Validation and application of Caco-2 assays for the in vitro evaluation of development candidate drugs as substrates or inhibitors of P-glycoprotein to support regulatory submissions

References

• Alderman CP, Allcroft PD. Digoxin–itraconazole interaction: Possible mechanism. Annals of Pharmacotherapy 1998; 31: 438–440
   Web of Science ®Google Scholar
• Artursson P, Karlsson J. Correlation between oral drug absorption in humans and apparent drug permeability coefficients in human intestinal epithelia (Caco-2) cells. Biochemical and Biophysical Research Communications 1991; 175: 880–890
   PubMed Web of Science ®Google Scholar
• Ayrton A, Morgan P. Role of transport proteins in drug absorption, distribution and excretion. Xenobiotica 2001; 31: 469–497
   PubMed Web of Science ®Google Scholar
• Balimane PV, Han Y-H, Chong S. Current industrial practices of assessing permeability and P-glycoprotein interaction. AAPS Journal 2006; 8: 1–13
   PubMed Web of Science ®Google Scholar
• Bjornsson TD, Callaghan JT, Einolf HJ, Fischer V, Gan L, Grimm S, Kao J, King SP, Miwa G, Ni L, et al. The conduct of in vitro and in vivo drug–drug interaction studies: A pharmaceutical research and manufacturers of America (PhRMA) perspective. Drug Metabolism and Disposition 2003; 31: 815–832
   PubMed Web of Science ®Google Scholar
• Englund G, Rorsman F, Rönnblom A, Karlbom U, Lazorova L, Gråsjö J, Kindmark A, Artursson P. Regional levels of drug transporters along the human intestinal tract: Co-expression of ABC and SLC transporters and comparison with Caco-2 cells. European Journal of Pharmaceutical Sciences 2006; 29: 269–277
   PubMed Web of Science ®Google Scholar
• Fromm MF, Kim RB, Stein CM, Wilkinson GR, Roden DM. Inhibition of p-glycoprotein-mediated drug transport: A unifying mechanism to explain the interaction between digoxin and quinidine. Circulation 1999; 99: 472–474
   PubMed Web of Science ®Google Scholar
• Greiner B, Eichelbaum M, Fritz P, Kreichgauer HP, Von RO, Zundler J, Kroemer HK. The role of intestinal P-glycoprotein in the interaction of digoxin and rifampin. Journal of Clinical Investigation 1999; 104: 147–153
   PubMed Web of Science ®Google Scholar
• Gupta A, Unadkat JD, Mao Q. Interactions of azole antifungal agents with the human breast cancer resistance protein (BCRP). Journal of Pharmaceutical Sciences 2007; 96: 3226–3235
   PubMed Web of Science ®Google Scholar
• Gutmann H, Fricker G, Török M, Michael S, Beglinger C, Drewe J. Evidence for different ABC-transporters in Caco-2 cells modulating drug uptake. Pharmaceutical Research 1999; 16: 402–407
   PubMed Web of Science ®Google Scholar
• Hedman A, Angelin B, Arvidsson A, Dahlqvist R, Nilsson B. Interactions in the renal and biliary elimination of digoxin: Stereoselective difference between quinine and quinidine. Clinical Pharmacology and Therapeutics 1990; 47: 20–26
   PubMed Web of Science ®Google Scholar
• Hilgendorf C, Ahlin G, Seithel A, Artursson P, Ungell A-L, Karlsson J. Expression of thirty-six drug transporter genes in human intestine, liver, kidney, and organotypic cell lines. Drug Metabolism and Disposition 2007; 35: 1333–1340
   PubMed Web of Science ®Google Scholar
• Jalava KM, Partanen J, Neuvonen PJ. Itraconazole decreases renal clearance of digoxin. Therapeutic Drug Monitoring 1997; 19: 609–613
   PubMed Web of Science ®Google Scholar
• Keogh JP, Kunta JR. Development, validation and utility of an in vitro technique for assessment of potential clinical drug–drug interactions involving P-glycoprotein. European Journal of Pharmaceutical Sciences 2006; 27: 543–554
   PubMed Web of Science ®Google Scholar
• Kim RB. Transporters and drug discovery: Why, when, and how. Molecular Pharmaceutics 2006; 3: 26–32
   PubMed Web of Science ®Google Scholar
• Kim RB, Wandel C, Leake B, Cvetkovic M, Fromm MF, Dempsey PJ, Roden MM, Belas F, Chaudhary AK, Roden DM, et al. Interrelationship between substrates and inhibitors of human CYP3A and P-glycoprotein. Pharmaceutical Research 1999; 16: 408–414
   PubMed Web of Science ®Google Scholar
• Koren G, Woodland C, Ito S. Toxic digoxin–drug interactions: The major role of renal P-glycoprotein. Veterinary and Human Toxicology 1998; 40: 45–46
   PubMedGoogle Scholar
• Kusuhara H, Sugiyama Y. Role of transporters in the tissue-selective distribution and elimination of drugs: Transporters in the liver, small intestine, brain and kidney. Journal of Controlled Release 2002; 78: 43–54
   PubMed Web of Science ®Google Scholar
• Martin C, Berridge G, Higgins CF, Mistry P, Charlton P, Callaghan R. Communication between multiple drug binding sites on P-glycoprotein. Molecular Pharmacology 2000; 58: 624–632
