Involvement of breast cancer resistance protein (BCRP/ABCG2) in the biliary excretion and intestinal efflux of troglitazone sulfate, the major metabolite of troglitazone with a cholestatic effect

Drug Metabolism and Disposition

Volumn 35, Issue 2, 2007, Pages 209-214

  Enokizono, Junichi ^a   Kusuhara, Hiroyuki ^a   Sugiyama, Yuichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; COMPLEMENTARY DNA; DRUG METABOLITE; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 1B1; TROGLITAZONE; TROGLITAZONE SULFATE; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILIARY EXCRETION; CHOLESTASIS; CONTINUOUS INFUSION; CONTROLLED STUDY; DRUG BILE LEVEL; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DISPOSITION; DRUG EFFECT; DRUG EXCRETION; DRUG LIVER LEVEL; DRUG TRANSPORT; INTESTINE ABSORPTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS RECOMBINANT;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BILE; CHOLESTASIS; CHROMANS; HUMANS; HYPOGLYCEMIC AGENTS; INTESTINAL MUCOSA; LIVER; MALE; MICE; NEOPLASM PROTEINS; ORGANIC ANION TRANSPORTERS; THIAZOLIDINEDIONES;

ADENOVIRIDAE; MUS;

EID: 33846424578     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.106.012567     Document Type: Article

References (42)

