Role of the bile salt export pump, BSEP, in acquired forms of cholestasis

References

• Adachi, Y., Kobayashi, H., Kurumi, Y., Shouji, M., Kitano, M., Yamamoto, T. (1991). ATP-dependent taurocholate transport by rat liver canalicular membrane vesicles. Hepatology 14:655–659.
   PubMed Web of Science ®Google Scholar
• Akita, H., Suzuki, H., Ito, K., Kinoshita, S., Sato, N., Takikawa, H., et al. (2001). Characterization of bile acid transport mediated by multidrug resistance–associated protein 2 and bile salt export pump. Biochim Biophys Acta 1511:7–16.
   PubMed Web of Science ®Google Scholar
• Alrefai, W.A., Gill, R. K. (2007). Bile acid transporters: structure, function, regulation, and pathophysiological implications. Pharm Res 24:1803–1823.
   PubMed Web of Science ®Google Scholar
• Ballatori, N., Li, N., Fang, F., Boyer, J. L., Christian, W.V., Hammond, C. L. (2009). OST alpha-OST beta: a key membrane transporter of bile acids and conjugated steroids. Front Biosci 14:2829–2844.
   PubMed Web of Science ®Google Scholar
• Bleibel, W., Kim, S., D’Silva, K., Lemmer, E. R. (2007.) Drug-induced liver injury: review article. Dig Dis Sci 52:2463–2471.
   PubMed Web of Science ®Google Scholar
• Bode, K. A., Donner, M. G., Leier, I., Keppler, D. (2002). Inhibition of transport across the hepatocyte canalicular membrane by the antibiotic fusidate. Biochem Pharmacol 64:151–158.
   PubMed Web of Science ®Google Scholar
• Bohme, M., Muller, M., Leier, I., Jedlitschky, G., Keppler, D. (1994). Cholestasis caused by inhibition of the adenosine triphosphate-dependent bile salt transport in rat liver. Gastroenterology 107:255–265.
   PubMed Web of Science ®Google Scholar
• Byrne, J. A., Strautnieks, S. S., Ihrke, G., Pagani, F., Knisely, A. S., Linton, K. J., et al. (2009). Missense mutations and single-nucleotide polymorphisms in ABCB11 impair bile salt export pump processing and function or disrupt premessenger RNA splicing. Hepatology 49:352–354.
   PubMedGoogle Scholar
• Byrne, J. A., Strautnieks, S. S., Mieli-Vergani, G., Higgins, C. F., Linton, K. J., Thompson, RJ. (2002). The human bile salt export pump: characterization of substrate specificity and identification of inhibitors. Gastroenterology 123:1649–1658.
   PubMed Web of Science ®Google Scholar
• Carlton, V. E., Harris, B. Z., Puffenberger, E. G., Batta, A. K., Knisely, A. S., Robinson, D. L., et al. (2003). Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT. Nat Genet 34:91–96.
   PubMed Web of Science ®Google Scholar
• Dawson, P. A., Lan, T., Rao, A. (2009). Bile acid transporters. J Lipid Res 50:2340–2357.
   PubMed Web of Science ®Google Scholar
• Dixon, PH, van Mil, S, Chambers, J, Strautnieks, S, Thompson, R, Lammert, F, et al. (2009). Contribution of variant alleles of ABCB11 to susceptibility to intrahepatic cholestasis of pregnancy. Gut 58:537–544.
   PubMed Web of Science ®Google Scholar
• Fattinger, K., Funk, C., Pantze, M., Weber, C., Reichen, J., Stieger, B., et al. (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.
   PubMed Web of Science ®Google Scholar
• Fouassier, L., Kinnman, N., Lefevre, G., Lasnier, E., Rey, C., Poupon, R., et al. (2002). Contribution of mrp2 in alterations of canalicular bile formation by the endothelin antagonist bosentan. J Hepatol 37:184–191.
