Erratum: In vitro methods to support transporter evaluation in drug discovery and development (Clinical Pharmacology and Therapeutics (2013) 91 (95-112) DOI 10.1038/clpt.2013.81);In vitro methods to support transporter evaluation in drug discovery and development

Clinical Pharmacology and Therapeutics

Volumn 94, Issue 1, 2013, Pages 95-112

  Brouwer, K L R ^a   Keppler, D ^b   Hoffmaster, K A ^c   Bow, D A J ^d   Cheng, Y ^e   Lai, Y ^e   Palm, J E ^f   Stieger, B ^g   Evers, R ^h  

^a University of North Carolina   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^d ABBVIE INC   (United States)

^e BRISTOL MYERS SQUIBB   (United States)

^f ASTRAZENECA R AND D   (Sweden)

^g UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^h MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DRUG METABOLITE; MULTIDRUG RESISTANCE PROTEIN;

BILIARY EXCRETION; CELL LINE; DRUG DEVELOPMENT; DRUG DISPOSITION; DRUG INDUSTRY; DRUG INTERACTION; HUMAN; KINETICS; LIVER CELL; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW;

EID: 84879417097     PISSN: 00099236     EISSN: 15326535     Source Type: Journal    
DOI: 10.1038/clpt.2013.130     Document Type: Erratum

References (75)

