Correction to Drug-induced perturbations of the bile acid pool, cholestasis, and hepatotoxicity: Mechanistic considerations beyond the direct inhibition of the bile salt export pump (Drug Metabolism and Disposition (2014) 42 (566-574) DOI: 10.1124/dmd.113.054205);Drug-induced perturbations of the bile acid pool, cholestasis, and hepatotoxicity: Mechanistic considerations beyond the direct inhibition of the bile salt export pump

Drug Metabolism and Disposition

Volumn 42, Issue 4, 2014, Pages 566-574

  Rodrigues, A David ^a   Lai, Yurong ^a   Cvijic, Mary Ellen ^a   Elkin, Lisa L ^a   Zvyaga, Tatyana ^a   Soars, Matthew G ^a  

^a BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOPHOSPHOLIPID; ATPASE AMINOPHOSPHOLIPID TRANSPORTER; BILE ACID; BILE SALT EXPORT PUMP; CONSTITUTIVE ANDROSTANE RECEPTOR; FARNESOID X RECEPTOR; MULTIDRUG RESISTANCE PROTEIN 3; PREGNANE X RECEPTOR; PROTEIN KINASE; UNCLASSIFIED DRUG;

AMIDATION; BILE ACID METABOLISM; BILIARY EXCRETION; CHOLESTASIS; COMPETITIVE INHIBITION; ENTEROHEPATIC CIRCULATION; ENZYME INHIBITION; HUMAN; LIPID METABOLISM; LIVER TOXICITY; METABOLIC INHIBITION; METABOLIC REGULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; REVIEW; SULFATION; TOXIC HEPATITIS;

ATP-BINDING CASSETTE TRANSPORTERS; BILE ACIDS AND SALTS; BILE CANALICULI; BIOLOGICAL TRANSPORT; CHOLESTASIS; DRUG-INDUCED LIVER INJURY; FECES; HEPATOCYTES; HUMANS; MODELS, BIOLOGICAL;

EID: 84896108804     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.114.054205err     Document Type: Erratum

References (73)