   PubMed Web of Science ®Google Scholar
• Funk, C. (2008). The role of hepatic transporters in drug elimination. Exp Opin Drug Metab Toxicology 4:363–379.
   PubMed Web of Science ®Google Scholar
• Funk, C., Ponelle, C., Scheuermann, G., 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.
   PubMed Web of Science ®Google Scholar
• Geier, A., Wagner, M., Dietrich, C.G., Trauner, M. (2007). Principles of hepatic organic anion transporter regulation during cholestasis, inflammation and liver regerenation. Biochim Biophys Acta 1773:283–308.
   PubMed Web of Science ®Google Scholar
• Gerloff, T., Stieger, B., Hagenbuch, B., Madon, J., Landmann, L., Roth, J., et al. (1998). The sister of P-glycoprotein represents the canalicular bile salt export pump of mammalian liver. J Biol Chem 273:10046–10050.
   PubMed Web of Science ®Google Scholar
• Green, R. M., Hoda, F., Ward, K. L. (2000). Molecular cloning and characterization of the murine bile salt export pump. Gene 241:117–123.
   PubMed Web of Science ®Google Scholar
• Hayashi, H., Takada, T., Suzuki, H., Onuki, R., Hofmann, A. F., Sugiyama, Y. (2005). Transport by vesicles of glycine- and taurine-conjugated bile salts and taurolithocholate 3-sulfate: a comparison of human BSEP with rat Bsep. Biochim Biophys Acta 1738:54–62.
   PubMed Web of Science ®Google Scholar
• Hirano, M., Maeda, K., Hayashi, H., Kusuhara, H., Sugiyama, Y. (2005). Bile salt export pump (BSEP/ABCB11) can transport a nonbile acid substrate, pravastatin. J. Pharmacol Exp Ther 314:876–882.
   PubMed Web of Science ®Google Scholar
• Hirano, H., Kurata, A., Onishi, Y., Sakurai, A., Saito, H., Nakagawa, H., et al. (2006). High-speed screening and QSAR analysis of human ATP-binding cassette transporter ABCB11 (bile salt export pump) to predict drug-induced intrahepatic cholestasis. Mol Pharm 3:252–265.
   PubMed Web of Science ®Google Scholar
• Hofmann, A. F. (2009). Bile acids: trying to understand their chemistry and biology with the hope of helping patients. Hepatology 49:1403–1418.
   PubMed Web of Science ®Google Scholar
• Hofmann, A. F., Hagey, L. R. (2008). Bile acids: chemistry, pathochemistry, biology, pathobiology, and therapeutics. Cell Mol Life Sci 65:2461–2483.
   PubMed Web of Science ®Google Scholar
• Horikawa, M., Kato, Y., Tyson, C. A., 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.
   PubMedGoogle Scholar
• Huang, L., Smit, J. W., Meijer, D. K., Vore, M. (2000). Mrp2 is essential for estradiol-17beta(beta-D-glucuronide)-induced cholestasis in rats. Hepatology 32:66–72.
   PubMed Web of Science ®Google Scholar
• Jansen, P. L. M., Strautnieks, S. S., Jacquemin, E., Hadchouel, M., Sokal, E. M., Hooiveld, G. J., et al. (1999). Hepatocanalicular bile salt export pump deficiency in patients with progressive familial intrahepatic cholestasis. Gastroenterology 117:1370–1379.
   PubMed Web of Science ®Google Scholar
• Julie, N. L., Julie, I. M., Kende, A. I., Wilson, G. L. (2008). Mitochondrial dysfunction and delayed hepatotoxicity: another lesson from troglitazone. Diabetologia 51:2108–2116.
   PubMed Web of Science ®Google Scholar
• Keitel, V., Vogt, C., Haussinger, D., Kubitz, R. (2006). Combined mutations of canalicular transporter proteins cause severe intrahepatic cholestasis of pregnancy. Gastroenterology 131:624–629.
