Species differences in hepatobiliary disposition of taurocholic acid in human and rat sandwich-cultured hepatocytes: Implications for drug-induced liver injury

Journal of Pharmacology and Experimental Therapeutics

Volumn 353, Issue 2, 2015, Pages 415-423

  Yang, Kyunghee ^a,b   Pfeifer, Nathan D ^a   Köck, Kathleen ^a   Brouwer, Kim L R ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b HAMNER INSTITUTES FOR HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 4; TAUROCHOLIC ACID; TROGLITAZONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ABCC4 PROTEIN, HUMAN; CHROMAN DERIVATIVE; MULTIDRUG RESISTANCE PROTEIN; PRASTERONE; SULFATE; TROGLITAZONE SULFATE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; BILE FLOW; BILIARY EXCRETION; BIOLOGICAL FUNCTIONS; BIOLOGICAL MODEL; CELL ASSAY; CONTROLLED STUDY; DISEASE PREDISPOSITION; HEPATOBILIARY SYSTEM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LIVER CELL; LIVER TOXICITY; MEMBRANE VESICLE; METABOLITE; NONHUMAN; PHARMACOKINETICS; PRIORITY JOURNAL; RAT; SIMULATION; SPECIES DIFFERENCE; TOXIC HEPATITIS; ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; BILE DUCT; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FEMALE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ADULT; ANIMALS; BILE DUCTS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CHROMANS; DEHYDROEPIANDROSTERONE; DRUG-INDUCED LIVER INJURY; FEMALE; HEPATOCYTES; HUMANS; MALE; MIDDLE AGED; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; RATS; SPECIES SPECIFICITY; SULFURIC ACID ESTERS; TAUROCHOLIC ACID; THIAZOLIDINEDIONES;

EID: 84931305900     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.221564     Document Type: Article

References (42)