1. Abu-Hayyeh S, Martinez-Becerra P, Sheikh Abdul Kadir SH, Selden C, Romero MR, Rees M, Marschall HU, Marin JJ, and Williamson C (2010) Inhibition of Na+-taurocholate co-transporting polypeptide-mediated bile acid transport by cholestatic sulfated progesterone metabolites. J Biol Chem 285:16504-16512.
2. Abu-Hayyeh S, Papacleovoulou G, Lövgren-Sandblom A, Tahir M, Oduwole O, Jamaludin NA, Ravat S, Nikolova V, Chambers J, and Selden C, et al. (2013) Intrahepatic cholestasis of pregnancy levels of sulfated progesterone metabolites inhibit farnesoid X receptor resulting in a cholestatic phenotype. Hepatology 57:716-726.
3. Alnouti Y (2009) Bile acid sulfation: a pathway of bile acid elimination and detoxification. Toxicol Sci 108:225-246.
4. Ballatori N, Li N, Fang F, Boyer JL, Christian WV, and Hammond CL (2009) OST alpha-OST beta: a key membrane transporter of bile acids and conjugated steroids. Front Biosci (Landmark Ed) 14:2829-2844.
5. Bjornsson ES and Jonasson JG (2013) Drug-induced cholestasis. Clin Liver Dis 17:191-209.
6. Boaglio AC, Zucchetti AE, Sánchez Pozzi EJ, Pellegrino JM, Ochoa JE, Mottino AD, Vore M, Crocenzi FA, and Roma MG (2010) Phosphoinositide 3-kinase/protein kinase B signaling pathway is involved in estradiol 17β-D-glucuronide-induced cholestasis: complementarity with classical protein kinase C. Hepatology 52:1465-1476.
7. Brandoni A, Hazelhoff MH, Bulacio RP, and Torres AM (2012) Expression and function of renal and hepatic organic anion transporters in extrahepatic cholestasis. World J Gastroenterol 18:6387-6397.
8. Chang JH, Plise E, Cheong J, Ho Q, and Lin M (2013) Evaluating the in vitro inhibition of UGT1A1, OATP1B1, OATP1B3, MRP2, and BSEP in predicting drug-induced hyperbilirubinemia. Mol Pharm 10:3067-3075.
9. Chen J, Terada T, Ogasawara K, Katsura T, and Inui K (2008) Adaptive responses of renal organic anion transporter 3 (OAT3) during cholestasis. Am J Physiol Renal Physiol 295:F247-F252.
10. Cowen AE, Korman MG, Hofmann AF, and Cass OW (1975) Metabolism of lethocholate in healthy man. I. Biotransformation and biliary excretion of intravenously administered lithocholate, lithocholylglycine, and their sulfates. Gastroenterology 69:59-66.
11. Crocenzi FA, Zucchetti AE, Boaglio AC, Barosso IR, Sanchez Pozzi EJ, Mottino AD, and Roma MG (2012) Localization status of hepatocellular transporters in cholestasis. Front Biosci (Landmark Ed) 17:1201-1218.
12. Dawson S, Stahl S, Paul N, Barber J, and Kenna JG (2012) In vitro inhibition of the bile salt export pump correlates with risk of cholestatic drug-induced liver injury in humans. Drug Metab Dispos 40:130-138.
13. Dzagania T, Engelmann G, Häussinger D, Schmitt L, Flechtenmacher C, Rtskhiladze I, and Kubitz R (2012) The histidine-loop is essential for transport activity of human MDR3: a novel mutation of MDR3 in a patient with progressive familial intrahepatic cholestasis type 3. Gene 506:141-145.
14. Falany CN, Johnson MR, Barnes S, and Diasio RB (1994) Glycine and taurine conjugation of bile acids by a single enzyme: molecular cloning and expression of human liver bile acid CoA: amino acid N-acyltransferase. J Biol Chem 269:19375-19379.
15. Funk C, Pantze M, Jehle L, Ponelle C, Scheuermann G, Lazendic M, and Gasser R (2001) 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. (Pubitemid 32830949)
16. García-Cañaveras JC, Donato MT, Castell JV, and Lahoz A (2012) Targeted profiling of circulating and hepatic bile acids in human, mouse, and rat using a UPLC-MRM-MS-validated method. J Lipid Res 53:2231-2241.
17. Godoy P, Hewitt NJ, Albrecht U, Andersen ME, Ansari N, Bhattacharya S, Bode JG, Bolleyn J, Borner C, and Böttger J, et al. (2013) Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Arch Toxicol 87:1315-1530.
18. Gonzalez FJ (2012) Nuclear receptor control of enterohepatic circulation. Compr Physiol 2:2811-2828.
19. Gradhand U, Lang T, Schaeffeler E, Glaeser H, Tegude H, Klein K, Fritz P, Jedlitschky G, Kroemer HK, and Bachmakov I, et al. (2008) Variability in human hepatic MRP4 expression: influence of cholestasis and genotype. Pharmacogenomics J 8:42-52.