1. Adachi Y, Suzuki H, Schinkel AH, and Sugiyama Y (2005) Role of breast cancer resistance protein (Bcrp1/Abcg2) in the extrusion of glucuronide and sulfate conjugates from enterocytes to intestinal lumen. Mol Pharmacol 67:923-928.
2. Akimoto K, Sano N, and Takikawa H (2001) Biliary excretion of tauroursodeoxycholate-3-sulfate in the rat. Steroids 66:701-705.
3. Chen C (1998) Troglitazone: an antidiabetic agent. Am J Health Syst Pharm 55:905-925.
4. Fukano M, Amano S, Sato J, Yamamoto K, Adachi H, Okabe H, Fujiyama Y, and Bamba T (2000) Subacute hepatic failure associated with a new antidiabetic agent, troglitazone: a case report with autopsy examination. Hum Pathol 31:250-253.
5. Funk C, Pantze M, Jehle L, Ponelle C, Scheuermann G, Lazendic M, and Gasser R (2001a) Troglitazone-induced intrahepatic cholestasis by an interference with the hepatobiliary export of bile acids in male and female rats. Correlation with the gender difference in troglitazone sulfate formation and the inhibition of the canalicular bile salt export pump (Bsep) by troglitazone and troglitazone sulfate. Toxicology 167:83-98.
6. Funk C, Ponelle C, Scheuermann G, and Pantze M (2001b) 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.
7. Hirano M, Maeda K, Matsushima S, Nozaki Y, Kusuhara H, and Sugiyama Y (2005) Involvement of BCRP (ABCG2) in the biliary excretion of pitavastatin. Mol Pharmacol 68:800-807.
8. Honma W, Shimada M, Sasano H, Ozawa S, Miyata M, Nagata K, Ikeda T, and Yamazoe Y (2002) Phenol sulfotransferase, ST1A3, as the main enzyme catalyzing sulfation of troglitazone in human liver. Drug Metab Dispos 30:944-949.
9. Imai Y, Nakane M, Kage K, Tsukahara S, Ishikawa E, Tsuruo T, Miki Y, and Sugimoto Y (2002) C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance. Mol Cancer Ther 1:611-616.
10. Jonker JW, Buitelaar M, Wagenaar E, Van Der Valk MA, Scheffer GL, Scheper RJ, Plosch T, Kuipers F, Elferink RP, Rosing H, et al. (2002) The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci USA 99:15649-15654.
11. Jonker JW, Merino G, Musters S, van Herwaarden AE, Bolscher E, Wagenaar E, Mesman E, Dale TC, and Schinkel AH (2005) The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 11:127-129.
12. Kawai K, Hirota T, Muramatsu S, Tsuruta F, Ikeda T, Kobashi K, and Nakamura KI (2000) Intestinal absorption and excretion of troglitazone sulphate, a major biliary metabolite of troglitazone. Xenobiotica 30:707-715.
13. Kawai K, Kawasaki-Tokui Y, Odaka T, Tsuruta F, Kazui M, Iwabuchi H, Nakamura T, Kinoshita T, Ikeda T, Yoshioka T, et al. (1997) Disposition and metabolism of the new oral antidiabetic drug troglitazone in rats, mice and dogs. Arzneimittelforschung 47:356-368.
14. Kobayashi D, Ieiri I, Hirota T, Takane H, Maegawa S, Kigawa J, Suzuki H, Nanba E, Oshimura M, Terakawa N, et al. (2005) Functional assessment of ABCG2 (BCRP) gene polymorphisms to protein expression in human placenta. Drug Metab Dispos 33:94-101.
15. Kondo C, Onuki R, Kusuhara H, Suzuki H, Suzuki M, Okudaira N, Kojima M, Ishiwata K, Jonker JW, and Sugiyama Y (2005) Lack of improvement of oral absorption of ME3277 by prodrug formation is ascribed to the intestinal efflux mediated by breast cancer resistant protein (BCRP/ABCG2). Pharm Res (NY) 22:613-618.
16. Kondo C, Suzuki H, Itoda M, Ozawa S, Sawada J, Kobayashi D, Ieiri I, Mine K, Ohtsubo K, and Sugiyama Y (2004) Functional analysis of SNPs variants of BCRP/ABCG2. Pharm Res (NY) 21:1895-1903.
17. Kostrubsky VE, Vore M, Kindt E, Burliegh J, Rogers K, Peter G, Altrogge D, and Sinz MW (2001) The effect of troglitazone biliary excretion on metabolite distribution and cholestasis in transporter-deficient rats. Drug Metab Dispos 29:1561-1566.
18. Maeda K, Ieiri I, Yasuda K, Fujino A, Fujiwara H, Otsubo K, Hirano M, Watanabe T, Kitamura Y, Kusuhara H, et al. (2006) Effects of organic anion transporting polypeptide 1B1 haplotype on pharmacokinetics of pravastatin, valsartan, and temocapril. Clin Pharmacol Ther 79:427-439.
19. Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, and Schellens JH (2001) Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 61:3458-3464.
20. Matsushima S, Maeda K, Kondo C, Hirano M, Sasaki M, Suzuki H, and Sugiyama Y (2005) Identification of the Hepatic efflux transporters of organic anions using double-transfected madin-darby canine kidney II cells expressing human organic anion-transporting polypeptide 1B1 (OATP1B1)/multidrug resistance-associated protein 2, OATP1B1/multidrug resistance 1, and OATP1B1/breast cancer resistance protein. J Pharmacol Exp Ther 314:1059-1067.
21. Menon KVN, Angulo P, and Lindor KD (2001) Severe cholestatic hepatitis from troglitazone in a patient with nonalcoholic steatohepatitis and diabetes mellitus. Am J Gastroenterol 96:1631-1634.
