Evaluation of the immortalised mouse brain capillary endothelial cell line, b.End3, as an in vitro blood-brain barrier model for drug uptake and transport studies

Brain Research

Volumn 990, Issue 1-2, 2003, Pages 95-112

  Omidi, Yadollah ^a,b   Campbell, Lee ^a   Barar, Jaleh ^a   Connell, David ^a   Akhtar, Saeed ^c   Gumbleton, Mark ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b TABRIZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

B.End3; Blood brain barrier; Endocytosis; In vitro model; Permeability; Transport

Indexed keywords

AMINO ACID TRANSPORTER; CAVEOLIN 1; CLATHRIN; CLAUDIN; CLAUDIN 1; DYNAMIN; FLOTILLIN; GLUCOSE; LEUCINE; NUCLEOSIDE; OCCLUDIN; PHENYLALANINE; PROPRANOLOL; PROTEIN; PROTEIN ZO1; RHODAMINE 123; SODIUM; SUCROSE; SYNAPTOBREVIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CAPILLARY ENDOTHELIUM; CELL CULTURE; CELL ISOLATION; CELL LINE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; DRUG TRANSPORT; DRUG UPTAKE; ELECTRIC RESISTANCE; EVALUATION; IN VITRO STUDY; MACROGLIA; MICHAELIS CONSTANT; MODEL; MORPHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYOMA VIRUS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA TRANSCRIPTION; TIGHT JUNCTION;

EID: 0141894132     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(03)03443-7     Document Type: Article

References (71)

