Itraconazole-induced cholestasis: Involvement of the inhibition of bile canalicular phospholipid translocator MDR3/ABCB4

Molecular Pharmacology

Volumn 79, Issue 2, 2011, Pages 241-250

  Yoshikado, Takashi ^a,b   Takada, Tappei ^a   Yamamoto, Takehito ^a   Yamaji, Hiroko ^a   Ito, Kousei ^a   Santa, Tomofumi ^b   Yokota, Hiromitsu ^a   Yatomi, Yutaka ^a   Yoshida, Haruhiko ^a   Goto, Jun ^a   Tsuji, Shoji ^a   Suzuki, Hiroshi ^a  

^a UNIVERSITY OF TOKYO HOSPITAL   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BILE ACID; GLYCOPROTEIN P; ITRACONAZOLE; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID; PHOSPHOLIPID TRANSFER PROTEIN; PROTEIN BSEP; PROTEIN MDR3; TAUROCHOLIC ACID; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE SECRETION; CASE REPORT; CHOLESTASIS; DRUG BLOOD LEVEL; DRUG WITHDRAWAL; FEMALE; HUMAN; IN VIVO STUDY; LIVER FUNCTION TEST; LIVER INJURY; MALE; MICELLE; NONHUMAN; PRIORITY JOURNAL; RAT; SIDE EFFECT;

ANIMALS; ANTIFUNGAL AGENTS; BILE CANALICULI; BLOTTING, WESTERN; CHOLESTASIS; ITRACONAZOLE; LLC-PK1 CELLS; MALE; P-GLYCOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 78751555741     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.067256     Document Type: Article

References (41)

