Construction of triple-transfected cells [organic anion-transporting polypeptide (OATP) 1B1/multidrug resistance-associated protein (MRP) 2/MRP3 and OATP1B1/MRP2/MRP4] for analysis of the sinusoidal function of MRP3 and MRP4

Drug Metabolism and Disposition

Volumn 37, Issue 10, 2009, Pages 2103-2111

  Hirouchi, Masakazu ^a   Kusuhara, Hiroyuki ^a   Onuki, Reiko ^a   Ogilvie, Brian W ^b   Parkinson, Andrew ^b   Sugiyama, Yuichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b XenoTech LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; 6 HYDROXY 5,7 DIMETHYL 2 METHYLAMINO 4 (3 PYRIDYLMETHYL)BENZOTHIAZOLE; ANION TRANSPORT PROTEIN; ESTRADIOL; GEMFIBROZIL; HYMECROMONE; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; ORGANIC ANION TRANSPORTING POLYOPEPTIDE 1B1; TROGLITAZONE; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL EXPERIMENT; ARTICLE; BASEMENT MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG UPTAKE; EMBRYO; GENETIC TRANSFECTION; HEPATOBILIARY SYSTEM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; IN VIVO STUDY; MALE; MEMBRANE VESICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CELLS, CULTURED; HEPATOCYTES; HYMECROMONE; MALE; MICE; MICE, KNOCKOUT; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; ORGANIC ANION TRANSPORTERS; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; SWINE; TRANSFECTION;

ADENOVIRIDAE; MUS;

EID: 70349282243     PISSN: 00909556     EISSN: 1521009X     Source Type: Journal    
DOI: 10.1124/dmd.109.027193     Document Type: Article

References (45)