20. Groen A, Romero MR, Kunne C, Hoosdally SJ, Dixon PH, Wooding C, Williamson C, Seppen J, Van den Oever K, and Mok KS,, et al. (2011) Complementary functions of the flippase ATP8B1 and the floppase ABCB4 in maintaining canalicular membrane integrity. Gastroenterology 141:1927-1937, e1-e4.
21. Guo GL, Lambert G, Negishi M, Ward JM, Brewer HB, Jr, Kliewer SA, Gonzalez FJ, and Sinal CJ (2003) Complementary roles of farnesoid X receptor, pregnane X receptor, and constitutive androstane receptor in protection against bile acid toxicity. J Biol Chem 278:45062-45071. (Pubitemid 37432638)
22. Hadžić N, Bull LN, Clayton PT, and Knisely AS (2012) Diagnosis in bile acid-CoA: amino acid N-acyltransferase deficiency. World J Gastroenterol 18:3322-3326.
23. Halilbasic E, Claudel T, and Trauner M (2013) Bile acid transporters and regulatory nuclear receptors in the liver and beyond. J Hepatol 58:155-168.
24. Hamilton JP, Xie G, Raufman JP, Hogan S, Griffin TL, Packard CA, Chatfield DA, Hagey LR, Steinbach JH, and Hofmann AF (2007) Human cecal bile acids: concentration and spectrum. Am J Physiol Gastrointest Liver Physiol 293:G256-G263. (Pubitemid 47105194)
25. Harris MJ, Le Couteur DG, and Arias IM (2005) Progressive familial intrahepatic cholestasis: genetic disorders of biliary transporters. J Gastroenterol Hepatol 20:807-817. (Pubitemid 40897160)
26. Hayashi H, Takada T, Suzuki H, Onuki R, Hofmann AF, and 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. (Pubitemid 43122130)
27. Heuman DM, Hylemon PB, and Vlahcevic ZR (1989) Regulation of bile acid synthesis. III. Correlation between biliary bile salt hydrophobicity index and the activities of enzymes regulating cholesterol and bile acid synthesis in the rat. J Lipid Res 30:1161-1171. (Pubitemid 19213256)
28. Huang H, Wang H, Sinz M, Zoeckler M, Staudinger J, Redinbo MR, Teotico DG, Locker J, Kalpana GV, and Mani S (2007) Inhibition of drug metabolism by blocking the activation of nuclear receptors by ketoconazole. Oncogene 26:258-268. (Pubitemid 46095736)
29. Huang J, Bathena SP, Tong J, RothM, Hagenbuch B, and Alnouti Y (2010) Kinetic analysis of bile acid sulfation by stably expressed human sulfotransferase 2A1 (SULT2A1). Xenobiotica 40:184-194.
30. Humbert L, Maubert MA, Wolf C, Duboc H, Mahé M, Farabos D, Seksik P, Mallet JM, Trugnan G, and Masliah J, et al. (2012) Bile acid profiling in human biological samples: comparison of extraction procedures and application to normal and cholestatic patients. J Chromatogr B Analyt Technol Biomed Life Sci 899:135-145.
31. Keppler D (2011) Cholestasis and the role of basolateral efflux pumps. Z Gastroenterol 49:1553-1557.
32. Kubitz R, Dröge C, Stindt J, Weissenberger K, and Häussinger D (2012) The bile salt export pump (BSEP) in health and disease. Clin Res Hepatol Gastroenterol 36:536-553.
33. Li T and Chiang JY (2013) Nuclear receptors in bile acid metabolism. Drug Metab Rev 45:145-155.
34. Lööf L and Wengle B (1979) Enzymatic sulphation of bile salts in man. Scand J Gastroenterol 14:513-519. (Pubitemid 9240712)
35. Meier PJ, Eckhardt U, Schroeder A, Hagenbuch B, and Stieger B (1997) Substrate specificity of sinusoidal bile acid and organic anion uptake systems in rat and human liver. Hepatology 26: 1667-1677. (Pubitemid 27520039)
36. Mercado-Lubo R and McCormick BA (2010) The interaction of gut microbes with host ABC transporters. Gut Microbes 1:301-306.
37. Miyata M, Yamakawa H, Hamatsu M, Kuribayashi H, Takamatsu Y, and Yamazoe Y (2011) Enterobacteria modulate intestinal bile acid transport and homeostasis through apical sodiumdependent bile acid transporter (SLC10A2) expression. J Pharmacol Exp Ther 336:188-196.
38. Morgan RE, Trauner M, van Staden CJ, Lee PH, Ramachandran B, Eschenberg M, Afshari CA, Qualls CW, Jr, Lightfoot-Dunn R, and Hamadeh HK (2010) Interference with bile salt export pump function is a susceptibility factor for human liver injury in drug development. Toxicol Sci 118:485-500.
