE; GLUTATHIONE TRANSFERASE; COUMARIN DERIVATIVE; GLUTATHIONE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILIRUBIN BLOOD LEVEL; BODY WEIGHT; CELL FUNCTION; CONTROLLED STUDY; ENZYME BLOOD LEVEL; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LIVER FUNCTION TEST; LIVER NECROSIS; LIVER TOXICITY; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; ORGAN WEIGHT; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; ANIMAL; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG ADMINISTRATION; DRUG EFFECTS; LIVER MITOCHONDRION; METABOLISM; NECROSIS; PATHOLOGY; SPRAGUE DAWLEY RAT; TOXIC HEPATITIS;

ACONITATE HYDRATASE; ANIMALS; CHEMICAL AND DRUG INDUCED LIVER INJURY; COUMARINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; GLUTATHIONE; MALE; MITOCHONDRIA, LIVER; NECROSIS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84956943053     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2016.01.007     Document Type: Article

References (40)

1. Abraham K., Wöhrlin F., Lindtner O., Heinemeyer G., Lampen A. Toxicology and risk assessment of coumarin: focus on human data. Mol. Nutr. Food Res. 2010, 54:228-239.
2. Bansal S., Liu C.P., Sepuri N.B., Anandatheerthavarada H.K., Selvaraj V., Hoek J., Milne G.L., Guengerich F.P., Avadhani N.G. Mitochondria-targeted cytochrome P450 2E1 induces oxidative damage and augments alcohol-mediated oxidative stress. J. Biol. Chem. 2010, 285:24609-24619.
3. Bansal S., Anandatheerthavarada H.K., Prabu G.K., Milne G.L., Martin M.V., Guengerich F.P., Avadhani N.G. Human cytochrome P450 2E1 mutations that alter mitochondrial targeting efficiency and susceptibility to ethanol-induced toxicity in cellular models. J. Biol. Chem. 2013, 288:12627-12644.
4. Begriche K., Massart J., Robin M.A., Borgne-Sanchez A., Fromenty B. Drug-induced toxicity on mitochondria and lipid metabolism: mechanistic diversity and deleterious consequences for the liver. J. Hepatol. 2011, 54:773-794.
5. Born S.L., Rodriguez P.A., Eddy C.L., Lehman-McKeeman L.D. Synthesis and reactivity of coumarin 3,4-epoxide. Drug Metab. Dispos. 1997, 25:1318-1324.
6. Born S.L., Hu J.K., Lehman-McKeeman L.D. o-hydroxyphenylacetaldehyde is a hepatotoxic metabolite of coumarin. Drug Metab. Dispos. 2000, 28:218-223.
7. Born S.L., Caudill D., Fliter K.L., Purdon M.P. Identification of the cytochromes P450 that catalyze coumarin 3,4-epoxidation and 3-hydroxylation. Drug Metab. Dispos. 2002, 30:483-487.
8. Chandrasekaran V.R., Hsu D.Z., Liu M.Y. The protective effect of sesamol against mitochondrial oxidative stress and hepatic injury in acetaminophen-overdosed rats. Shock 2009, 32:89-93.
9. Chandrasekaran V.R., Chien S.P., Hsu D.Z., Chang Y.C., Liu M.Y. Effects of sesame oil against after the onset of acetaminophen-induced acute hepatic injury in rats. J. Parenter. Enter. Nutr. 2010, 34:567-573.
10. Cohen A.J. Critical review of the toxicology of coumarin with special reference to interspecies differences in metabolism and hepatotoxic response and their significance to man. Food Cosmet. Toxicol. 1979, 17:277-289.
11. Den Besten C., Körösi S.A., Beamand J.A., Walters D.G., Lake B.G. Studies on the mechanism of coumarin-induced toxicity in rat hepatocytes. Toxicol. Vitro 1990, 4:518-521.
12. Fentem J.H., Fry J.R., Thomas N.W. Species differences in the hepatotoxicity of coumarin: a comparison of rat and Mongolian gerbil. Toxicology 1992, 71:129-136.
13. Fentem J.H., Fry J.R. Species differences in the metabolism and hepatotoxicity of coumarin. Comp. Biochem. Physiol. 1993, 104:1-8.
14. Gatley S.J., Sherratt S.A. The effects of diphenyleneiodonium on mitochondrial reactions. Relation of binding of diphenylene[125I]iodonium to mitochondria to the extent of inhibition of oxygen uptake. Biochem. J. 1976, 158:307-315.
15. Grasso P., Wright M.G., Gangolli S.D., Hendy R.J. Liver response tests. IX. Cytopathological changes in the enlarged but histologically normal rat liver. Food Cosmet. Toxicol. 1974, 12:341-350.
16. Ikonen E., Fiedler K., Parton R.G., Simons K. Prohibitin, an antiproliferative protein, is localized to mitochondria. FEBS Lett. 1995, 358:273-277.
17. Kienhuis A.S., Wortelboer H.M., Hoflack J.C., Moonen E.J., Kleinjans J.C., van Ommen B., van Delft J.H., Stierum R.H. Comparison of coumarin-induced toxicity between sandwich-cultured primary rat hepatocytes and rats in vivo: a toxicogenomics approach. Drug Metab. Dispos. 2006, 34:2083-2090.
18. Kienhuis A.S., van de Poll M.C., Dejong C.H., Gottschalk R., van Herwijnen M., Boorsma A., Kleinjans J.C., Stierum R.H., van Delft J.H. A toxicogenomics-based parallelogram approach to evaluate the relevance of coumarin-induced responses in primary human hepatocytes in vitro for humans in vivo. Toxicol. Vitro 2009, 23:1163-1169.
