A functional in vitro model of rat blood-brain barrier for molecular analysis of efflux transporters

Brain Research

Volumn 1150, Issue 1, 2007, Pages 1-13

  Perrière, Nicolas ^a,b,c,d,e,f   Yousif, Salah ^d,e   Cazaubon, Sylvie ^a,b,c,d   Chaverot, Nathalie ^a,b,c,d   Bourasset, Fanchon ^d,e   Cisternino, Salvatore ^d,e   Declèves, Xavier ^d,e   Hori, Satoko ^g   Terasaki, Tetsuya ^g   Deli, Maria ^h   Scherrmann, Jean Michel ^d,e   Temsamani, Jamal ^f   Roux, Françoise ^d,e   Couraud, Pierre Olivier ^a,b,c,d  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e HÔPITAL FERNAND WIDAL   (France)

^f Synt:em   (France)

^g TOHOKU UNIVERSITY   (Japan)

^h INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

ABC transporters; Blood brain barrier; Functional polarity; In vitro model; In vitro in vivo correlation; Tight junction

Indexed keywords

CLAUDIN 3; CLAUDIN 5; CYCLIC AMP; DAUNORUBICIN; GLYCOPROTEIN P; HYDROCORTISONE; MULTIDRUG RESISTANCE PROTEIN 3; MULTIDRUG RESISTANCE PROTEIN 4; OCCLUDIN; PROTEIN BCRP; PROTEIN OATP 2; PROTEIN ZO1; PUROMYCIN; RHODAMINE 123; SUCROSE; UNCLASSIFIED DRUG; VALSPODAR; VERLUKAST;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL CULTURE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIPOPHILICITY; MOLECULAR BIOLOGY; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CAPILLARY PERMEABILITY; CELLS, CULTURED; COCULTURE TECHNIQUES; CYCLIC AMP; ELECTRIC IMPEDANCE; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HYDROCORTISONE; MEMBRANE PROTEINS; MODELS, ANIMAL; PROTEIN TRANSPORT; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

RATTUS; RODENTIA;

EID: 34248173562     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2007.02.091     Document Type: Article

References (51)

