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

Xenobiotica

Volumn 44, Issue 3, 2014, Pages 283-294

  Hakkarainen, Jenni J ^a   Rilla, Kirsi ^a   Suhonen, Marjukka ^a,b   Ruponen, Marika ^a   Forsberg, Markus M ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b Kuopio Innovation Ltd   (Finland)

Author keywords

Bidirectional transport; Blood brain barrier; Drug transport; Efflux

Indexed keywords

CYCLOSPORIN A; DIGOXIN; MULTIDRUG RESISTANCE PROTEIN; OCCLUDIN; PACLITAXEL; PROGESTERONE; PROTEIN ZO1; VERAPAMIL; VINBLASTINE; VON WILLEBRAND FACTOR; XENOBIOTIC AGENT;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN BLOOD VESSEL; CALCEIN-AM ASSAY; CATTLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG PENETRATION; ENDOTHELIUM CELL; EVALUATION STUDY; IN VITRO STUDY; MONOCULTURE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; WESTERN BLOTTING;

ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; BRAIN; CATTLE; CELLS, CULTURED; ENDOTHELIAL CELLS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROVESSELS; MODELS, BIOLOGICAL; P-GLYCOPROTEIN; PERMEABILITY;

EID: 84893604648     PISSN: 00498254     EISSN: 13665928     Source Type: Journal    
DOI: 10.3109/00498254.2013.823529     Document Type: Article

References (58)

1. 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.
2. 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.
3. 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.
4. Audus KL, Ng L, Wang W, Borchardt RT. (1996). Brain microvessel endothelial cell culture systems. Pharm Biotechnol 8:239-58.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. Chappa AK, Audus KL, Lunte SM. (2006). Characteristics of substance P transport across the blood-brain barrier. Pharm Res 23:1201-8.
12. 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.
13. Dehouck MP, Dehouck B, Schluep C, et al. (1995). Drug transport to the brain: comparison between in vitro and in vivo models of the bloodbrain barrier. Eur J Pharm Sci 3:357-65.
14. 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.
15. 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.
16. 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.
17. Eneroth A, A ° ström 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.
18. 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.
19. 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.
20. 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.
21. Garberg P, Ball M, Borg N, et al. (2005). In vitro models for the bloodbrain barrier. Toxicol in Vitro 19:299-334.
22. Giacomini KM, Huang SM, Tweedie DJ, et al. (2010). Membrane transporters in drug development. Nat Rev Drug Discov 9:215-36.
23. Gumbleton M, Audus KL. (2001). Progress and limitations in the use of in vitro cell cultures to serve as a permeability screen for the bloodbrain barrier. J Pharm Sci 90:1681-98.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Iwanaga K, Yoneda S, Hamahata Y, et al. (2011). Inhibitory effects of furanocoumarin derivatives in Kampo extract medicines on Pglycoprotein at the blood-brain barrier. Biol Pharm Bull 34:1246-51.
32. 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.
33. 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.
34. 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.
35. Lentz KA, Polli JW, Wring SA, et al. (2000). Influence of passive permeability on apparent P-glycoprotein kinetics. Pharm Res 17: 1456-60.
36. 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.
37. Martin C, Berridge G, Higgins CF, et al. (2000). Communication between multiple drug binding sites on P-glycoprotein. Mol Pharmacol 58:624-32.
38. 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.
39. 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.
40. 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.
41. 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.
42. Pardridge WM, Triguero D, Yang J, Cancilla PA. (1990). Comparison of in vitro and in vivo models of drug transcytosis through the bloodbrain barrier. J Pharmacol Exp Ther 253:884-91.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. Sun YL, Chen JJ, Kumar P, et al. (2013). Reversal of MRP7 (ABCC10)-mediated multidrug resistance by tariquidar. PLoS ONE 8:e55576.
49. doi:10.1371/journal.pone.0055576.
50. 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.
51. 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.
52. 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.
53. Tsuji A, Tamai I. (1997). Blood-brain barrier function of P-glycoprotein. Adv Drug Deliv Rev 25:287-98.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.