1. Akita H, Suzuki H, Hirohashi T, Takikawa H, and Sugiyama Y (2002) Transport activity of human MRP3 expressed in Sf9 cells: comparative studies with rat MRP3. Pharm Res 19:34-41.
2. Akita H, Suzuki H, and Sugiyama Y (2001) Sinusoidal efflux of taurocholate is enhanced in Mrp2-deficient rat liver. Pharm Res 18:1119-1125.
3. 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.
4. Chiang JY (2009) Bile acids: regulation of synthesis. J Lipid Res 50:1955-1966.
5. 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.
6. 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.
7. Ghibellini G, Leslie EM, Pollack GM, and Brouwer KLR (2008) Use of Tc-99m mebrofenin as a clinical probe to assess altered hepatobiliary transport: integration of in vitro, pharmacokinetic modeling, and simulation studies. Pharm Res 25:1851-1860.
8. Hofmann AF (1999a) Bile Acids: The good, the bad, and the ugly. News Physiol Sci 14:24-29.
9. Hofmann AF (1999b) The continuing importance of bile acids in liver and intestinal disease. Arch Intern Med 159:2647-2658.
10. Hofmann AF (2004) Detoxification of lithocholic acid, a toxic bile acid: relevance to drug hepatotoxicity. Drug Metab Rev 36:703-722.
11. Iusuf D, van de Steeg E, and Schinkel AH (2012) Hepatocyte hopping of OATP1B substrates contributes to efficient hepatic detoxification. Clin Pharmacol Ther 92: 559-562.
12. Jansen PL, Strautnieks SS, Jacquemin E, Hadchouel M, Sokal EM, Hooiveld GJ, Koning JH, De Jager-Krikken A, Kuipers F, Stellaard F, et al. (1999) Hepatocanalicular bile salt export pump deficiency in patients with progressive familial intrahepatic cholestasis. Gastroenterology 117:1370-1379.
13. Jemnitz K, Veres Z, and Vereczkey L (2010) Contribution of high basolateral bile salt efflux to the lack of hepatotoxicity in rat in response to drugs inducing cholestasis in human. Toxicol Sci 115:80-88.
14. Köck K, Ferslew BC, Netterberg I, Yang K, Urban TJ, Swaan PW, Stewart PW, and Brouwer KLR (2014) Risk factors for development of cholestatic drug-induced liver injury: inhibition of hepatic basolateral bile acid transporters multidrug resistance-associated proteins 3 and 4. Drug Metab Dispos 42:665-674.
15. Kotani N, Maeda K, Watanabe T, Hiramatsu M, Gong LK, Bi YA, Takezawa T, Kusuhara H, and Sugiyama Y (2011) Culture period-dependent changes in the uptake of transporter substrates in sandwich-cultured rat and human hepatocytes. Drug Metab Dispos 39:1503-1510.
16. LeCluyse EL, Bullock PL, Parkinson A, and Hochman JH (1996) Cultured rat hepatocytes. Pharm Biotechnol 8:121-159.
17. Lee JK and Brouwer KR (2010) Determination of intracellular volume of rat and human sandwich-cultured hepatocytes (Abstract ID 1595). The Toxicologist. Supplement to Toxicological Sciences 114:339.
18. Lee JK, Marion TL, Abe K, Lim C, Pollack GM, and Brouwer KLR (2010) Hepatobiliary disposition of troglitazone and metabolites in rat and human sandwich-cultured hepatocytes: use of Monte Carlo simulations to assess the impact of changes in biliary excretion on troglitazone sulfate accumulation. J Pharmacol Exp Ther 332:26-34.
19. Leslie EM, Watkins PB, Kim RB, and Brouwer KLR (2007) Differential inhibition of rat and human Na+-dependent taurocholate cotransporting polypeptide (NTCP/SLC10A1) by bosentan: a mechanism for species differences in hepatotoxicity. J Pharmacol Exp Ther 321:1170-1178.
20. Liu X, Brouwer KLR, Gan LS, Brouwer KR, Stieger B, Meier PJ, Audus KL, and LeCluyse EL (1998) Partial maintenance of taurocholate uptake by adult rat hepatocytes cultured in a collagen sandwich configuration. Pharm Res 15: 1533-1539.
21. Maillette de Buy Wenniger L and Beuers U (2010) Bile salts and cholestasis. Dig Liver Dis 42:409-418.
22. Marion TL, Leslie EM, and Brouwer KLR (2007) Use of sandwich-cultured hepatocytes to evaluate impaired bile acid transport as a mechanism of drug-induced hepatotoxicity. Mol Pharm 4:911-918.
23. 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.
24. 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 136:216-241.
25. Nguyen A and Bouscarel B (2008) Bile acids and signal transduction: role in glucose homeostasis. Cell Signal 20:2180-2197.
26. Oshio C and Phillips MJ (1981) Contractility of bile canaliculi: implications for liver function. Science 212:1041-1042.
27. Pedersen JM, Matsson P, Bergström CA, Hoogstraate J, Norén A, LeCluyse EL, and Artursson P (2013) Early identification of clinically relevant drug interactions with the human bile salt export pump (BSEP/ABCB11). Toxicol Sci 136:328-343.
28. Perez MJ and Briz O (2009) Bile-acid-induced cell injury and protection. World J Gastroenterol 15:1677-1689.
29. Pfeifer ND, Hardwick RN, and Brouwer KLR (2014) Role of hepatic efflux transporters in regulating systemic and hepatocyte exposure to xenobiotics. Annu Rev Pharmacol Toxicol 54:509-535.
30. Pfeifer ND, Yang K, and Brouwer KLR (2013) Hepatic basolateral efflux contributes significantly to rosuvastatin disposition I: characterization of basolateral versus biliary clearance using a novel protocol in sandwich-cultured hepatocytes. J Pharmacol Exp Ther 347:727-736.
31. Phillips MJ, Oshio C, Miyairi M, Katz H, and Smith CR (1982) A study of bile canalicular contractions in isolated hepatocytes. Hepatology 2:763-768.
32. 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.
33. Saha S, New LS, Ho HK, Chui WK, and Chan EC (2010) Direct toxicity effects of sulfo-conjugated troglitazone on human hepatocytes. Toxicol Lett 195:135-141.
34. Setchell KD, Rodrigues CM, Clerici C, Solinas A, Morelli A, Gartung C, and Boyer J (1997) Bile acid concentrations in human and rat liver tissue and in hepatocyte nuclei. Gastroenterology 112:226-235.
35. Sohlenius-Sternbeck AK (2006) Determination of the hepatocellularity number for human, dog, rabbit, rat and mouse livers from protein concentration measurements. Toxicol In Vitro 20:1582-1586.
36. Swift B, Pfeifer ND, and Brouwer KLR (2010) Sandwich-cultured hepatocytes: an in vitro model to evaluate hepatobiliary transporter-based drug interactions and hepatotoxicity. Drug Metab Rev 42:446-471.
37. Tchaparian EH, Houghton JS, Uyeda C, Grillo MP, and Jin L (2011) Effect of culture time on the basal expression levels of drug transporters in sandwich-cultured primary rat hepatocytes. Drug Metab Dispos 39:2387-2394.
38. Trauner M, Wagner M, Fickert P, and Zollner G (2005) Molecular regulation of hepatobiliary transport systems: clinical implications for understanding and treating cholestasis. J Clin Gastroenterol 39(4, Suppl 2):S111-S124.
39. Watanabe N, Tsukada N, Smith CR, and Phillips MJ (1991) Motility of bile canaliculi in the living animal: implications for bile flow. J Cell Biol 113:1069-1080.
40. Watkins PB and Seeff LB (2006) Drug-induced liver injury: summary of a single topic clinical research conference. Hepatology 43:618-631.
41. Zamek-Gliszczynski MJ, Kalvass JC, Pollack GM, and Brouwer KLR (2009) Relationship between drug/metabolite exposure and impairment of excretory transport function. Drug Metab Dispos 37:386-390.
42. Zollner G, Wagner M, Fickert P, Silbert D, Gumhold J, Zatloukal K, Denk H, and Trauner M (2007) Expression of bile acid synthesis and detoxification enzymes and the alternative bile acid efflux pump MRP4 in patients with primary biliary cirrhosis. Liver Int 27:920-929.