1. Giacomini, K.M. et al. Membrane transporters in drug development. Nat. Rev. Drug Discov. 9, 215-236 (2010).
2. Morrissey, K.M., Wen, C.C., Johns, S.J., Zhang, L., Huang, S.M. & Giacomini, K.M. The UCSF-FDA TransPortal: a public drug transporter database. Clin. Pharmacol. Ther. 92, 545-546 (2012).
3. Zamek-Gliszczynski, M.J., Hofmaster, K.A., Tweedie, D.J., Giacomini, K.M. & Hillgren, K.M. Highlights from the International Transporter Consortium second workshop. Clin. Pharmacol. Ther. 92, 553-556 (2012).
4. Feng, B. et al. In vitro P-glycoprotein assays to predict the in vivo interactions of P-glycoprotein with drugs in the central nervous system. Drug Metab. Dispos. 36, 268-275 (2008).
5. yamazaki, M. et al. In vitro substrate identifcation studies for p-glycoprotein-mediated transport: species diference and predictability of in vivo results. J. Pharmacol. Exp. Ther. 296, 723-735 (2001).
6. Hirano, M., Maeda, K., Shitara, Y. & Sugiyama, Y. Contribution of OATP2 (OATP1B1) and OATP8 (OATP1B3) to the hepatic uptake of pitavastatin in humans. J. Pharmacol. Exp. Ther. 311, 139-146 (2004).
7. Bjornsson, T.D. et al.; Pharmaceutical Research and Manufacturers of America (PhRMA) Drug Metabolism/Clinical Pharmacology Technical Working Group; FDA Center for Drug Evaluation and Research (CDER). The conduct of in vitro and in vivo drug-drug interaction studies: a Pharmaceutical Research and Manufacturers of America (PhRMA) perspective. Drug Metab. Dispos. 31, 815-832 (2003).
8. Kondo, T., Dale, G.L. & Beutler, E. Glutathione transport by inside-out vesicles from human erythrocytes. Proc. Natl. Acad. Sci. USA 77, 6359-6362 (1980).
9. Ahlin, G., Hilgendorf, C., Karlsson, J., Szigyarto, C.A., Uhlén, M. & Artursson, P. Endogenous gene and protein expression of drug-transporting proteins in cell lines routinely used in drug discovery programs. Drug Metab. Dispos. 37, 2275-2283 (2009).
10. Meier, P.J. & Boyer, J.L. Preparation of basolateral (sinusoidal) and canalicular plasma membrane vesicles for the study of hepatic transport processes. Meth. Enzymol. 192, 534-545 (1990).
11. Tabas, L.B. & Dantzig, A.H. A high-throughput assay for measurement of multidrug resistance protein-mediated transport of leukotriene C4 into membrane vesicles. Anal. Biochem. 310, 61-66 (2002).
12. Keppler, D., Jedlitschky, G. & Leier, I. Transport function and substrate specifcity of multidrug resistance protein. Meth. Enzymol. 292, 607-616 (1998).
13. Böhme, M., Müller, M., Leier, I., Jedlitschky, G. & Keppler, D. Cholestasis caused by inhibition of the adenosine triphosphate-dependent bile salt transport in rat liver. Gastroenterology 107, 255-265 (1994).
14. Loe, D.W., Deeley, R.G. & Cole, S.P. Characterization of vincristine transport by the M(r) 190, 000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res. 58, 5130-5136 (1998).
15. Bakos, E., Evers, R., Sinkó, E., Váradi, A., Borst, P. & Sarkadi, B. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 57, 760-768 (2000).
16. Rius, M., Nies, A.T., Hummel-Eisenbeiss, J., Jedlitschky, G. & Keppler, D. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38, 374-384 (2003).
17. Evers, R. et al. Vinblastine and sulfnpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br. J. Cancer 83, 375-383 (2000).
18. Zelcer, N. et al. Evidence for two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). J. Biol. Chem. 278, 23538-23544 (2003).
19. de Waart, D.R. et al. Hepatic transport mechanisms of cholyl-L-lysyl-fuorescein. J. Pharmacol. Exp. Ther. 334, 78-86 (2010).
20. de Graaf, W. et al. Transporters involved in the hepatic uptake of (99m)Tc-mebrofenin and indocyanine green. J. Hepatol. 54, 738-745 (2011).
21. Chu, X. et al. Intracellular drug concentrations and transporters in the liver: measurement, modeling, and implications. Clin. Pharmacol. Ther. 94, 126-141 (2013).
22. Jacquemin, E., Hagenbuch, B., Stieger, B., Wolkof, A.W. & Meier, P.J. Expression cloning of a rat liver Na(+)-independent organic anion transporter. Proc. Natl. Acad. Sci. USA 91, 133-137 (1994).
23. Kessler, M., Tannenbaum, V., Tannenbaum, C. A simple apparatus for performing short-time (1-2 seconds) uptake measurements in small volumes; its application to D-glucose transport studies in brush border vesicles from rabbit jejunum and ileum. Biochim. Biophys. Acta. 509, 348-359 (1978).
24. Schomig, E., Lazar, A., Grundemann, D. Extraneuronal monoamine transporter and organic cation transporters 1 and 2: a review of transport efciency. Handb Exp Pharmacol. 175, 151-180 (2006).
25. O'Gorman, S., Fox, D.T. & Wahl, G.M. Recombinase-mediated gene activation and site-specifc integration in mammalian cells. Science 251, 1351-1355 (1991).
26. Keppler, D. Uptake and efux transporters for conjugates in human hepatocytes. Meth. Enzymol. 400, 531-542 (2005).
27. Shitara, Y., Horie, T. & Sugiyama, Y. Transporters as a determinant of drug clearance and tissue distribution. Eur. J. Pharm. Sci. 27, 425-446 (2006).