39. Morgan RE, van Staden CJ, Chen Y, Kalyanaraman N, Kalanzi J, Dunn RT, 2nd, Afshari CA, and Hamadeh HK (2013) A multifactorial approach to hepatobiliary transporter assessment enables improved therapeutic compound development. Toxicol Sci 2013 Aug 16 [Epub ahead of print].
40. Northfield TC and McColl I (1973) Postprandial concentrations of free and conjugated bile acids down the length of the normal human small intestine. Gut 14:513-518.
41. O'Byrne J, Hunt MC, Rai DK, Saeki M, and Alexson SE (2003) The human bile acid-CoA:amino acid N-acyltransferase functions in the conjugation of fatty acids to glycine. J Biol Chem 278:34237-34244. (Pubitemid 37553266)
42. Ozer J, Ratner M, Shaw M, Bailey W, and Schomaker S (2008) The current state of serum biomarkers of hepatotoxicity. Toxicology 245:194-205.
43. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, and Moore DD, et al. (1999) Bile acids: natural ligands for an orphan nuclear receptor. Science 284:1365-1368. (Pubitemid 29289664)
44. Pauli-Magnus C and Meier PJ (2006) Hepatobiliary transporters and drug-induced cholestasis. Hepatology 44:778-787. (Pubitemid 46489540)
45. Pedersen JM, Matsson P, Bergström CA, Hoogstraate J, Norén A, Lecluyse E, and Artursson P (2013) Early identification of clinically relevant drug interactions with the human bile salt export pump (BSEP; ABCB11). Toxicol Sci 2013 Oct 14 [Epub ahead of print].
46. Pérez LM, Milkiewicz P, Elias E, Coleman R, Sánchez Pozzi EJ, and Roma MG (2006) Oxidative stress induces internalization of the bile salt export pump, Bsep, and bile salt secretory failure in isolated rat hepatocyte couplets: a role for protein kinase C and prevention by protein kinase A. Toxicol Sci 91:150-158.
47. Renga B, Migliorati M, Mencarelli A, Cipriani S, D'Amore C, Distrutti E, and Fiorucci S (2011) Farnesoid X receptor suppresses constitutive androstane receptor activity at the multidrug resistance protein-4 promoter. Biochim Biophys Acta 1809:157-165.
48. Riches Z, Stanley EL, Bloomer JC, and Coughtrie MW (2009) Quantitative evaluation of the expression and activity of five major sulfotransferases (SULTs) in human tissues: the SULT "pie". Drug Metab Dispos 37:2255-2261.
49. Ridlon JM, Kang DJ, and Hylemon PB (2006) Bile salt biotransformations by human intestinal bacteria. J Lipid Res 47:241-259. (Pubitemid 43276911)
50. Rius M, Hummel-Eisenbeiss J, Hofmann AF, and Keppler D (2006) Substrate specificity of human ABCC4 (MRP4)-mediated cotransport of bile acids and reduced glutathione. Am J Physiol Gastrointest Liver Physiol 290:G640-G649.
51. Robben J, Janssen G, Merckx R, and Eyssen H (1989) Formation of delta 2- and delta 3-cholenoic acids from bile acid 3-sulfates by a human intestinal Fusobacterium strain. Appl Environ Microbiol 55:2954-2959. (Pubitemid 19272172)
52. Roma MG, Crocenzi FA, and Mottino AD (2008) Dynamic localization of hepatocellular transporters in health and disease. World J Gastroenterol 14:6786-6801.
53. Rossi SS, Converse JL, and Hofmann AF (1987) High pressure liquid chromatographic analysis of conjugated bile acids in human bile: simultaneous resolution of sulfated and unsulfated lithocholyl amidates and the common conjugated bile acids. J Lipid Res 28:589-595. (Pubitemid 17116189)
54. Sekine S, Ito K, Saeki J, and Horie T (2011) Interaction of Mrp2 with radixin causes reversible canalicular Mrp2 localization induced by intracellular redox status. Biochim Biophys Acta 1812:1427-1434.
55. Solaas K, Ulvestad A, Söreide O, and Kase BF (2000) Subcellular organization of bile acid amidation in human liver: a key issue in regulating the biosynthesis of bile salts. J Lipid Res 41:1154-1162. (Pubitemid 30483021)
56. Stahl S, Davies MR, Cook DI, and Graham MJ (2008) Nuclear hormone receptor-dependent regulation of hepatic transporters and their role in the adaptive response in cholestasis. Xenobiotica 38:725-777.