1. Akita H, Suzuki H, Hirohashi T, Takikawa H, and Sugiyama Y (2002a) Transport activity of human MRP3 expressed in Sf9 cells: comparative studies with rat MRP3. Pharm Res 19:34-41. (Pubitemid 34075104)
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. (Pubitemid 32900396)
3. Akita H, Suzuki H, and Sugiyama Y (2002b) Sinusoidal efflux of taurocholate correlates with the hepatic expression level of Mrp3. Biochem Biophys Res Commun 299:681-687. (Pubitemid 36034540)
4. Belinsky MG, Dawson PA, Shchaveleva I, Bain LJ, Wang R, Ling V, Chen ZS, Grinberg A, Westphal H, Klein-Szanto A, et al. (2005) Analysis of the in vivo functions of Mrp3. Mol Pharmacol 68:160-168.
5. Büchler M, König J, Brom M, Kartenbeck J, Spring H, Horie T, and Keppler D (1996) cDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J Biol Chem 271:15091-15098. (Pubitemid 26197579)
6. Chen ZS, Lee K, and Kruh GD (2001) Transport of cyclic nucleotides and estradiol 17-β-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J Biol Chem 276:33747-33754. (Pubitemid 37384594)
7. Ci L, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, and Sugiyama Y (2007) Involvement of MRP4 (ABCC4) in the luminal efflux of ceftizoxime and cefazolin in the kidney. Mol Pharmacol 71:1591-1597. (Pubitemid 47010912)
8. Cui Y, König J, Buchholz JK, Spring H, Leier I, and Keppler D (1999) Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol Pharmacol 55:929-937. (Pubitemid 29214613)
9. Cui Y, König J, Leier I, Buchholz U, and Keppler D (2001) Hepatic uptake of bilirubin and its conjugates by the human organic anion transporter SLC21A6. J Biol Chem 276:9626-9630. (Pubitemid 37391856)
10. Evers R, Kool M, van Deemter L, Janssen H, Calafat J, Oomen LC, Paulusma CC, Oude Elferink RP, Baas F, Schinkel AH, et al. (1998) Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Invest 101:1310-1319. (Pubitemid 28166828)
11. 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. (Pubitemid 28183107)
12. Grams B, Harms A, Braun S, Strassburg CP, Manns MP, and Obermayer-Straub P (2000) Distribution and inducibility by 3-methylcholanthrene of family 1 UDP-glucuronosyltransferases in the rat gastrointestinal tract. Arch Biochem Biophys 377:255-265. (Pubitemid 30331886)
13. Hasegawa M, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, and Sugiyama Y (2007) Multidrug resistance-associated protein 4 is involved in the urinary excretion of hydrochlorothiazide and furosemide. J Am Soc Nephrol 18:37-45. (Pubitemid 46053420)
14. Hirohashi T, Suzuki H, Chu XY, Tamai I, Tsuji A, and Sugiyama Y (2000) Function and expression of multidrug resistance-associated protein family in human colon adenocarcinoma cells (Caco-2). J Pharmacol Exp Ther 292:265-270. (Pubitemid 30026380)
15. Hirouchi M, Suzuki H, Itoda M, Ozawa S, Sawada J, Ieiri I, Ohtsubo K, and Sugiyama Y (2004) Characterization of the cellular localization, expression level, and function of SNP variants of MRP2/ABCC2. Pharm Res 21:742-748. (Pubitemid 39011294)
16. Imaoka T, Kusuhara H, Adachi M, Schuetz JD, Takeuchi K, and Sugiyama Y (2007) Functional involvement of multidrug resistance-associated protein 4 (MRP4/ABCC4) in the renal elimination of the antiviral drugs adefovir and tenofovir. Mol Pharmacol 71:619-627. (Pubitemid 46147926)
17. Ishiguro N, Maeda K, Saito A, Kishimoto W, Matsushima S, Ebner T, Roth W, Igarashi T, and Sugiyama Y (2008) Establishment of a set of double transfectants coexpressing organic anion transporting polypeptide 1B3 and hepatic efflux transporters for the characterization of the hepatobiliary transport of telmisartan acylglucuronide. Drug Metab Dispos 36:796-805.
18. Keppler D and König J (2000) Hepatic secretion of conjugated drugs and endogenous substances. Semin Liver Dis 20:265-272. (Pubitemid 30807964)
19. Kitamura Y, Hirouchi M, Kusuhara H, Schuetz JD, and Sugiyama Y (2008) Increasing systemic exposure of methotrexate by active efflux mediated by multidrug resistance-associated protein 3 (Mrp3/Abcc3). J Pharmacol Exp Ther 327:465-473.
20. Kiuchi Y, Suzuki H, Hirohashi T, Tyson CA, and Sugiyama Y (1998) cDNA cloning and inducible expression of human multidrug resistance associated protein 3 (MRP3). FEBS Lett 433:149-152. (Pubitemid 28386747)
21. Klaassen CD and Watkins JB 3rd (1984) Mechanisms of bile formation, hepatic uptake, and biliary excretion. Pharmacol Rev 36:1-67.
22. König J, Nies AT, Cui Y, Leier I, and Keppler D (1999a) Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim Biophys Acta 1461:377-394.
23. König J, Rost D, Cui Y, and Keppler D (1999b) Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane. Hepatology 29:1156-1163. (Pubitemid 29168750)