28. Yonezawa, A. & Inui, K. Importance of the multidrug and toxin extrusion MATE/SLC47A family to pharmacokinetics, pharmacodynamics/ toxicodynamics and pharmacogenomics. Br. J. Pharmacol. 164, 1817-1825 (2011).
29. Tran, T.T. et al. The elementary mass action rate constants of P-gp transport for a confuent monolayer of MDCKII-hMDR1 cells. Biophys. J. 88, 715-738 (2005).
30. Acharya, P., O'Connor, M.P., Polli, J.W., Ayrton, A., Ellens, H. & Bentz, J. Kinetic identifcation of membrane transporters that assist P-glycoprotein-mediated transport of digoxin and loperamide through a confuent monolayer of MDCKII-hMDR1 cells. Drug Metab. Dispos. 36, 452-460 (2008).
31. Bartholomé, K., Rius, M., Letschert, K., Keller, D., Timmer, J. & Keppler, D. Data-based mathematical modeling of vectorial transport across double-transfected polarized cells. Drug Metab. Dispos. 35, 1476-1481 (2007).
32. Zamek-Gliszczynski, M.J. et al. ITC recommendations for transporter kinetic parameter estimation and translational modeling of transport-mediated PK and DDIs in humans. Clin. Pharmacol. Ther. 94, 64-79 (2013).
33. Sharom, F.J., Lugo, M.R. & Eckford, P.D. New insights into the drug binding, transport and lipid fippase activities of the p-glycoprotein multidrug transporter. J. Bioenerg. Biomembr. 37, 481-487 (2005).
34. Kalvass, J.C. & Pollack, G.M. Kinetic considerations for the quantitative assessment of efux activity and inhibition: implications for understanding and predicting the efects of efux inhibition. Pharm. Res. 24, 265-276 (2007).
35. Lumen, A.A., Acharya, P., Polli, J.W., Ayrton, A., Ellens, H. & Bentz, J. If the KI is defned by the free energy of binding to P-glycoprotein, which kinetic parameters defne the IC50 for the Madin-Darby canine kidney II cell line overexpressing human multidrug resistance 1 confuent cell monolayer? Drug Metab. Dispos. 38, 260-269 (2010).
36. Hayeshi, R. et al. Comparison of drug transporter gene expression and functionality in Caco-2 cells from 10 diferent laboratories. Eur. J. Pharm. Sci. 35, 383-396 (2008).
37. Hubatsch, I., Ragnarsson, E.G. & Artursson, P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat. Protoc. 2, 2111-2119 (2007).
38. Hidalgo, I.J., Raub, T.J. & Borchardt, R.T. Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96, 736-749 (1989).
39. Volpe, D.A. Drug-permeability and transporter assays in Caco-2 and MDCK cell lines. Future Med. Chem. 3, 2063-2077 (2011).
40. Thiel-Demby, V.E. et al. Biopharmaceutics classifcation system: validation and learnings of an in vitro permeability assay. Mol. Pharm. 6, 11-18 (2009).
41. LeCluyse, E.L., Bullock, P.L., Parkinson, A. & Hochman, J.H. Cultured rat hepatocytes. Pharm. Biotechnol. 8, 121-159 (1996).
42. Hofmaster, K.A., Zamek-Gliszczynski, M.J., Pollack, G.M. & Brouwer, K.L.R Multiple transport systems mediate the hepatic uptake and biliary excretion of the metabolically stable opioid peptide [D-penicillamine2, 5]enkephalin. Drug Metab. Dispos. 33, 287-293 (2005).
43. Yabe, Y., Galetin, A. & Houston, J.B. Kinetic characterization of rat hepatic uptake of 16 actively transported drugs. Drug Metab. Dispos. 39, 1808-1814 (2011).
44. Leslie, E.M., Watkins, P.B., Kim, R.B. & Brouwer, K.L.R. Diferential inhibition of rat and human Na+-dependent taurocholate cotransporting polypeptide (NTCP/SLC10A1)by bosentan: a mechanism for species diferences in hepatotoxicity. J. Pharmacol. Exp. Ther. 321, 1170-1178 (2007).
45. Häussinger, D., Lang, F. & Gerok, W. Regulation of cell function by the cellular hydration state. Am. J. Physiol. 267, E343-E355 (1994).
46. Li, M. et al. Identifcation of interspecies diference in efux transporters of hepatocytes from dog, rat, monkey and human. Eur. J. Pharm. Sci. 35, 114-126 (2008).
47. Ishigami, M., Tokui, T., Komai, T., Tsukahara, K., yamazaki, M. & Sugiyama, Y. Evaluation of the uptake of pravastatin by perfused rat liver and primary cultured rat hepatocytes. Pharm. Res. 12, 1741-1745 (1995).
48. Houle, R., Raoul, J., Lévesque, J.F., Pang, K.S., Nicoll-Grifth, D.A. & Silva, J.M. Retention of transporter activities in cryopreserved, isolated rat hepatocytes. Drug Metab. Dispos. 31, 447-451 (2003).
49. Jørgensen, L., Van Beek, J., Lund, S., Schousboe, A. & Badolo, L. Evidence of Oatp and Mdr1 in cryopreserved rat hepatocytes. Eur. J. Pharm. Sci. 30, 181-189 (2007).
50. Bow, D.A., Perry, J.L., Miller, D.S., Pritchard, J.B. & Brouwer, K.L.R. Localization of P-gp (Abcb1) and Mrp2 (Abcc2) in freshly isolated rat hepatocytes. Drug Metab. Dispos. 36, 198-202 (2008).
51. Kimoto, E. et al. Characterization of organic anion transporting polypeptide (OATP) expression and its functional contribution to the uptake of substrates in human hepatocytes. Mol. Pharm;e-pub ahead of print 2 November 2012.