1. Abbruscato T.J., Davis T.P. Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity. J. Pharmacol. Exp. Ther. 289:1999;668-675.
2. Abulrob A.G., Gumbleton M. Transport of phosphatidylcholine in MDR3-negative epithelial cell lines via drug-induced MDR1 P-glycoprotein. Biochem. Biophys. Res. Commun. 262:1999;121-126.
3. Adson A., Raub T.J., Burton P.S., Barsuhn C.L., Hilgers A.R., Audus K.L., Ho N.F. Quantitative approaches to delineate paracellular diffusion in cultured epithelial cell monolayers. J. Pharm. Sci. 83:1994;1529-1536.
4. Asaba H., Hosoya K., Takanaga H., Ohtsuki S., Tamura E., Takizawa T., Terasaki T. Blood-brain barrier is involved in the efflux transport of a neuroactive steroid, dehydroepiandrosterone sulfate, via organic anion transporting polypeptide 2. J. Neurochem. 75:2000;1907-1916.
5. Bacon J.A., Katofiasc M.A., Chernet E., Phebus L.A., Ackermann B.L., Scism J.L. Development of a cell-based moderate throughput model of the blood-brain barrier. Drug Metabol. Rev. 32:2000;180.
6. Begley D.J., Lechardeur D., Chen Z.D., Rollinson C., Bardoul M., Roux F., Scherman D., Abbott N.J. Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4. J. Neurochem. 67:1996;988-995.
7. Bhardwaj R.K., Glaeser H., Becquemont L., Klotz U., Gupta S.K., Fromm M.F. Piperine, a major constituent of black pepper, inhibits human P-glycoprotein and CYP3A4. J. Pharmacol. Exp. Ther. 302:2002;645-650.
8. Boado R.J., Pardridge W.M. Glucose deprivation causes post transcriptional enhancement of brain capillary endothelial glucose transporter gene expression via GLUT1 mRNA stabilization. J. Neurochem. 60:1993;2290-2296.
9. Boado R.J., Tsukamoto H., Pardridge W.M. Evidence for translational control elements within the 5′-untranslated region of GLUT1 glucose transporter mRNA. J. Neurochem. 67:1996;1335-1343.
10. Boado R.J., Li Y., Nagaya M., Zhang C., Pardridge W.M. Selective expression of the large neutral amino acid transporter at the blood-brain barrier. Proc. Natl. Acad. Sci. U. S. A. 96:1999;12079-12084.
11. Broer A., Friedrich B., Wagner C.A., Fillon S., Ganapathy V., Lang F., Broer S. Association of 4F2hc with light chains LAT1, LAT2 or y+LAT2 requires different domains. Biochem. J. 355:2001;725-731.
12. Campbell L., Hollins A.J., Al Eid A., Newman G.R., von Ruhland C., Gumbleton M. Caveolin-1 expression and caveolae biogenesis during cell transdifferentiation in lung alveolar epithelial primary cultures. Biochem. Biophys. Res. Commun. 262:1999;744-751.
13. Chishty M., Reichel A., Begley D.J., Abbott N.J. Glial induction of blood-brain barrier-like L-system amino acid transport in the ECV304 cell line. Glia. 39:2002;99-104.
14. Duelli R., Enerson B.E., Gerhart D.Z., Drewes L.R. Expression of large amino acid transporter LAT1 in rat brain endothelium. J. Cereb. Blood Flow Metab. 20:2000;1557-1562.
15. El Hafny B., Cano N., Piciotti M., Regina A., Scherrmann J.M., Roux F. Role of P-glycoprotein in colchicine and vinblastine cellular kinetics in an immortalized rat brain microvessel endothelial cell line. Biochem. Pharmacol. 53:1997;1735-1742.
16. Fraga S., Serrao M.P., Soares-da-Silva P. L-type amino acid transporters in two intestinal epithelial cell lines function as exchangers with neutral amino acids. J. Nutr. 132:2002;733-738.
17. Franke H., Galla H.J., Beuckmann C.T. An improved low-permeability in vitro-model of the blood-brain barrier: transport studies on retinoids, sucrose, haloperidol, caffeine and mannitol. Brain Res. 818:1999;65-71.
18. Franke H., Galla H.J., Beuckmann C.T. Primary cultures of brain microvessel endothelial cells: a valid and flexible model to study drug transport through the blood-brain barrier in vitro. Brain Res. Brain Res. Protoc. 5:2000;248-256.
19. Gao B., Stieger B., Noe B., Fritschy J.-M., Mier P.J. Localisation of the organic anion transporting polypeptide 2 (Oatp2) in capillary endothelium and choroid plexus epithelium of rat brain. J. Histochem. Cytochem. 47:1999;1255-1263.
20. Gumbleton M., 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.
21. Gumbleton M., Abulrob A.G., Campbell L. Caveolae: an alternative membrane transport compartment. Pharm. Res. 17:2000;1035-1048.
22. Hallmann R., Savigni D.L., Morgan E.H., Baker E. Characterization of iron uptake from transferrin by murine endothelial cells. Endothelium. 7:2000;135-147.
23. Hoheisel D., Nitz T., Franke H., Wegener J., Hakvoort A., Tilling T., Galla H.J. Hydrocortisone reinforces the blood-brain barrier properties in a serum free cell culture system [corrected and republished in Biochem Biophys Res Commun 1998 Jun 18;247 (2), 312-5]. Biochem. Biophys. Res. Commun. 244:1998;312-316.
24. Hurst R.D., Clark J.B. Alterations in transendothelial electrical resistance by vasoactive agonists and cyclic AMP in a blood-brain barrier model system. Neurochem. Res. 23:1998;149-154.