1. Abbott N.J., Hughes C.C., Revest P.A., and Greenwood J. Development and characterisation of a rat brain capillary endothelial culture: towards an in vitro blood-brain barrier. J. Cell Sci. 10 M M3 Pt. 1 (1992) 23-37
2. Allen J.D., van Loevezijn A., Lakhai J.M., van der Valk M., van Tellingen O., Reid G., Schellens J.H., Koomen G.J., and Schinkel A.H. Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol. Cancer Ther. 1 (2002) 417-425
3. Barrand M.A., Robertson K.J., and von Weikersthal S.F. Comparisons of P-glycoprotein expression in isolated rat brain microvessels and in primary cultures of endothelial cells derived from microvasculature of rat brain, epididymal fat pad and from aorta. FEBS Lett. 374 (1995) 179-183
4. Beaulieu E., Demeule M., Ghitescu L., and Beliveau R. P-glycoprotein is strongly expressed in the luminal membranes of the endothelium of blood vessels in the brain. Biochem. J. 326 (1997) 539-544
5. Begley D.J. ABC transporters and the blood-brain barrier. Curr. Pharm. Des. 10 (2004) 1295-1312
6. Berezowski V., Landry C., Dehouck M.P., Cecchelli R., and Fenart L. Contribution of glial cells and pericytes to the mRNA profiles of P-glycoprotein and multidrug resistance-associated proteins in an in vitro model of the blood-brain barrier. Brain Res. 1018 (2004) 1-9
7. Booher J., and Sensenbrenner M. Growth and cultivation of dissociated neurons and glial cells from embryonic chick, rat and human brain in flask cultures. Neurobiology 2 (1972) 97-105
8. Bowman P.D., Ennis S.R., Rarey K.E., Betz A.L., and Goldstein G.W. Brain microvessel endothelial cells in tissue culture: a model for study of blood-brain barrier permeability. Ann. Neurol. 14 (1983) 396-402
9. Calabria A.R., Weidenfeller C., Jones A.R., de Vries H.E., and Shusta E.V. Puromycin-purified rat brain microvascular endothelial cell cultures exhibit improved barrier properties in response to glucocorticoid induction. J. Neurochem. 97 (2006) 922-933
10. Cecchelli R., Dehouck B., Descamps L., Fenart L., Buee-Scherrer V.V., Duhem C., Lundquist S., Rentfel M., Torpier G., and Dehouck M.P. In vitro model for evaluating drug transport across the blood-brain barrier. Adv. Drug Deliv. Rev. 36 (1999) 165-178
11. Cisternino S., Mercier C., Bourasset F., Roux F., and Scherrmann J.M. Expression, up-regulation, and transport activity of the multidrug-resistance protein Abcg2 at the mouse blood-brain barrier. Cancer Res. 64 (2004) 3296-3301
12. Cooray H.C., Blackmore C.G., Maskell L., and Bartrand M.A. Localisation of breast cancer resistance protein in microvessel endothelium of human brain. NeuroReport 13 (2002) 2059-2063
13. Copin J.C., and Gasche Y. Morphologie et physiologie de la barrière hématoencéphalique. Ann. Fr. Anesth. Réanim. 22 (2003) 202-214
14. Cordon-Cardo C., O'Brien J.P., Casals D., Rittman-Grauer L., Biedler J.L., Melamed M.R., and Bertino J.R. Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 695-698
15. Cucullo L., Hallene K., Dini G., Dal Toso R., and Janigro D. Glycerophosphoinositol and dexamethasone improve transendothelial electrical resistance in an in vitro study of the blood-brain barrier. Brain Res. 997 (2004) 147-151
16. Dagenais C., Rousselle C., Pollack G.M., and Scherrmann J.-M. Development of an in situ mouse brain perfusion model an its application to mdr1a P-glycoprotein deficient mice. J. Cereb. Blood Flow Metab. 20 (2000) 381-386
17. Eisenblatter T., Huwel S., and Galla H.J. Characterisation of the brain multidrug resistance protein (BMDP/ABCG2/BCRP) expressed at the blood-brain barrier. Brain Res. 971 (2003) 221-231
18. Gaillard P.J., van der Sandt I.C., Voorwinden L.H., Vu D., Nielsen J.L., de Boer A.G., and Breimer D.D. Astrocytes increase the functional expression of P-glycoprotein in an in vitro model of the blood-brain barrier. Pharm. Res. 17 (2000) 1198-1205
19. Gaillard P.J., Voorwinden L.H., Nielsen J.L., Ivanov A., Atsumi R., Engman H., Ringbom C., de Boer A.G., and Breimer D.D. Establishment and functional characterization of an in vitro model of the blood-brain barrier, comprising a co-culture of brain capillary endothelial cells and astrocytes. Eur. J. Pharm. Sci. 12 (2001) 215-222
20. Garberg P., Ball M., Borg N., Cecchelli R., Fenart L., Hurst R.D., Lindmark T., Mabondzo A., Nilsson J.E., Raub T.J., Stanimirovic D., Terasaki T., Oberg J.O., and Osterberg T. In vitro models for the blood-brain barrier. Toxicol. In Vitro 3 (2005) 299-334
21. Ge S., Song L., and Pachter J.S. Where is the blood-brain barrier... really?. J. Neurosci. Res. 79 (2005) 421-427
22. Gekeler V., Ise W., Sanders K.H., Ulrich W.R., and Beck J. The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208 (1995) 345-352
23. Gumbleton M., and Audus K.L. 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 (2001) 1681-1698
24. Gutmann H., Torok M., Fricker G., Huwyler J., Beglinger C., and Drewe J. Modulation of multidrug resistance protein expression in porcine brain capillary endothelial cells in vitro. Drug Metab. Dispos. 27 (1999) 937-941
25. Hayer-Zillgen M., Bruss M., and Bonisch H. Expression and pharmacological profile of the human organic cation transporters hOCT1, hOCT2 and hOCT3. Br. J. Pharmacol. 136 (2002) 829-836
26. Hoheisel D., Nitz T., Franke H., Wegener J., Hakvoort A., Tilling T., and Galla H.J. Hydrocortisone reinforces the blood-brain properties in a serum free cell culture system. Biochem. Biophys. Res. Commun. 247 (1998) 312-315