22. Merino G, Jonker JW, Wagenaar E, van Herwaarden AE, and Schinkel AH (2005) The breast cancer resistance protein (BCRP/ABCG2) affects pharmacokinetics, hepatobiliary excretion, and milk secretion of the antibiotic nitrofurantoin. Mol Pharmacol 67:1758-1764.
23. Mizuno N, Suzuki M, Kusuhara H, Suzuki H, Takeuchi K, Niwa T, Jonker JW, and Sugiyama Y (2004) Impaired renal excretion of 6-hydroxy-5,7-dimethyl-2- methylamino-4-(3-pyridylmethyl) benzothiazole (E3040) sulfate in breast cancer resistance protein (BCRP1/ABCG2) knockout mice. Drug Metab Dispos 32:898-901.
24. Mwinyi J, Johne A, Bauer S, Roots I, and Gerloff T (2004) Evidence for inverse effects of OATP-C (SLC21A6) 5 and 1b haplotypes on pravastatin kinetics. Clin Pharmacol Ther 75:415-421.
25. Nishizato Y, Ieiri I, Suzuki H, Kimura M, Kawabata K, Hirota T, Takane H, Irie S, Kusuhara H, Urasaki Y, et al. (2003) Polymorphisms of OATP-C (SLC21A6) and OAT3 (SLC22A8) genes: consequences for pravastatin pharmacokinetics. Clin Pharmacol Ther 73:554-565.
26. Nowell S, Sweeney C, Winters M, Stone A, Lang NP, Hutchins LF, Kadlubar FF, and Ambrosone CB (2002) Association between sulfotransferase 1A1 genotype and survival of breast cancer patients receiving tamoxifen therapy. J Natl Cancer Inst 94:1635-1640.
27. Nozawa T, Sugiura S, Nakajima M, Goto A, Yokoi T, Nezu J, Tsuji A, and Tamai I (2004) Involvement of organic anion transporting polypeptides in the transport of troglitazone sulfate: implications for understanding troglitazone hepatotoxicity. Drug Metab Dispos 32:291-294.
28. Ott P, Ranek L, and Young MA (1998) Pharmacokinetics of troglitazone, a PPAR-gamma agonist, in patients with hepatic insufficiency. Eur J Clin Pharmacol 54:567-571.
29. Raftogianis RB, Wood TC, Otterness DM, Van Loon JA, and Weinshilboum RM (1997) Phenol sulfotransferase pharmacogenetics in humans: association of common SULT1A1 alleles with TS PST phenotype. Biochem Biophys Res Commun 239:298-304.
30. Smith MT (2003) Mechanisms of troglitazone hepatotoxicity. Chem Res Toxicol 16:679-687.
31. Sparreboom A, Gelderblom H, Marsh S, Ahluwalia R, Obach R, Principe P, Twelves C, Verweij J, and McLeod HL (2004) Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype. Clin Pharmacol Ther 76:38-44.
32. Sparreboom A, Loos WJ, Burger H, Sissung TM, Verweij J, Figg WD, Nooter K, and Gelderblom H (2005) Effect of ABCG2 genotype on the oral bioavailability of topotecan. Cancer Biol Ther 4:650-658.
33. Suzuki M, Suzuki H, Sugimoto Y, and Sugiyama Y (2003) ABCG2 transports sulfated conjugates of steroids and xenobiotics. J Biol Chem 278:22644-22649.
34. Takikawa H, Sano N, Narita T, Uchida Y, Yamanaka M, Horie T, Mikami T, and Tagaya O (1991) Biliary excretion of bile acid conjugates in a hyperbilirubinemic mutant Sprague-Dawley rat. Hepatology 14:352-360.
35. Tanaka H, Sano N, and Takikawa H (2003) Biliary excretion of phenolphthalein sulfate in rats. Pharmacology 68:177-182.
36. van Herwaarden AE, Jonker JW, Wagenaar E, Brinkhuis RF, Schellens JH, Beijnen JH, and Schinkel AH (2003) The breast cancer resistance protein (Bcrp1/Abcg2) restricts exposure to the dietary carcinogen 2-amino-1-methyl-6- phenylimidazo[4,5-b]pyridine. Cancer Res 63:6447-6452.
37. Wang DQ, Paigen B, and Carey MC (2001) Genetic factors at the enterocyte level account for variations in intestinal cholesterol absorption efficiency among inbred stains of mice. J Lipid Res 42:1820-1830.
38. Wegman P, Vainikka L, Stal O, Nordenskjold B, Skoog L, Rutqvist LE, and Wingren S (2005) Genotype of metabolic enzymes and the benefit of tamoxifen in postmenopausal breast cancer patients. Breast Cancer Res 7:R284-R290.
39. Werner A, Minich DM, Havinga R, Bloks V, Van Goor H, Kulipers F, and Verkade HJ (2002) Fat malabsorption in essential fatty acid-deficient mice is not due to impaired bile formation. Am J Physiol 283:G900-G908.
40. Zamek-Gliszczynski MJ, Hoffmaster KA, Tian X, Zhao R, Polli JW, Humphreys JE, Webster LO, Bridges AS, Kalvass JC, and Brouwer KL (2005) Multiple mechanisms are involved in the biliary excretion of acetaminophen sulfate in the rat: role of Mrp2 and Bcrp1. Drug Metab Dispos 33:1158-1165.
41. Zamek-Gliszcynski MJ, Nezasa K, Tian X, Kalvass JC, Patel NJ, Raub TJ, and Brouwer KL (2006) The important role of Bcrp (Abcg2) in the biliary excretion of sulfate and glucuronide metabolites of acetaminophen, 4-methylumbelliferone, and harmol in mice. Mol Pharmacol 70:2127-2133.
42. Zhang W, Yu BN, He YJ, Fan L, Li Q, Liu ZQ, Wang A, Liu YL, Tan ZR, Fen J, et al. (2006) Role of BCRP 421C>A polymorphism on rosuvastatin pharmacokinetics in healthy Chinese males. Clin Chim Acta 373:99-103.