25. Hurtenbach U., Boggemeyer E., Stehle T., Museteanu C., Del Pozo E., Simon M.M. Prednisolone reduces experimental arthritis and inflammatory tissue destruction in SCID mice infected with Borrelia burgdorferi. Int. J. Immunopharmacol. 18:1996;281-288.
26. Huwyler J., Froidevaux S., Roux F., Eberle A.N. Characterization of transferrin receptor in an immortalized cell line of rat brain endothelial cells, RBE4. J. Recept. Signal. Transduct. Res. 19:1999;729-739.
27. Kageyama T., Nakamura M., Matsuo A., Yamasaki Y., Takakura Y., Hashida M., Kanai Y., Naito M., Tsuruo T., Minato N., Shimohama S. The 4F2hc/LAT1 complex transports L-DOPA across the blood-brain barrier. Brain Res. 879:2000;115-121.
28. Kanai Y., Segawa H., Miyamoto K., Uchino H., Takeda E., Endou H. Expression cloning and characterization of a transporter for large neutral amino acids activated by the heavy chain of 4F2 antigen (CD98). J. Biol. Chem. 273:1998;23629-23632.
29. Kerns E.H. High throughput physicochemical profiling for drug discovery. J. Pharm. Sci. 90:2001;1838-1858.
30. Kido Y., Tamai I., Okamoto M., Suzuki F., Tsuji A. Functional clarification of MCT1-mediated transport of monocarboxylic acids at the blood-brain barrier using in vitro cultured cells and in vivo BUI studies. Pharm. Res. 17:2000;55-62.
31. Kido Y., Tamai I., Uchino H., Suzuki F., Sai Y., Tsuji A. Molecular and functional identification of large neutral amino acid transporters LAT1 and LAT2 and their pharmacological relevance at the blood-brain barrier. J. Pharm. Pharmacol. 53:2001;497-503.
32. Lagrange P., Romero I.A., Minn A., Revest P.A. Transendothelial permeability changes induced by free radicals in an in vitro model of the blood-brain barrier. Free Radic. Biol. Med. 27:1999;667-672.
33. Lee J.S., Paull L., Alvarez M., Hose C., Monks A., Grever M., Fojo A.T., Bates S.E. Rhodamine efflux patterns predict P-glycoprotein substrates in the National Cancer Institute drug screen. Mol. Pharmacol. 46:1994;627-638.
34. Lee W.J., Peterson D.R., Sukowski E.J., Hawkins R.A. Glucose transport by isolated plasma membranes of the bovine blood-brain barrier. Am. J. Physiol. 272:1997;C1552-C1557.
35. Mann G.E., Yudilevich D.L., Sobrevia L. Regulation of amino acid and glucose transporters in endothelial and smooth muscle cells. Physiol. Rev. 83:2003;183-252.
36. Muruganandam A., Herx L.M., Monette R., Durkin J.P., Stanimirovic D.B. Development of immortalized human cerebromicrovascular endothelial cell line as an in vitro model of the human blood-brain barrier. FASEB J. 11:1997;1187-1197.
37. Negri L., Lattanzi R., Tabacco F., Scolaro B., Rocchi R. Glycodermorphins: opioid peptides with potent and prolonged analgesic activity and enhanced blood-brain barrier penetration. Br. J. Pharmacol. 124:1998;1516-1522.
38. Newman G.R., Campbell L., von Ruhl C., Jasani B., Gumbleton M. Caveolin and its cellular and subcellular immunolocalisation in lung alveolar epithelium: implications for alveolar epithelial type I cell function. Cell Tissue Res. 295:1999;111-120.
39. Oh P., McIntosh D.P., Schnitzer J.E. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J. Cell Biol. 141:1998;101-114.
40. Pinkofsky H.B., Dwyer D.S., Bradley R.J. The inhibition of GLUT1 glucose transport and cytochalasin B binding activity by tricyclic antidepressants. Life Sci. 66:2000;271-278.
41. Prasad P.D., Wang H., Huang W., Kekuda R., Rajan D.P., Leibach F.H., Ganapathy V. Human LAT1, a subunit of system L amino acid transporter: molecular cloning and transport function. Biochem. Biophys. Res. Commun. 255:1999;283-288.
42. Raub T.J., Kuentzel S.L., Sawada G.A. Permeability of bovine brain microvessel endothelial cells in vitro: barrier tightening by a factor released from astroglioma cells. Exp. Cell Res. 199:1992;330-340.
43. Reardon P.M., Audus K.L. Applications of primary cultures of brain microvessel endothelial cell monolayers in the study of vasoactive peptide interaction with the blood-brain barrier. S.T.P. Pharm. Sci. 3:1993;63-68.
44. Regina A., Roux F., Revest P.A. Glucose transport in immortalized rat brain capillary endothelial cells in vitro: transport activity and GLUT1 expression. Biochim. Biophys. Acta. 1335:1997;135-143.
45. Regina A., Koman A., Piciotti M., El Hafny B., Center M.S., Bergmann R., Couraud P.O., Roux F. Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells. J. Neurochem. 71:1998;705-715.
46. Regina A., Romero I.A., Greenwood J., Adamson P., Bourre J.M., Couraud P.O., Roux F. Dexamethasone regulation of P-glycoprotein activity in an immortalized rat brain endothelial cell line, GPNT. J. Neurochem. 73:1999;1954-1963.
47. Reichel A., Abbott N.J., Begley D.J. Evaluation of the RBE4 cell line to explore carrier-mediated drug delivery to the CNS via the L-system amino acid transporter at the blood-brain barrier. J. Drug Target. 10:2002;277-283.