   PubMed Web of Science ®Google Scholar
• Kis, E., Ioja, E., Nagy, T., Szente, L., Heredi-Szabo, K., Krajcsi, P. (2009). Effect of membrane cholesterol on BSEP/Bsep activity: species specificity studies for substrates and inhibitors. Drug Metab Dispos 37:1878–1886. [Epub Jun 11].
   PubMed Web of Science ®Google Scholar
• Knisely, A. S., Strautnieks, S. S., Meier, Y., Stieger, B., Byrne, J. A., Portmann, B. C., et al. (2006). Hepatocellular carcinoma in 10 children under 5 years of age with bile salt export pump deficiency. Hepatology 44:478–486.
   PubMed Web of Science ®Google Scholar
• Kosters, A., Karpen, S. J. (2008). Bile acid transporters in health and disease. Xenobiotica 38:1043–1071.
   PubMed Web of Science ®Google Scholar
• Kostrubsky, S. E., Strom, S. C., Kalgutkar, A. S., Kulkarni, S., Atherton, J., Mireles, R., et al. (2006). Inhibition of hepatobiliary transport as a predictive method for clinical hepatotoxicity of nefazodone. Toxicol Sci 90:451–459.
   PubMed Web of Science ®Google Scholar
• Kostrubsky, V. E., Strom, S. C., Hanson, J., Urda, E., Rose, K., Burliegh, J., et al. (2003). Evaluation of hepatotoxic potential of drugs by inhibition of bile-acid transport in cultured primary human hepatocytes and intact rats. Toxicol Sci 76:220–228.
   PubMed Web of Science ®Google Scholar
• Krahenbuhl, S., Talos, C., Fischer, S., Reichen, J. (1994). Toxicity of bile acids on the electron transport chain of isolated rat liver mitochondria. Hepatology 19:471–479.
   PubMed Web of Science ®Google Scholar
• Kullak-Ublick, G.A., Stieger, B., Meier, P.J. (2004). Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 126:322–342.
   PubMed Web of Science ®Google Scholar
• Kubitz, R., Keitel, V., Scheuring, S., Kohrer, K., Haussinger, D. (2006). Benign recurrent intrahepatic cholestasis associated with mutations of the bile salt export pump. J Clin Gastroenterol 40:171–175.
   PubMed Web of Science ®Google Scholar
• Lam, P., Wang, R., Ling, V. (2005). Bile acid transport in sister of P-glycoprotein (ABCB11) knockout mice. Biochemistry 44:12598–12605.
   PubMed Web of Science ®Google Scholar
• Lang, C., Meier, Y., Stieger, B., Beuers, U., Lang, T., Kerb, R., et al. (2007). Mutations and polymorphisms in the bile salt export pump and the multidrug resistance protein 3 associated with drug-induced liver injury. Pharmacogenet Genom 17:47–60.
   PubMed Web of Science ®Google Scholar
• Lang, T., Haberl, M., Jung, D., Drescher, A., Schlagenhaufer, R., Keil, A., et al. (2006). Genetic variability, haplotype structures, and ethnic diversity of hepatic transporters MDR3 (ABCB4) and bile salt export pump (ABCB11). Drug Metab Dispos 34:1582–1599.
   PubMed Web of Science ®Google Scholar
• Link, E., Parish, S., Armitage, J., Bowman, L., Heath, S., Matsuda, F., et al. (2008). SLCO1B1 variants and statin-induced myopathy—a genomewide study. NEJM 359:789–799.
   PubMed Web of Science ®Google Scholar
• Liu, X., LeCluyse, E. L., Brouwer, K. R., Gan, L. S., Lemasters, J. J, Stieger, B., et al. (1999). Biliary excretion in primary rat hepatocytes cultured in a collagen-sandwich configuration. Am J Physiol 277:G12–G21.
   PubMed Web of Science ®Google Scholar
• Mano, Y., Usui, T., Kamimura, H. (2007). Effects of bosentan, an endothelin receptor antagonist, on bile salt export pump and multidrug resistance-associated protein 2. Biopharm Drug Dispos 28:13–18.