27. Hori S., Ohtsuki S., Tachikawa M., Kimura N., Kondo T., Watanabe M., Nakashima E., and Terasaki T. Functional expression of rat ABCG2 on the luminal side of brain capillaries and its enhancement by astrocyte-derived soluble factor(s). J. Neurochem. 90 (2004) 526-536
28. Jette L., Murphy G.F., Leclerc J.M., and Beliveau R. Interaction of drugs with P-glycoprotein in brain capillaries. Biochem. Pharmacol. 50 (1995) 1701-1709
29. Joo F. Endothelial cells of the brain and other organ systems: some similarities and differences. Prog. Neurobiol. 48 (1996) 255-273
30. Konig J., Seithel A., Gradhand U., and Fromm M.F. Pharmacogenomics of human OATP transporters. Naunyn-Schmiedeberg's Arch. Pharmacol. 372 (2006) 432-443
31. Lampugnani M.G., Resnati M., Raiteri M., Pigott R., Pisacane A., Houen G., Ruco L.P., and Dejana E. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118 (1992) 1511-1522
32. Marie-Claire C., Courtin C., Roques B.P., and Noble F. Cytoskeletal genes regulation by chronic morphine treatment in rat striatum. Neuropsychopharmacology 29 (2004) 2208-2215
33. Mayer U., Wagenaar E., Dorobek B., Beijnen J.H., Borst P., and Schinkel A.H. Full blockade of intestinal P-glycoprotein and extensive inhibition of blood-brain barrier P-glycoprotein by oral treatment of mice with PSC833. J. Clin. Invest. 100 (1997) 2430-2436
34. Megard I., Garrigues A., Orlowski S., Jorajuria S., Clayette P., Ezan E., and Mabondzo A. A co-culture-based model of human blood-brain barrier: application to active transport of indinavir and in vivo-in vitro correlation. Brain Res. 927 (2002) 153-167
35. Ohtsuki S., Sato S., Yamaguchi H., Kamoi M., Asashima T., and Terasaki T. Exogenous expression of claudin-5 induces barrier properties in cultured rat brain capillary endothelial cells. J. Cell. Physiol. 210 (2007) 81-86
36. Perrière N., Demeuse P., Garcia E., Regina A., Debray M., Andreux J.P., Couvreur P., Scherrmann J.M., Temsamani J., Couraud P.O., Deli M.A., and Roux F. Puromycin-based purification of rat brain capillary endothelial cell cultures. Effect on the expression of blood-brain barrier-specific properties. J. Neurochem. 93 (2005) 279-289
37. Regina A., Koman A., Piciotti M., El Hafny B., Center M.S., Bergmann R., Couraud P.-O., and Roux F. Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells. J. Neurochem. 71 (1998) 705-715
38. Regina A., Romero I.A., Greenwood J., Adamson P., Bourre J.M., Couraud P.O., and Roux F. Dexamethasone regulation of P-glycoprotein activity in an immortalized rat brain endothelial cell line, GPNT. J. Neurochem. 73 (1999) 1954-1963
39. Regina A., Morchoisne S., Borson N.D., McCall A.L., Drewes L.R., and Roux F. Factor(s) released by glucose-deprived astrocytes enhance glucose transporter expression and activity in rat brain endothelial cells. Biochim. Biophys. Acta 1540 (2001) 233-242
40. Romero I.A., Radewicz K., Jubin E., Michel C.C., Greenwood J., Couraud P.O., and Adamson P. Changes in cytoskeletal and tight junctional proteins correlate with decreased permeability induced by dexamethasone in cultured rat brain endothelial cells. Neurosci. Lett. 344 (2003) 112-116
41. Roux F.S., Mokni R., Hughes C.C., Clouet P.M., Lefauconnier J.M., and Bourre J.M. Lipid synthesis by rat brain microvessel endothelial cells in tissue culture. J. Neuropathol. Exp. Neurol. 48 (1989) 437-447
42. Rubin L.L., Hall D.E., Porter S., Bartbu K., Cannon C., Horner H.C., Janatpour M., Liaw C.W., Manning K., Morales J., Tanner L.I., Tomaselli K.J., et al. A cell-culture model of the blood-brain barrier. J. Cell Biol. 115 (1991) 1725-1735
43. Scherrmann J.M. Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin. Drug Metab. Toxicol. 1 (2005) 233-246
44. Schinkel A.H., Smit J.J., van Tellingen O., Beijnen J.H., Wagenaar E., van Deemter L., Mol C.A., van der Valk M.A., Robanus-Maandag E.C., te Riele H.P., et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77 (1994) 491-502
45. Seetharaman S., Barrand M.A., Maskell L., and Scheper R.J. Multidrug resistance-related transport proteins in isolated human brain microvessels and in cells cultured from these isolates. J. Neurochem. 70 (1998) 1151-1159
46. Szabo C.A., Deli M.A., Ngo T.K., and Joo F. Production of pure primary rat cerebral endothelial cell culture: a comparison of different methods. Neurobiology (Bp) 5 (1997) 1-16
47. Terasaki T., Ohtsuki S., Hori S., Takanaga H., Nakashima E., and Hosoya K. New approaches to in vitro models of blood-brain barrier drug transport. Drug Discov. Today 8 (2003) 944-954
48. van der Sandt I.C., Blom-Roosemalen M.C., de Boer A.G., and Breimer D.D. Specificity of doxorubicin versus rhodamine-123 in assessing P-glycoprotein functionality in the LLC-PK1, LLC-PK1:MDR1 and Caco-2 cell lines. Eur. J. Pharm. Sci. 11 (2000) 207-214
49. Weksler B.B., Subileau E.A., Perrière N., Charneau P., Holloway K., Leveque M., Tricoire-Leignel H., Nicotra A., Bourdoulous S., Turowski P., Male D.K., Roux F., Greenwood J., Romero I.A., and Couraud P.O. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 19 (2005) 1872-1874
50. Wolburg H., Wolburg-Buchholz K., Kraus J., Rascher-Eggstein G., Liebner S., Hamm S., Duffner F., Grote E.H., Risau W., and Engelhardt B. Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme. Acta Neuropathol. 105 (2003) 586-592
51. Zhang Y., Schuetz J.D., Elmquist W.F., and Miller D.W. Plasma membrane localization of multidrug resistance-associated protein homologs in brain capillary endothelial cells. J. Pharmacol. Exp. Ther. 311 (2004) 449-455