48. Rist R.J., Romero I.A., Chan M.W., Couraud P.O., Roux F., Abbott N.J. F-actin cytoskeleton and sucrose permeability of immortalised rat brain microvascular endothelial cell monolayers: effects of cyclic AMP and astrocytic factors. Brain Res. 768:1997;10-18.
49. Rossier G., Meier C., Bauch C., Summa V., Sordat B., Verrey F., Kuhn L.C. LAT2, a new basolateral 4F2hc/CD98-associated amino acid transporter of kidney and intestine. J. Biol. Chem. 274:1999;34948-34954.
50. Roux F., Durieu-Trautmann O., Chaverot N., Claire M., Mailly P., Bourre J.M., Strosberg A.D., Couraud P.O. Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J. Cell Physiol. 159:1994;101-113.
51. Rubin L.L., Hall D.E., Porter S., Barbu K., Cannon C., Horner H.C., Janatpour M., Liaw C.W., Manning K., Morales J. A cell culture model of the blood-brain barrier. J. Cell Biol. 115:1991;1725-1735.
52. Schinkel A.H. P-Glycoprotein, a gatekeeper in the blood-brain barrier. Adv. Drug Deliv. Rev. 36:1999;179-194.
53. Schinkel A.H., Wagenaar E., van Deemter L., Mol C.A., Borst P. Absence of the mdr1a P-Glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporin A. J. Clin. Invest. 96:1995;1698-1705.
54. Sobue K., Yamamoto N., Yoneda K., Hodgson M.E., Yamashiro N., Tsuruoka N., Tsuda T., Katsuya H., Miura Y., Asai K., Kato T. Induction of blood-brain barrier properties in immortalized bovine brain endothelial cells by astrocytic factors. Neurosci. Res. 35:1999;155-164.
55. Soga N., Connolly J.O., Chellaiah M., Kawamura J., Hruska K.A. Rac regulates vascular endothelial growth factor stimulated motility. Cell Commun. Adhes. 8:2001;1-13.
56. Stephens R.H., O'Neill C.A., Warhurst A., Carlson G.L., Rowland M., Warhurst G. Kinetic profiling of P-glycoprotein-mediated drug efflux in rat and human intestinal epithelia. J. Pharmacol. Exp. Ther. 296:2001;584-591.
57. Stewart P.A. Endothelial vesicles in the blood-brain barrier: are they related to permeability? Cell Mol. Neurobiol. 20:2000;149-163.
58. Tan K.H., Dobie M.S., Felix R.A., Hurst R.D., Barrand M.A. A comparison of the induction of immortalized endothelial cell impermeability by astrocytes. NeuroReport. 12:2001;1329-1334.
59. Tatsuta T., Naito M., Oh-hara T., Sugawara I., Tsuruo T. Functional involvement of P-glycoprotein in blood-brain barrier. J. Biol. Chem. 267:1992;20383-20391.
60. Tilling T., Korte D., Hoheisel D., Galla H.J. Basement membrane proteins influence brain capillary endothelial barrier function in vitro. J. Neurochem. 71:1998;1151-1157.
61. Uchino H., Kanai Y., Kim D.K., Wempe M.F., Chairoungdua A., Morimoto E., Anders M.W., Endou H. Transport of amino acid-related compounds mediated by L-type amino acid transporter 1 (LAT1): Insights into the mechanisms of substrate recognition. Mol. Pharmacol. 61:2002;729-737.
62. Van Dam E.M., Stoorvogel W. Dynamin-dependent transferrin receptor recycling by endosome-derived clathrin-coated vesicles. Mol. Biol. Cell. 13:2002;169-182.
63. van Montfoort J.E., Schmid T.E., Adler I.D., Meier P.J., Hagenbuch B. Functional characterisation of the mouse organic anion transporting polypeptide2. Biochim. Biophys. Acta. 1564:2002;183-188.
64. Verrey F., Meier C., Rossier G., Kuhn L.C. Glycoprotein-associated amino acid exchangers: broadening the range of transport specificity. Pflugers Arch. 440:2000;503-512.
65. Virgintino D., Robertson D., Errede M., Benagiano V., Girolamo F., Maiorano E., Roncali L., Bertossi M. Expression of P-glycoprotein in human cerebral cortex microvessels. J. Histochem. Cytochem. 50:2002;1671-1676.
66. Volonte D., Galbiati F., Li S., Nishiyama K., Okamoto T., Lisanti M.P. Flotillins/caveolins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J. Biol. Chem. 274:1999;12702-12709.
67. Wagner C.A., Lang F., Broer S. Function and structure of heterodimeric amino acid transporters. Am. J. Physiol. 281:2001;C1077-C1093.
68. Williams R.L., Risau W., Zerwes H.G., Drexler H., Aguzzi A., Wagner E.F. Endothelioma cells expressing the polyoma middle T oncogene induce hemangiomas by host cell recruitment. Cell. 57:1989;1053-1063.
69. Yanagida O., Kanai Y., Chairoungdua A., Kim D.K., Segawa H., Nii T., Cha S.H., Matsuo H., Fukushima J., Fukasawa Y., Tani Y., Taketani Y., Uchino H., Kim J.Y., Inatomi J., Okayasu I., Miyamoto K., Takeda E., Goya T., Endou H. Human L-type amino acid transporter 1 (LAT1): characterization of function and expression in tumor cell lines. Biochim. Biophys. Acta. 1514:2001;291-302.
70. Yoder E.J. Modifications in astrocyte morphology and calcium signaling induced by a brain capillary endothelial cell line. Glia. 38:2002;137-145.
71. Zhou R., Vander Heiden M.G., Rudin C.M. Genotoxic exposure is associated with alterations in glucose uptake and metabolism. Cancer Res. 62:2002;3515-3520.