   PubMed Web of Science ®Google Scholar
• Marion, T. L., Leslie, E. M., Brouwer, K. L. (2007). Use of sandwich-cultured hepatocytes to evaluate impaired bile acid transport as a mechanism of drug-induced hepatotoxicity. Mol Pharm 4:911–918.
   PubMed Web of Science ®Google Scholar
• Masubuchi, Y. (2006). Metabolic and nonmetabolic factors determining troglitazone hepatotoxicity: a review. Drug Metab Pharmacokinet 21:347–356.
   PubMed Web of Science ®Google Scholar
• McRae, M. P., Lowe, C. M., Tian, X., Bourdet, D. L., Ho, R. H., Leake, B. F., et al. (2006). Ritonavir, saquinavir, and efavirenz, but not nevirapine, inhibit bile acid transport in human and rat hepatocytes. J Pharmacol Exp Ther 318:1068–1075.
   PubMed Web of Science ®Google Scholar
• Meier, P. J., Stieger, B. (2002). Bile salt transporters. Annu Rev Physiol 64:635–661.
   PubMed Web of Science ®Google Scholar
• Meier, Y., Cavallaro, M., Roos, M., Pauli-Magnus, C., Folkers, G., Meier, P. J., et al. (2005). Incidence of drug-induced liver injury in medical inpatients. Eur J Clin Pharmacol 61:135–143.
   PubMed Web of Science ®Google Scholar
• Meier, Y., Pauli-Magnus, C., Zanger, U. M., Klein, K., Schaeffeler, E., Nussler, A. K., et al. (2006). Interindividual variability of canalicular ATP-binding-cassette (ABC)-transporter expression in human liver. Hepatology 44:62–74.
   PubMed Web of Science ®Google Scholar
• Meier, Y., Zodan, T., Lang, C., Zimmermann, R., Kullak-Ublick, G. A., Meier, P. J., et al. (2008). Increased susceptibility for intrahepatic cholestasis of pregnancy and contraceptive-induced cholestasis in carriers of the 1331T>C polymorphism in the bile salt export pump. World J Gastroenterol 14:38–45.
   PubMed Web of Science ®Google Scholar
• Mita, S., Suzuki, H., Akita, H., Stieger, B., Meier, P. J., Hofmann, A. F., Sugiyama, Y. (2005). Vectorial transport of bile salts across MDCK cells expressing both rat Na+-taurocholate cotransporting polypeptide and rat bile salt export pump. Am J Physiol Gastrointest Liver Physiol 288:G159–G167.
   PubMed Web of Science ®Google Scholar
• Muehlenberg, K., Wiedmann, K., Keppeler, H., Sauerbruch, T., Lammert, F. (2008). Recurrent intrahepatic cholestasis of pregnancy and chain-like choledocholithiasis in a female patient with stop codon in the ABDC4-gene of the hepatobiliary phospholipid transporter. Z Gastroenterol 46:48–53.
   PubMed Web of Science ®Google Scholar
• Muller, M., Ishikawa, T., Berger, U., Klunemann, C., Lucka, L., Schreyer, A., et al. (1991). ATP-dependent transport of taurocholate across the hepatocyte canalicular membrane mediated by a 110-kDa glycoprotein binding ATP and bile salt. J Biol Chem 266:18920–18926.
   PubMed Web of Science ®Google Scholar
• Nishida, T., Gatmaitan, Z., Che, M., Arias, I. M. (1991). Rat liver canalicular membrane vesicles contain an ATP-dependent bile acid transport system. Proc Natl Acad Sci U S A 88:6590–6594.
   PubMed Web of Science ®Google Scholar
• Noe, J., Kullak-Ublick, G. A., Jochum, W., Stieger, B., Kerb, R., Haberl, M., et al. (2005). Impaired expression and function of the bile salt export pump due to three novel ABCB11 mutations in intrahepatic cholestasis. J Hepatol 43:536–543.