   PubMed Web of Science ®Google Scholar
• Mizuno N, Niwa T, Yotsumoto Y, Sugiyama Y. Impact of drug transporter studies on drug discovery and development. Pharmacological Reviews 2003; 55: 425–461
   PubMed Web of Science ®Google Scholar
• Müller J, Lips KS, Metzner L, Neubert RHH, Koepsell H, Brandsch M. Drug specificity and intestinal membrane localization of human organic transporters (OCT). Biochemical Pharmacology 2005; 70: 1851–1860
   PubMed Web of Science ®Google Scholar
• Partanen J, Jalava KM, Neuvonen PJ. Itraconazole increases serum digoxin concentration. Pharmacology and Toxicology 1996; 79: 274–276
   PubMedGoogle Scholar
• Pederson KE, Christiansen BD, Klitgaard NA, Nielsen-Kudsk F. Effect of quinidine on digoxin bioavailability. European Journal of Clinical Pharmacology 1983; 24: 41–47
   PubMed Web of Science ®Google Scholar
• Polli JW, Wring SA, Humphreys JE, Huang L, Morgan JB, Webster LO, Serabjit-Singh CS. Rational use of in vitro P-glycoprotein assays in drug discovery. Journal of Pharmacology and Experimental Therapeutics 2001; 299: 620–628
   PubMed Web of Science ®Google Scholar
• Prime-Chapman HM, Fearn RA, Cooper AE, Moore V, Hirst BH. Differential multidrug resistance-associated protein 1 through 6 isoform expression and function in human intestinal epithelial Caco-2 cells. Journal of Pharmacology and Experimental Therapeutics 2004; 311: 476–484
   PubMed Web of Science ®Google Scholar
• Rosenberg MF, Velarde G, Ford RC, Martin C, Berridge G, Kerr ID, Callaghan R, Schmidin A, Wooding C, Linton KJ, et al. Repacking of the transmembrane domains of P-glycoprotein during the transport ATPase cycle. EMBO Journal 2001; 20: 5615–5625
   PubMed Web of Science ®Google Scholar
• Sadaque AJM, Wandel C, He H, Shah S, Wood AJJ. Increased drug delivery to the brain by P-glycoprotein inhibition. Clinical Pharmacology and Therapeutics 2000; 68: 231–237
   PubMed Web of Science ®Google Scholar
• Schinkel AH. P-glycoprotein, a gatekeeper in the blood–brain barrier. Advanced Drug Delivery Reviews 1999; 36: 179–194
   PubMed Web of Science ®Google Scholar
• Schwab D, Fischer H, Tabatabaei A, Poli S, Huwyler J. Comparison of in vitro P-glycoprotein screening assays: Recommendations for their use in drug discovery. Journal of Medicinal Chemistry 2003; 46: 1716–1725
   PubMed Web of Science ®Google Scholar
• Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues 1987; 84: 7735–7738
   Google Scholar
• Troutman MD, Thakker DR. Efflux ratio cannot assess P-glycoprotein mediated attenuation of absorptive transport: Asymmetric effect of P-glycoprotein on absorptive and secretory transport across Caco-2 cell monolayers. Pharmaceutical Research 2003; 20: 1200–1209
   PubMed Web of Science ®Google Scholar
• US Food and Drug Administration. Draft guidance for industry: Drug interaction studies — study design, data analysis, and implications for dosing and labeling. 2006, (available at: http://www.fda.gov/cder/guidance.com)
   Google Scholar
• Walgren RA, Walle T. The influence of plasma binding on absorption/exsorption in the Caco-2 model of human intestinal absorption. Journal of Pharmacy and Pharmacology 1999; 51: 1037–1040
   PubMed Web of Science ®Google Scholar
• Wang RB, Kuo CL, Lien LL, Lien EJ. Structure–activity relationships: Analyses of P-glycoprotein substrates and inhibitors. Journal of Clinical Pharmacy and Therapeutics 2003; 28: 203–228
   PubMed Web of Science ®Google Scholar
• Xia CQ, Liu N, Yang D, Miwa G, Gan L-S. Expression, localization, and functional characteristics of breast cancer resistance protein in Caco-2 cells. Drug Metabolism and Disposition 2005; 33: 637–643
   PubMed Web of Science ®Google Scholar
• Xia CQ, Milton MN, Gan L-S. Evaluation of drug–transporter interactions using in vitro and in vivo models. Current Drug Metabolism 2007; 8: 341–363
   PubMed Web of Science ®Google Scholar
• Yengi LG, Leung L, Kao J. The evolving role of drug metabolism in drug discovery and development. Pharmaceutical Research 2007; 24: 842–858
   PubMed Web of Science ®Google Scholar
• Zelcer N, Huisman MT, Reid G, Wielinga P, Breedveld P, Kuil A, Knipscheer P, Schellens JHM, Schinkel AH, Borst P. Evidence of two interacting ligand binding sites in human multidrug resistance protein 2 (ATP binding cassette C2). Journal of Biological Chemistry 2003; 278: 23538–23544
   PubMed Web of Science ®Google Scholar
• Zhang L, Strong JM, Qiu W, Lesko LJ, Huang S-M. Scientific perspectives on drug transporters and their role in drug interactions. Molecular Pharmaceutics 2006; 3: 62–69
   PubMed Web of Science ®Google Scholar