52. Soars, M.G., Grime, K., Sproston, J.L., Webborn, P.J. & Riley, R.J. Use of hepatocytes to assess the contribution of hepatic uptake to clearance in vivo. Drug Metab. Dispos. 35, 859-865 (2007).
53. Swift, B., Pfeifer, N.D. & Brouwer, K.L.R. Sandwich-cultured hepatocytes: an in vitro model to evaluate hepatobiliary transporter-based drug interactions and hepatotoxicity. Drug Metab. Rev. 42, 446-471 (2010).
54. Bi, Y.A. et al. In vitro evaluation of hepatic transporter-mediated clinical drug-drug interactions: hepatocyte model optimization and retrospective investigation. Drug Metab. Dispos. 40, 1085-1092 (2012).
55. Liu, X., LeCluyse, E.L., Brouwer, K.R., Lightfoot, R.M., Lee, J.I. & Brouwer, K.L.R. Use of Ca2+ modulation to evaluate biliary excretion in sandwich-cultured rat hepatocytes. J. Pharmacol. Exp. Ther. 289, 1592-1599 (1999).
56. Hofmaster, K.A., Turnclif, R.Z., LeCluyse, E.L., Kim, R.B., Meier, P.J. & Brouwer, K.L.R. P-glycoprotein expression, localization, and function in sandwich-cultured primary rat and human hepatocytes: relevance to the hepatobiliary disposition of a model opioid peptide. Pharm. Res. 21, 1294-1302 (2004).
57. Lee, J.K., Marion, T.L., Abe, K., Lim, C., Pollock, G.M. & Brouwer, K.L.R. 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 (2010).
58. Li, N., Singh, P., Mandrell, K.M. & Lai, Y. Improved extrapolation of hepatobiliary clearance from in vitro sandwich cultured rat hepatocytes through absolute quantifcation of hepatobiliary transporters. Mol. Pharm. 7, 630-641 (2010).
59. Jones, H.M. et al. Mechanistic pharmacokinetic modeling for the prediction of transporter-mediated disposition in humans from sandwich culture human hepatocyte data. Drug Metab. Dispos. 40, 1007-1017 (2012).
60. Yan, G.Z. et al. A semiphysiologically based pharmacokinetic modeling approach to predict the dose-exposure relationship of an antiparasitic prodrug/active metabolite pair. Drug Metab. Dispos. 40, 6-17 (2012).
61. Abe, K., Bridges, A.S., yue, W. & Brouwer, K.L.R. In vitro biliary clearance of angiotensin II receptor blockers and 3-hydroxy-3-methylglutaryl- coenzyme A reductase inhibitors in sandwich-cultured rat hepatocytes: comparison with in vivo biliary clearance. J. Pharmacol. Exp. Ther. 326, 983-990 (2008).
62. Fukuda, H., Ohashi, R., Tsuda-Tsukimoto, M. & Tamai, I. Efect of plasma protein binding on in vitro-in vivo correlation of biliary excretion of drugs evaluated by sandwich-cultured rat hepatocytes. Drug Metab. Dispos. 36, 1275-1282 (2008).
63. Abe, K., Bridges, A.S. & Brouwer, K.L.R. Use of sandwich-cultured human hepatocytes to predict biliary clearance of angiotensin II receptor blockers and HMG-CoA reductase inhibitors. Drug Metab. Dispos. 37, 447-452 (2009).
64. Ghibellini, G. et al. In vitro-in vivo correlation of hepatobiliary drug clearance in humans. Clin. Pharmacol. Ther. 81, 406-413 (2007).
65. Chandra, P., Zhang, P. & Brouwer, K.L.R. Short-term regulation of multidrug resistance-associated protein 3 in rat and human hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G1252-G1258 (2005).
66. Benet, L.Z. The role of BCS (biopharmaceutics classifcation system) and BDDCS (biopharmaceutics drug disposition classifcation system) in drug development. J. Pharm. Sci. 102, 34-42 (2013).
67. Tweedie, D. et al. Transporter studies in drug development: experience to date and follow-up on decision trees from the International Transport Consortium. Clin. Pharmacol. Ther. 94, 113-125 (2013).
68. Pauli-Magnus, C. & Meier, P.J. Hepatobiliary transporters and drug-induced cholestasis. Hepatology 44, 778-787 (2006).
69. Hardwick, R.N., Fisher, C.D., Canet, M.J., Schefer, G.L. & Cherrington, N.J. Variations in ATP-binding cassette transporter regulation during the progression of human nonalcoholic fatty liver disease. Drug Metab. Dispos. 39, 2395-2402 (2011).
70. Shitara, Y., Takeuchi, K., Nagamatsu, Y., Wada, S., Sugiyama, Y. & Horie, T. Long-lasting inhibitory efects of cyclosporin A, but not tacrolimus, on OATP1B1-and OATP1B3-mediated uptake. Drug Metab. Pharmacokinet. 27, 368-378 (2012).
71. Chu, X., Bleasby, K. & Evers, R. Species diferences in drug transporters and implications for translating preclinical fndings to humans. Expert Opin. Drug Metab. Toxicol. 9, 237-252 (2013).
72. Yoshida, K., Maeda, K. & Sugiyama, Y. Hepatic and intestinal drug transporters: prediction of pharmacokinetic efects caused by drug-drug interactions and genetic polymorphisms. Annu. Rev. Pharmacol. Toxicol. 53, 581-612 (2013).
73. Dawson, S., Stahl, S., Paul, N., Barber, J. & Kenna, J.G. 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 (2012).
74. Morgan, R.E. et al. Interference with bile salt export pump function is a susceptibility factor for human liver injury in drug development. Toxicol. Sci. 118, 485-500 (2010).
75. Lee, K., Hart, R., & Brouwer, K. P187. Hepatobiliary disposition of bilirubin and its mono-and di-glucuronide metabolites in sandwich-cultured rat hepatocytes. Drug Metabol. Rev. 43, 128-129 (2011).