Re-evaluation of the role of P-glycoprotein in in vitro drug permeability studies with the bovine brain microvessel endothelial cells

References

• Abbott NJ. (2004). Prediction of blood–brain barrier permeation in drug discovery from in vivo. in vitro and in silico models. Drug Discov Today: Technol 1:407–16
   PubMedGoogle Scholar
• Arboix M, Paz OG, Colombo T, D'Incalci M. (1997). Multidrug resistance-reversing agents increase vinblastine distribution in normal tissues expressing the P-glycoprotein but do not enhance drug penetration in brain and testis. J Pharmacol Exp Ther 281:1226–30
   PubMed Web of Science ®Google Scholar
• Audus KL, Borchardt RT. (1987). Bovine brain microvessel endothelial cell monolayers as a model system for the blood-brain barrier. Ann N Y Acad Sci 507:9–18
   PubMed Web of Science ®Google Scholar
• Audus KL, Ng L, Wang W, Borchardt RT. (1996). Brain microvessel endothelial cell culture systems. Pharm Biotechnol 8:239–58
   PubMedGoogle Scholar
• Avdeef A. (2011). How well can in vitro brain microcapillary endothelial cell models predict rodent in vivo blood-brain barrier permeability? Eur J Pharm Sci 43:109–24
   PubMed Web of Science ®Google Scholar
• Batrakova EV, Han HY, Miller DW, Kabanov AV. (1998). Effects of pluronic P85 unimers and micelles on drug permeability in polarized BBMEC and Caco-2 cells. Pharm Res 15:1525–32
   PubMed Web of Science ®Google Scholar
• Batrakova EV, Miller DW, Li S, et al. (2001). Pluronic P85 enhances the delivery of digoxin to the brain: in vitro and in vivo studies. J Pharmacol Exp Ther 296:551–7
   PubMed Web of Science ®Google Scholar
• Beaulieu E, Demeule M, Pouliot JF, et al. (1995). P-glycoprotein of blood brain barrier: cross-reactivity of Mab C219 with a 190 kDa protein in bovine and rat isolated brain capillaries. Biochim Biophys Acta 1233:27–32
   PubMedGoogle Scholar
• Borges N, Shi F, Azevedo I, Audus KL. (1994). Changes in brain microvessel endothelial cell monolayer permeability induced by adrenergic drugs. Eur J Pharmacol 269:243–8
   PubMedGoogle Scholar
• Cardoso FL, Brites D, Brito MA. (2010). Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev 64:328–63
   PubMed Web of Science ®Google Scholar
• Chappa AK, Audus KL, Lunte SM. (2006). Characteristics of substance P transport across the blood-brain barrier. Pharm Res 23:1201–8
   PubMedGoogle Scholar
• Chen L, Li Y, Yu H, et al. (2012). Computational models for predicting substrates or inhibitors of P-glycoprotein. Drug Discov Today 17:343–51
   PubMed Web of Science ®Google Scholar
• Dehouck MP, Dehouck B, Schluep C, et al. (1995). Drug transport to the brain: comparison between in vitro and in vivo models of the blood-brain barrier. Eur J Pharm Sci 3:357–65
   Google Scholar
• Di L, Kerns EH, Bezar IF, et al. (2009). Comparison of blood-brain barrier permeability assays: in situ brain perfusion, MDR1-MDCKII and PAMPA-BBB. J Pharm Sci 98:1980–91
   PubMed Web of Science ®Google Scholar
• Eddy EP, Maleef BE, Hart TK, Smith PL. (1997). In vitro models to predict blood-brain barrier permeability. Adv Drug Deliv Rev 23:185–98
   Google Scholar
• El Hafny B, Cano N, Piciotti M, et al. (1997). Role of P-glycoprotein in colchicine and vinblastine cellular kinetics in an immortalized rat brain microvessel endothelial cell line. Biochem Pharmacol 53:1735–42
   PubMedGoogle Scholar
• Eneroth A, Åström E, Hoogstraate J, et al. (2001). Evaluation of a vincristine resistant Caco-2 cell line for use in a calcein AM extrusion screening assay for P-glycoprotein interaction. Eur J Pharm Sci 12:205–14
   PubMed Web of Science ®Google Scholar
• Evers R, Kool M, Smith AJ, et al. (2000). Inhibitory effect of the reversal agents V-104, GF120918 and Pluronic L61 on MDR1 Pgp-, MRP1- and MRP2-mediated transport. Br J Cancer 83:366–74
   PubMed Web of Science ®Google Scholar
• Fenart L, Buée-Scherrer V, Descamps L, et al. (1998). Inhibition of P-glycoprotein: rapid assessment of its implication in blood-brain barrier integrity and drug transport to the brain by an in vitro model of the blood-brain barrier. Pharm Res 15:993–1000
   PubMed Web of Science ®Google Scholar