1. Adriaenssens B, Roskams T, Steger P, and Van Steenbergen W (2001) Hepatotoxicity related to itraconazole: report of three cases. Acta Clin Belg 56:364-369. (Pubitemid 34123364)
2. Alfirevic A, Mills T, Carr D, Barratt BJ, Jawaid A, Sherwood J, Smith JC, Tugwood J, Hartkoorn R, Owen A, et al. (2007) Tacrine-induced liver damage: an analysis of 19 candidate genes. Pharmacogenet Genomics 17:1091-1100.
3. Bode KA, Donner MG, Leier I, and Keppler D (2002) Inhibition of transport across the hepatocyte canalicular membrane by the antibiotic fusidate. Biochem Pharmacol 64:151-158.
4. + bile acid cotransport system in COS-7 cells. Am J Physiol 266:G382-G387.
5. Byrne JA, Strautnieks SS, Mieli-Vergani G, Higgins CF, Linton KJ, and Thompson RJ (2002) The human bile salt export pump: characterization of substrate specificity and identification of inhibitors. Gastroenterology 123:1649-1658.
6. Fattinger K, Funk C, Pantze M, Weber C, Reichen J, Stieger B, and Meier PJ (2001) The endothelin antagonist bosentan inhibits the canalicular bile salt export pump: a potential mechanism for hepatic adverse reactions. Clin Pharmacol Ther 69:223-231. (Pubitemid 32382504)
7. Fouassier L, Kinnman N, Lefèvre G, Lasnier E, Rey C, Poupon R, Elferink RP, and Housset C (2002) Contribution of mrp2 in alterations of canalicular bile formation by the endothelin antagonist bosentan. J Hepatol 37:184-191.
8. Funk C, Ponelle C, Scheuermann G, and Pantze M (2001) Cholestatic potential of troglitazone as a possible factor contributing to troglitazone-induced hepatotoxicity: in vivo and in vitro interaction at the canalicular bile salt export pump (Bsep) in the rat. Mol Pharmacol 59:627-635. (Pubitemid 32179943)
9. Gallardo-Quesada S, Luelmo-Aguilar J, and Guanyabens-Calvet C (1995) Hepatotoxicity associated with itraconazole. Int J Dermatol 34:589.
10. Gerloff T, Stieger B, Hagenbuch B, Madon J, Landmann L, Roth J, Hofmann AF, and Meier PJ (1998) The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273:10046-10050.
11. Gunawan BK and Kaplowitz N (2007) Mechanisms of drug-induced liver disease. Clin Liver Dis 11:459-475.
12. Gupta S, Kim J, and Gollapudi S (1991) Reversal of daunorubicin resistance in P388/ADR cells by itraconazole. J Clin Invest 87:1467-1469.
13. Hann SK, Kim JB, Im S, Han KH, and Park YK (1993) Itraconazole-induced acute hepatitis. Br J Dermatol 129:500-501.
14. Horikawa M, Kato Y, Tyson CA, and Sugiyama Y (2003) Potential cholestatic activity of various therapeutic agents assessed by bile canalicular membrane vesicles isolated from rats and humans. Drug Metab Pharmacokinet 18:16-22.
15. Iida N, Takara K, Ohmoto N, Nakamura T, Kimura T, Wada A, Hirai M, Sakaeda T, and Okumura K (2001) Reversal effects of antifungal drugs on multidrug resistance in MDR1-overexpressing HeLa cells. Biol Pharm Bull 24:1032-1036.
16. Ikebuchi Y, Takada T, Ito K, Yoshikado T, Anzai N, Kanai Y, and Suzuki H (2009) Receptor for activated C-kinase 1 regulates the cellular localization and function of ABCB4. Hepatol Res 39:1091-1107.
17. 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.
18. Lavrijsen AP, Balmus KJ, Nugteren-Huying WM, Roldaan AC, van't Wout JW, and Stricker BH (1992) Hepatic injury associated with itraconazole. Lancet 340:251-252.
19. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275.
20. +/taurocholate cotransporting polypeptide (SLC10A1) and bile salt export pump (ABCB 11)-coexpressing LLCPK1 cells by cholestasis-inducing drugs. Drug Metab Dispos 34:1575-1581.
21. +-taurocholate cotransporting polypeptide and rat bile salt export pump. Am J Physiol Gastrointest Liver Physiol 288:G159-G167.
22. Morita SY, Kobayashi A, Takanezawa Y, Kioka N, Handa T, Arai H, Matsuo M, and Ueda K (2007) Bile salt-dependent efflux of cellular phospholipids mediated by ATP binding cassette protein B4. Hepatology 46:188-199.
23. Nivoix Y, Levêque D, Herbrecht R, Koffel JC, Beretz L, and Ubeaud-Sequier G (2008) The enzymatic basis of drug-drug interactions with systemic triazole antifungals. Clin Pharmacokinet 47:779-792.
24. Noé J, Stieger B, and Meier PJ (2002) Functional expression of the canalicular bile salt export pump of human liver. Gastroenterology 123:1659-1666. (Pubitemid 35231665)
25. Oude Elferink RP and Paulusma CC (2007) Function and pathophysiological importance of ABCB4 (MDR3 P-glycoprotein). Pflugers Arch 453:601-610.
26. Oude Elferink RP, Paulusma CC, and Groen AK (2006) Hepatocanalicular transport defects: pathophysiologic mechanisms of rare diseases. Gastroenterology 130:908-925.
27. Smit JJ, Schinkel AH, Oude Elferink RP, Groen AK, Wagenaar E, van Deemter L, Mol CA, Ottenhoff R, van der Lugt NM, and van Roon MA (1993) Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease. Cell 75:451-462.
28. Smith AJ, Timmermans-Hereijgers JL, Roelofsen B, Wirtz KW, van Blitterswijk WJ, Smit JJ, Schinkel AH, and Borst P (1994) The human MDR3 P-glycoprotein promotes translocation of phosphatidylcholine through the plasma membrane of fibroblasts from transgenic mice. FEBS Lett 354:263-266.
29. Smith AJ, van Helvoort A, van Meer G, Szabo K, Welker E, Szakacs G, Varadi A, Sarkadi B, and Borst P (2000) MDR3 P-glycoprotein, a phosphatidylcholine translocase, transports several cytotoxic drugs and directly interacts with drugs as judged by interference with nucleotide trapping. J Biol Chem 275:23530-23539.
30. Somchit N, Norshahida AR, Hasiah AH, Zuraini A, Sulaiman MR, and Noordin MM (2004) Hepatotoxicity induced by antifungal drugs itraconazole and fluconazole in rats: a comparative in vivo study. Hum Exp Toxicol 23:519-525. (Pubitemid 39627221)
31. Song JC and Deresinski S (2005) Hepatotoxicity of antifungal agents. Curr Opin Investig Drugs 6:170-177.
32. Srebrnik A, Levtov S, Ben-Ami R, and Brenner S (2005) Liver failure and transplantation after itraconazole treatment for toenail onychomycosis. J Eur Acad Dermatol Venereol 19:205-207. (Pubitemid 40450426)
33. Stieger B, Fattinger K, Madon J, Kullak-Ublick GA, and Meier PJ (2000) Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118:422-430. (Pubitemid 30067515)
34. Takara K, Tanigawara Y, Komada F, Nishiguchi K, Sakaeda T, and Okumura K (1999) Cellular pharmacokinetic aspects of reversal effect of itraconazole on P-glycoprotein-mediated resistance of anticancer drugs. Biol Pharm Bull 22:1355-1359.
35. Vallejo M, Briz O, Serrano MA, Monte MJ, and Marin JJ (2006) Potential role of trans-inhibition of the bile salt export pump by progesterone metabolites in the etiopathogenesis of intrahepatic cholestasis of pregnancy. J Hepatol 44:1150-1157.
36. van Helvoort A, Smith AJ, Sprong H, Fritzsche I, Schinkel AH, Borst P, and van Meer G (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell 87:507-517.
37. Wagner H, Hoerhammer L, and Wolff P (1961) [Thin layer chromatography of phosphatides and glycolipids.]. Biochem Z 334:175-184.
38. Wang EJ, Casciano CN, Clement RP, and Johnson WW (2003) Fluorescent substrates of sister-P-glycoprotein (BSEP) evaluated as markers of active transport and inhibition: evidence for contingent unequal binding sites. Pharm Res 20:537-544.
39. Wang R, Salem M, Yousef IM, Tuchweber B, Lam P, Childs SJ, Helgason CD, Ackerley C, Phillips MJ, and Ling V (2001) Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive but persistent intrahepatic cholestasis. Proc Natl Acad Sci USA 98:2011-2016.
40. Yamaguchi H, Enomoto S, Kaku M, Sakamaki H, Tanaka K, and Yoshida M (2006) An open randomized parallel-comparison study of itraconazole oral solution versus itraconazole capsules in treatment of patients with oropharyngeal candidiasis. Jpn J Chemother 54:18-31.
41. Yamano K, Yamamoto K, Kotaki H, Sawada Y, and Iga T (1999) Quantitative prediction of metabolic inhibition of midazolam by itraconazole and ketoconazole in rats: implication of concentrative uptake of inhibitors into liver. Drug Metab Dispos 27:395-402.