19. Knockaert L., Descatoire V., Vadrot N., Fromenty B., Robin M.A. Mitochondrial CYP2E1 is sufficient to mediate oxidative stress and cytotoxicity induced by ethanol and acetaminophen. Toxicol. Vitro 2011, 25:475-484.
20. Knockaert L., Fromenty B., Robin M.A. Mechanisms of mitochondrial targeting of cytochrome P450 2E1: physiopathological role in liver injury and obesity. FEBS J. 2011, 278:4252-4260.
21. Lake B.G. Investigations into the mechanism of coumarin-induced hepatotoxicity in the rat. Arch. Toxicol. Suppl. 1984, 7:16-29.
22. Lake B.G., Gray T.J., Evans J.G., Lewis D.F., Beamand J.A., Hue K.L. Studies on the mechanism of coumarin-induced toxicity in rat hepatocytes: comparison with dihydrocoumarin and other coumarin metabolites. Toxicol. Appl. Pharmacol. 1989, 97:311-323.
23. Lake B.G., Evans J.G., Lewis D.F., Price R.J. Studies on the acute effects of coumarin and some coumarin derivatives in the rat. Food Chem. Toxicol. 1994, 32:357-363.
24. Lake B.G., Grasso P. Comparison of the hepatotoxicity of coumarin in the rat, mouse, and Syrian hamster: a dose and time response study. Fundam. Appl. Toxicol. 1996, 34:105-117.
25. Lake B.G., Evans J.G., Chapuis F., Walters D.G., Price R.J. Studies on the disposition, metabolism and hepatotoxicity of coumarin in the rat and Syrian hamster. Food Chem. Toxicol. 2002, 40:809-823.
26. Masubuchi Y., Suda C., Horie T. Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice. J. Hepatol. 2005, 42:110-116.
27. McClung J.K., Jupe E.R., Liu X.T., Dell'Orco R.T. Prohibitin: potential role in senescence, development, and tumor suppression. Exp. Gerontol. 1995, 30:99-124.
28. Meyer J.N., Leung M.C., Rooney J.P., Sendoel A., Hengartner M.O., Kisby G.E., Bess A.S. Mitochondria as a target of environmental toxicants. Toxicol. Sci. 2013, 134:1-17.
29. Pessayre D., Mansouri A., Haouzi D., Fromenty B. Hepatotoxicity due to mitochondrial dysfunction. Cell Biol. Toxicol. 1999, 15:367-373.
30. Pessayre D., Fromenty B., Berson A., Robin M.A., Lettéron P., Moreau R., Mansouri A. Central role of mitochondria in drug-induced liver injury. Drug Metab. Rev. 2012, 44:34-87.
31. Raza H., Prabu S.K., Robin M.A., Avadhani N.G. Elevated mitochondrial cytochrome P450 2E1 and glutathione S-transferase A4-4 in streptozotocin-induced diabetic rats: tissue-specific variations and roles in oxidative stress. Diabetes 2004, 53:185-194.
32. Robin M.A., Anandatheerthavarada H.K., Fang J.K., Cudic M., Otvos L., Avadhani N.G. Mitochondrial targeted cytochrome P450 2E1 (P450 MT5) contains an intact N-terminus and requires mitochondrial specific electron transfer proteins for activity. J. Biol. Chem. 2001, 276:24680-24689.
33. Robin M.A., Anandatheerthavarada H.K., Biswas G., Sepuri N.B.V., Gordon D.M., Pain D., Avadhani N.G. Bimodal targeting of microsomal CYP2E1 to mitochondria through activation of an N-terminal chimeric signal by cAMP-mediated phosphorylation. J. Biol. Chem. 2002, 277:40583-40593.
34. Robin M.A., Sauvage I., Grandperret T., Descatoire V., Pessayre D., Fromenty B. Ethanol increases mitochondrial cytochrome P450 2E1 in mouse liver and rat hepatocytes. FEBS Lett. 2005, 579:6895-6902.
35. Roos N., Benz R., Brdiczka D. Identification and characterization of the pore-forming protein in the outer membrane of rat liver mitochondria. Biochim. Biophys. Acta 1982, 686:204-214.
36. Sano T., Ozaki K., Matsuura T., Narama I. Giant mitochondria in pancreatic acinar cells of alloxan-induced diabetic rats. Toxicol. Pathol. 2010, 38:658-665.
37. Serviddio G., Bellanti F., Giudetti A.M., Gnoni G.V., Capitanio N., Tamborra R., Romano A.D., Quinto M., Blonda M., Vendemiale G., Altomare E. Mitochondrial oxidative stress and respiratory chain dysfunction account for liver toxicity during amiodarone but not dronedarone administration. Free Radic. Biol. Med. 2011, 51:2234-2242.
38. Toyosawa K., Koujitani T., Matsumoto I., Mikami S., Kouchi M., Michimae Y., Inoue T., Seki T. Application of Prohibitin immunohistochemistry to rat livers treated with methapyrilene hydrochloride. J. Toxicol. Pathol. 2008, 21:119-122.
39. Vassallo J.D., Hicks S.M., Daston G.P., Lehman-McKeeman L.D. Metabolic detoxification determines species differences in coumarin-induced hepatotoxicity. Toxicol. Sci. 2004, 80:249-257.
40. Wang Y.H., Avula B., Nanayakkara N.P., Zhao J., Khan I.A. Cassia cinnamon as a source of coumarin in cinnamon-flavored food and food supplements in the United States. J. Agric. Food Chem. 2013, 61:4470-4476.