• Gaillard PJ, van der Sandt IC, Voorwinden LH, et al. (2000). Astrocytes increase the functional expression of P-glycoprotein in an in vitro model of the blood-brain barrier. Pharm Res 17:1198–205
   PubMed Web of Science ®Google Scholar
• Garberg P, Ball M, Borg N, et al. (2005). In vitro models for the blood-brain barrier. Toxicol in Vitro 19:299–334
   PubMed Web of Science ®Google Scholar
• Giacomini KM, Huang SM, Tweedie DJ, et al. (2010). Membrane transporters in drug development. Nat Rev Drug Discov 9:215–36
   PubMed Web of Science ®Google Scholar
• Gumbleton M, Audus KL. (2001). Progress and limitations in the use of in vitro cell cultures to serve as a permeability screen for the blood-brain barrier. J Pharm Sci 90:1681–98
   PubMed Web of Science ®Google Scholar
• Hakkarainen JJ, Jalkanen AJ, Kääriäinen TM, et al. (2010). Comparison of in vitro cell models in predicting in vivo brain entry of drugs. Int J Pharm 402:27–36
   PubMed Web of Science ®Google Scholar
• Hamilton KO, Backstrom G, Yazdanian MA, Audus KL. (2001). P-glycoprotein efflux pump expression and activity in Calu-3 cells. J Pharm Sci 90:647–58
   PubMed Web of Science ®Google Scholar
• Hansen DK, Scott DO, Otis KW, Lunte SM. (2002). Comparison of in vitro BBMEC permeability and in vivo CNS uptake by microdialysis sampling. J Pharm Biomed Anal 27:945–58
   PubMed Web of Science ®Google Scholar
• Hellinger E, Veszelka S, Tóth AE, et al. (2012). Comparison of brain capillary endothelial cell-based and epithelial (MDCK-MDR1, Caco-2, and VB-Caco-2) cell-based surrogate blood-brain barrier penetration models. Eur J Pharm Biopharm 82:340–51
   PubMed Web of Science ®Google Scholar
• Hirase T, Staddon JM, Saitou M, et al. (1997). Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110:1603–13
   PubMed Web of Science ®Google Scholar
• Hopper-Borge EA, Churchill T, Paulose C, et al. (2011). Contribution of Abcc10 (Mrp7) to in vivo paclitaxel resistance as assessed in Abcc10(-/-) mice. Cancer Res 71:3649–57
   PubMed Web of Science ®Google Scholar
• Hyafil F, Vergely C, Du Vignaud P, Grand-Perret T. (1993). In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Res 53:4595–602
   PubMed Web of Science ®Google Scholar
• Iwanaga K, Yoneda S, Hamahata Y, et al. (2011). Inhibitory effects of furanocoumarin derivatives in Kampo extract medicines on P-glycoprotein at the blood-brain barrier. Biol Pharm Bull 34:1246–51
   PubMedGoogle Scholar
• Karyekar CS, Fasano A, Raje S, et al. (2003). Zonula occludens toxin increases the permeability of molecular weight markers and chemotherapeutic agents across the bovine brain microvessel endothelial cells. J Pharm Sci 92:414–23
   PubMed Web of Science ®Google Scholar
• Kuhnline Sloan CD, Nandi P, Linz TH, et al. (2012). Analytical and biological methods for probing the blood-brain barrier. Annu Rev Anal Chem 5:505–31
   PubMedGoogle Scholar
• Lechardeur D, Scherman D. (1995). Functional expression of the P-glycoprotein mdr in primary cultures of bovine cerebral capillary endothelial cells. Cell Biol Toxicol 11:283–93
   PubMedGoogle Scholar
• Lentz KA, Polli JW, Wring SA, et al. (2000). Influence of passive permeability on apparent P-glycoprotein kinetics. Pharm Res 17:1456–60
   PubMed Web of Science ®Google Scholar
• Mahar Doan KM, Humphreys JE, Webster LO, et al. (2002). Passive permeability and P-glycoprotein-mediated efflux differentiate central nervous system (CNS) and non-CNS marketed drugs. J Pharmacol Exp Ther 303:1029–37
   PubMed Web of Science ®Google Scholar
• Martin C, Berridge G, Higgins CF, et al. (2000). Communication between multiple drug binding sites on P-glycoprotein. Mol Pharmacol 58:624–32
   PubMed Web of Science ®Google Scholar
• Masereeuw R, Jaehde U, Langemeijer MW, et al. (1994). In vitro and in vivo transport of zidovudine (AZT) across the blood-brain barrier and the effect of transport inhibitors. Pharm Res 11:324–30
   PubMed Web of Science ®Google Scholar
• Mease K, Sane R, Podila L, Taub ME. (2012). Differential selectivity of efflux transporter inhibitors in Caco-2 and MDCK-MDR1 monolayers: a strategy to assess the interaction of a new chemical entity with P-gp, BCRP, and MRP2. J Pharm Sci 101:1888–97
   PubMed Web of Science ®Google Scholar