   PubMed Web of Science ®Google Scholar
• Noe, J., Stieger, B., Meier, P. J. (2002). Functional expression of the canalicular bile salt export pump of human liver. Gastroenterology 123:1659–1666.
   PubMed Web of Science ®Google Scholar
• Pauli-Magnus, C., Kerb, R., Fattinger, K., Lang, T., Anwald, B., Kullak-Ublick, G. A., et al. (2004). BSEP and MDR3 haplotype structure in healthy Caucasians, primary biliary cirrhosis, and primary sclerosing cholangitis. Hepatology 39:779–791.
   PubMed Web of Science ®Google Scholar
• Pauli-Magnus, C., Stieger, B., Meier, Y., Kullak Ublick, G. A., Meier, P. J. (2005). Enterohepatic transport of bile salts and genetics of cholestasis. J Hepatol 43:342–357.
   PubMed Web of Science ®Google Scholar
• Paulusma, C. C., de Waart, D. R., Kunne, C., Mok, K. S., Elferink, R. P. (2009). Activity of the bile salt export pump (ABCB11) is critically dependent on canalicular membrane cholesterol content. J Biol Chem 284:9947–9954.
   PubMed Web of Science ®Google Scholar
• Pellicoro, A., Faber, K. N. (2007). Review article: the function and regulation of proteins involved in bile salt biosynthesis and transport. Aliment Pharmacol Ther 26(Suppl 2):149–160.
   PubMedGoogle Scholar
• Preininger, K., Stingl, H., Englisch, R., Furnsinn, C., Graf, J., Waldhausl, W., et al. (1999). Acute troglitazone action in isolated perfused rat liver. Br J Pharmacol 126:372–378.
   PubMed Web of Science ®Google Scholar
• Russmann, S., Kaye, J. A., Jick, S. S., Jick, H. (2005). Risk of cholestatic liver disease associated with flucloxacillin and flucloxacillin prescribing habits in the UK: cohort study using data from the UK General Practice Research Database. Br J Clin Pharmacol 60:76–82.
   PubMed Web of Science ®Google Scholar
• Saito, S., Iida, A., Sekine, A., Miura, Y., Ogawa, C., Kawauchi, S., et al. (2002). Three hundred twenty-six genetic variations in genes encoding nine members of ATP-binding cassette, subfamily B (ABCB/MDR/TAP), in the Japanese population. J Hum Genet 47:38–50.
   PubMed Web of Science ®Google Scholar
• Schuster, D., Laggner, C., Langer, T. (2005). Why drugs fail—a study on side effects in new chemical entities. Curr Pharm Des 11:3545–3559.
   PubMed Web of Science ®Google Scholar
• Smith, D. A., Schmid, E. F. (2006). Drug withdrawals and the lessons within. Curr Opin Drug Discov Devel 9:38–46.
   PubMed Web of Science ®Google Scholar
• Snow, K. L., Moseley, R. H. (2007). Effect of thiazolidinediones on bile acid transport in rat liver. Life Sci 80:732–740.
   PubMed Web of Science ®Google Scholar
• Stieger, B. (2009). Recent insights into the function and regulation of the bile salt export pump (ABCB11). Curr Opin Lipidol 20:176–181.
   PubMed Web of Science ®Google Scholar
• Stieger, B., Fattinger, K., Madon, J., Kullak, Ublick, G. A., Meier, P. J. (2000) Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 118:422–430.
   PubMed Web of Science ®Google Scholar
• Stieger, B., Meier, Y., Meier, P. J. (2007). The bile salt export pump. Pflugers Arch 453:611–620.
   PubMed Web of Science ®Google Scholar
• Stieger, B., O’Neill, B., Meier, P. J. (1992). ATP-dependent bile-salt transport in canalicular rat liver plasma-membrane vesicles. Biochem J 284:67–74.
   PubMed Web of Science ®Google Scholar
• Stieger, B., Zhang, J., O’Neill, B., Sjovall, J., Meier, P. J. (1997). Differential interaction of bile acids from patients with inborn errors of bile acid synthesis with hepatocellular bile acid transporters. Eur J Biochem 244:39–44.