24. Kopplow K, Letschert K, König J, Walter B, and Keppler D (2005) Human hepatobiliary transport of organic anions analyzed by quadruple- transfected cells. Mol Pharmacol 68:1031-1038. (Pubitemid 41345794)
25. Kruh GD and Belinsky MG (2003) The MRP family of drug efflux pumps. Oncogene 22:7537-7552.
26. Kusuhara H and Sugiyama Y (2009) In vitro-in vivo extrapolation of transporter-mediated clearance in the liver and kidney. Drug Metab Pharmacokinet 24:37-52.
27. Lai L and Tan TM (2002) Role of glutathione in the multidrug resistance protein 4 (MRP4/ ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem J 361:497-503. (Pubitemid 34177819)
28. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-267.
29. Manautou JE, de Waart DR, Kunne C, Zelcer N, Goedken M, Borst P, and Elferink RO (2005) Altered disposition of acetaminophen in mice with a disruption of the Mrp3 gene. Hepatology 42:1091-1098. (Pubitemid 43112676)
30. 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. (Pubitemid 41205969)
31. Mizuguchi H and Kay MA (1998) Efficient construction of a recombinant adenovirus vector by an improved in vitro ligation method. Hum Gene Ther 9:2577-2583. (Pubitemid 29004630)
32. Mizuguchi H and Kay MA (1999) A simple method for constructing E1- and E1/E4-deleted recombinant adenoviral vectors. Hum Gene Ther 10:2013-2017. (Pubitemid 29387915)
33. Ogilvie BW, Zhang D, Li W, Rodrigues AD, Gipson AE, Holsapple J, Toren P, and Parkinson A (2006) Glucuronidation converts gemfibrozil to a potent, metabolism-dependent inhibitor of CYP2C8: implications for drug-drug interactions. Drug Metab Dispos 34:191-197. (Pubitemid 43042661)
34. Paulusma CC, Bosma PJ, Zaman GJ, Bakker CT, Otter M, Scheffer GL, Scheper RJ, Borst P, and Oude Elferink RP (1996) Congenital jaundice in rats with a mutation in a multidrug resistance-associated protein gene. Science 271:1126-1128. (Pubitemid 26075228)
35. Rius M, Nies AT, Hummel-Eisenbeiss J, Jedlitschky G, and Keppler D (2003) Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38:374-384. (Pubitemid 36919858)
36. Rost D, Mahner S, Sugiyama Y, and Stremmel W (2002) Expression and localization of the multidrug resistance-associated protein 3 in rat small and large intestine. Am J Physiol Gastrointest Liver Physiol 282:G720-G726. (Pubitemid 34651651)
37. Sasaki M, Suzuki H, Ito K, Abe T, and Sugiyama Y (2002) Transcellular transport of organic anions across a double-transfected Madin-Darby canine kidney II cell monolayer expressing both human organic anion-transporting polypeptide (OATP2/SLC21A6) and multidrug resistance- associated protein 2 (MRP2/ABCC2). J Biol Chem 277:6497-6503. (Pubitemid 34968447)
38. Shoji T, Suzuki H, Kusuhara H, Watanabe Y, Sakamoto S, and Sugiyama Y (2004) ATPdependent transport of organic anions into isolated basolateral membrane vesicles from rat intestine. Am J Physiol Gastrointest Liver Physiol 287:G749-G756. (Pubitemid 39280432)
39. Suzuki H and Sugiyama Y (1998) Excretion of GSSG and glutathione conjugates mediated by MRP1 and cMOAT/MRP2. Semin Liver Dis 18:359-376. (Pubitemid 29011040)
40. Ueda K, Kato Y, Komatsu K, and Sugiyama Y (2001) Inhibition of biliary excretion of methotrexate by probenecid in rats: quantitative prediction of interaction from in vitro data. J Pharmacol Exp Ther 297:1036-1043. (Pubitemid 32472501)
41. Watanabe T, Kusuhara H, Maeda K, Shitara Y, and Sugiyama Y (2009) Physiologically based pharmacokinetic modeling to predict transporter-mediated clearance and distribution of pravastatin in humans. J Pharmacol Exp Ther 328:652-662.
42. Zamek-Gliszczynski MJ, Nezasa K, Tian X, Bridges AS, Lee K, Belinsky MG, Kruh GD, and Brouwer KL (2006) Evaluation of the role of multidrug resistance-associated protein (Mrp) 3 and Mrp4 in hepatic basolateral excretion of sulfate and glucuronide metabolites of acetaminophen, 4-methylumbelliferone, and harmol in Abcc3-/- and Abcc4-/- mice. J Pharmacol Exp Ther 319:1485-1491. (Pubitemid 44776498)
43. Zelcer N, Reid G, Wielinga P, Kuil A, van der Heijden I, Schuetz JD, and Borst P (2003) Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem J 371:361-367. (Pubitemid 36547618)
44. Zelcer N, van de Wetering K, Hillebrand M, Sarton E, Kuil A, Wielinga PR, Tephly T, Dahan A, Beijnen JH, and Borst P (2005) Mice lacking multidrug resistance protein 3 show altered morphine pharmacokinetics and morphine-6-glucuronide antinociception. Proc Natl Acad Sci U S A 102:7274-7279. (Pubitemid 40696369)
45. Zelcer N, van de Wetering K, de Waart R, Scheffer GL, Marschall HU, Wielinga PR, Kuil A, Kunne C, Smith A, van der Valk M, et al. (2006) Mice lacking Mrp3 (Abcc3) have normal bile salt transport, but altered hepatic transport of endogenous glucuronides. J Hepatol 44:768-775.