• Ohno K, Pettigrew KD, Rapoport SI. (1978). Lower limits of cerebrovascular permeability to nonelectrolytes in the conscious rat. Am J Physiol Heart Circ Physiol 235:H299–307
   PubMed Web of Science ®Google Scholar
• Otis KW, Avery ML, Broward-Partin SM, et al. (2001). Evaluation of the BBMEC model for screening the CNS permeability of drugs. J Pharmacol Toxicol Methods 45:71–7
   PubMedGoogle Scholar
• Pardridge WM, Triguero D, Yang J, Cancilla PA. (1990). Comparison of in vitro and in vivo models of drug transcytosis through the blood-brain barrier. J Pharmacol Exp Ther 253:884–91
   PubMed Web of Science ®Google Scholar
• Polli JW, Humphreys JE, Wring SA, et al. (2000). Comparison of MDCK and bovine brain endothelial cells (BBECs) as a blood-brain barrier screen in early drug discovery. In: Balls M, van Zeller A-M, Halder ME, eds. Progress in the reduction, refinement and replacement of animal experimentation. The Netherlands: Elsevier Science, 271–89
   Google Scholar
• Polli JW, Wring SA, Humphreys JE, et al. (2001). Rational use of in vitro P-glycoprotein assays in drug discovery. J Pharmacol Exp Ther 299:620–8
   PubMed Web of Science ®Google Scholar
• Rice A, Liu Y, Michaelis ML, et al. (2005). Chemical modification of paclitaxel (Taxol) reduces P-glycoprotein interactions and increases permeation across the blood-brain barrier in vitro and in situ. J Med Chem 48:832–8
   PubMed Web of Science ®Google Scholar
• Sloan CD, Audus KL, Aldrich JV, Lunte SM. (2012). The permeation of dynorphin A 1-6 across the blood brain barrier and its effect on bovine brain microvessel endothelial cell monolayer permeability. Peptides 38:414–17
   PubMedGoogle Scholar
• Sugano K, Kansy M, Artursson P, et al. (2010). Coexistence of passive and carrier-mediated processes in drug transport. Nat Rev Drug Discov 9:597–614
   PubMed Web of Science ®Google Scholar
• Sun YL, Chen JJ, Kumar P, et al. (2013). Reversal of MRP7 (ABCC10)-mediated multidrug resistance by tariquidar. PLoS ONE 8:e55576. doi:10.1371/journal.pone.0055576
   PubMed Web of Science ®Google Scholar
• Troutman MD, Thakker DR. (2003). Novel experimental parameters to quantify the modulation of absorptive and secretory transport of compounds by P-glycoprotein in cell culture models of intestinal epithelium. Pharm Res 20:1210–24
   PubMed Web of Science ®Google Scholar
• Tsaioun K, Bottlaender M, Mabondzo A; the Alzheimer's Drug Discovery Foundation. (2009). ADDME – Avoiding Drug Development Mistakes Early: central nervous system drug discovery perspective. BMC Neurol 9:S1. doi:10.1186/1471-2377-9-S1-S1
   Google Scholar
• Tsuji A, Terasaki T, Takabatake Y, et al. (1992). P-glycoprotein as the drug efflux pump in primary cultured bovine brain capillary endothelial cells. Life Sci 51:1427–37
   PubMed Web of Science ®Google Scholar
• Tsuji A, Tamai I. (1997). Blood-brain barrier function of P-glycoprotein. Adv Drug Deliv Rev 25:287–98
   Web of Science ®Google Scholar
• Varma MV, Sateesh K, Panchagnula R. (2005). Functional role of P-glycoprotein in limiting intestinal absorption of drugs: contribution of passive permeability to P-glycoprotein mediated efflux transport. Mol Pharm 2:12–21
   PubMed Web of Science ®Google Scholar
• Vellonen KS, Honkakoski P, Urtti A. (2004). Substrates and inhibitors of efflux proteins interfere with the MTT assay in cells and may lead to underestimation of drug toxicity. Eur J Pharm Sci 23:181–8
   PubMed Web of Science ®Google Scholar
• Wallstab A, Koester M, Böhme M, Keppler D. (1999). Selective inhibition of MDR1 P-glycoprotein-mediated transport by the acridone carboxamide derivative GG918. Br J Cancer 79:1053–60
   PubMed Web of Science ®Google Scholar
• Zhang Y, Schuetz JD, Elmquist WF, Miller DW. (2004). Plasma membrane localization of multidrug resistance-associated protein homologs in brain capillary endothelial cells. J Pharmacol Exp Ther 311:449–55
   PubMed Web of Science ®Google Scholar
• Zhang Y, Li CS, Ye Y, et al. (2006). Porcine brain microvessel endothelial cells as an in vitro model to predict in vivo blood-brain barrier permeability. Drug Metab Dispos 34:1935–43
   PubMed Web of Science ®Google Scholar