   PubMedGoogle Scholar
• Strautnieks, S. S., Bull, L. N., Knisely, A. S., Kocoshis, S. A., Dahl, N., Arnell, H., et al. (1998). A gene encoding a liver-specific ABC transporter is mutated in progressive familial intrahepatic cholestasis. Nat Genet 20:233–238.
   PubMed Web of Science ®Google Scholar
• Strautnieks, S. S., Byrne, J. A., Pawlikowska, L., Cebecauerova, D., Rayner, A., Dutton, L., et al. (2008). Severe bile salt export pump deficiency: 82 different ABCB11 mutations in 109 families. Gastroenterology 134:1203–1214.
   PubMed Web of Science ®Google Scholar
• Sundaram, S. S., Bove, K. E., Lovell, M. A., Sokol, R. J. (2008). Mechanisms of disease: inborn errors of bile acid synthesis. Nat Clin Pract Gastroenterol Hepatol 5:456–468.
   PubMedGoogle Scholar
• Takada, T., Weiss, H. M., Kretz, O., Gross, G., Sugiyama, Y. (2004). Hepatic transport of PKI166, an epidermal growth factor receptor kinase inhibitor of the pyrrolo-pyrimidine class, and its main metabolite, ACU154. Drug Metab Dispos 32:1272–1278.
   PubMed Web of Science ®Google Scholar
• Trauner, M., Boyer, J.L. (2003). Bile salt transporters: molecular characterization, function and regulation. Physiol Rev 83:633–671.
   PubMed Web of Science ®Google Scholar
• Treiber, A., Schneiter, R., Hausler, S., Stieger, B. (2007). Bosentan is a substrate of human OATP1B1 and OATP1B3: inhibition of hepatic uptake as the common mechanism of its interactions with cyclosporin A, rifampicin, and sildenafil. Drug Metab Dispos 35:1400–1407.
   PubMed Web of Science ®Google Scholar
• Vallejo, M., Briz, O., Serrano, M. A., Monte, M. J., Marin, J.J. (2005). Potential role of transinhibition of the bile salt export pump by progesterone metabolites in the etiopathogenesis of intrahepatic cholestasis of pregnancy. J Hepatol 44:1150–1157.
   PubMed Web of Science ®Google Scholar
• Wang, R., Lam, P., Liu, L., Forrest, D., Yousef, I. M., Mignault, D., et al. (2003). Severe cholestasis induced by cholic acid feeding in knockout mice of sister of P-glycoprotein. Hepatology 38:1489–1499.
   PubMed Web of Science ®Google Scholar
• Wang, R., Salem, M., Yousef, I. M., Tuchweber, B., Lam, P., Childs, S. J., et al. (2001). Targeted inactivation of sister of P-glycoprotein gene (spgp) in mice results in nonprogressive, but persistent, intrahepatic cholestasis. Proc Natl Acad Sci U S A 98:2011–2016.
   PubMed Web of Science ®Google Scholar
• Wasmuth, H. E., Glantz, A., Keppeler, H., Simon, E., Bartz, C., Rath, W., et al. (2007). Intrahepatic cholestasis of pregnancy: the severe form is associated with common variants of the hepatobiliary phospholipid transporter ABCB4 gene. Gut 56:265–270.
   PubMed Web of Science ®Google Scholar
• Yabuuchi, H., Tanaka, K., Maeda, M., Takemura, M., Oka, M., Ohashi, R., et al. (2008). Cloning of the dog bile salt export pump (BSEP; ABCB11) and functional comparison with the human and rat proteins. Biopharm Drug Dispos 29:441–448.
   PubMed Web of Science ®Google Scholar
• Zollner, G., Trauner, M. (2006). Molecular mechanisms of cholestasis. Wien Med Wochenschr 156:380–385.
   PubMedGoogle Scholar