57. Staudinger JL, Goodwin B, Jones SA, Hawkins-Brown D, MacKenzie KI, LaTour A, Liu Y, Klaassen CD, Brown KK, and Reinhard J, et al. (2001) The nuclear receptor PXR is a lithocholic acid sensor that protects against liver toxicity. Proc Natl Acad Sci USA 98:3369-3374. (Pubitemid 32220852)
58. Stepan AF, Walker DP, Bauman J, Price DA, Baillie TA, Kalgutkar AS, and Aleo MD (2011) Structural alert/reactive metabolite concept as applied in medicinal chemistry to mitigate the risk of idiosyncratic drug toxicity: a perspective based on the critical examination of trends in the top 200 drugs marketed in the United States. Chem Res Toxicol 24:1345-1410.
59. Takikawa H, Beppu T, and Seyama Y (1985) Profiles of bile acids and their glucuronide and sulphate conjugates in the serum, urine and bile from patients undergoing bile drainage. Gut 26:38-42. (Pubitemid 15109200)
60. Thompson RA, Isin EM, Li Y, Weidolf L, Page K, Wilson I, Swallow S, Middleton B, Stahl S, and Foster AJ, et al. (2012) In vitro approach to assess the potential for risk of idiosyncratic adverse reactions caused by candidate drugs. Chem Res Toxicol 25:1616-1632.
61. Trauner M and Boyer JL (2003) Bile salt transporters: molecular characterization, function, and regulation. Physiol Rev 83:633-671. (Pubitemid 36378680)
62. Trottier J, Perreault M, Rudkowska I, Levy C, Dallaire-Theroux A, Verreault M, Caron P, Staels B, Vohl MC, and Straka RJ, et al. (2013) Profiling serum bile acid glucuronides in humans: gender divergences, genetic determinants, and response to fenofibrate. Clin Pharmacol Ther 94:533-543.
63. Ulzurrun E, Stephens C, Crespo E, Ruiz-Cabello F, Ruiz-Nuñez J, Saenz-López P, Moreno-Herrera I, Robles-Díaz M, Hallal H, and Moreno-Planas JM, et al. (2013) Role of chemical structures and the 1331T.C bile salt export pump polymorphism in idiosyncratic drug-induced liver injury. Liver Int 33:1378-1385.
64. van Berge Henegouwen GP, Brandt KH, Eyssen H, and Parmentier G (1976) Sulphated and unsulphated bile acids in serum, bile, and urine of patients with cholestasis. Gut 17:861-869. (Pubitemid 8005662)
65. van de Steeg E, Stránecký V, Hartmannová H, Nosková L, Hřebíček M, Wagenaar E, van Esch A, de Waart DR, Oude Elferink RP, and Kenworthy KE, et al. (2012) Complete OATP1B1 and OATP1B3 deficiency causes human rotor syndrome by interrupting conjugated bilirubin reuptake into the liver. J Clin Invest 122:519-528.
66. Vessey DA and Kelley M (1995) Inhibition of bile acid conjugation by cyclosporin A. Biochim Biophys Acta 1272:49-52.
67. Vinken M, Landesmann B, Goumenou M, Vinken S, Shah I, Jaeschke H, Willett C, Whelan M, and Rogiers V (2013) Development of an adverse outcome pathway from drug-mediated bile salt export pump inhibition to cholestatic liver injury. Toxicol Sci 2013 Sep 20 [Epub ahead of print].
68. Wang R, Chen HL, Liu L, Sheps JA, Phillips MJ, and Ling V (2009) Compensatory role of P-glycoproteins in knockout mice lacking the bile salt export pump. Hepatology 50:948-956.
69. Warner DJ, Chen H, Cantin LD, Kenna JG, Stahl S, Walker CL, and Noeske T (2012) Mitigating the inhibition of human bile salt export pump by drugs: opportunities provided by physicochemical property modulation, in silico modeling, and structural modification. Drug Metab Dispos 40:2332-2341.
70. Xie W, Radominska-Pandya A, Shi Y, Simon CM, Nelson MC, Ong ES, Waxman DJ, and Evans RM (2001) An essential role for nuclear receptors SXR/PXR in detoxification of cholestatic bile acids. Proc Natl Acad Sci USA 98:3375-3380. (Pubitemid 32220853)
71. Yang K, Köck K, Sedykh A, Tropsha A, and Brouwer KL (2013) An updated review on drug-induced cholestasis: mechanisms and investigation of physicochemical properties and pharmacokinetic parameters. J Pharm Sci 102:3037-3057.
72. Yoshikado T, Takada T, Yamamoto T, Yamaji H, Ito K, Santa T, Yokota H, Yatomi Y, Yoshida H, and Goto J, et al. (2011) Itraconazole-induced cholestasis: involvement of the inhibition of bile canalicular phospholipid translocator MDR3/ABCB4. Mol Pharmacol 79:241-250.
73. Zeng H, Liu G, Rea PA, and Kruh GD (2000) Transport of amphipathic anions by human multidrug resistance protein 3. Cancer Res 60:4779-4784.