Primary porcine brain microvascular endothelial cells: Biochemical and functional characterisation as a model for drug transport and targeting

References

• Abbott NJ. Astrocyte-endothelial interactions and blood–brain barrier permeability. J Anat 2002; 200(6)629–638
   PubMed Web of Science ®Google Scholar
• Abbruscato TJ, Davis TP. Combination of hypoxia/aglycemia compromises in vitro blood–brain barrier integrity. J Pharmacol Exp Ther 1999; 289(2)668–675
   PubMed Web of Science ®Google Scholar
• Aoki T, Nomura R, Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999; 253(2)629–636
   PubMed Web of Science ®Google Scholar
• Arvanitis DN, Wang H, Bagshaw RD, Callahan JW, Boggs JM. Membrane-associated estrogen receptor and caveolin-1 are present in central nervous system myelin and oligodendrocyte plasma membranes. J Neurosci Res 2004; 75(5)603–613
   PubMed Web of Science ®Google Scholar
• Begley DJ. ABC transporters and the blood–brain barrier. Curr Pharm Des 2004; 10(12)1295–1312
   PubMed Web of Science ®Google Scholar
• Boado RJ, Pardridge WM. Glucose deprivation and hypoxia increase the expression of the GLUT1 glucose transporter via a specific mRNA cis-acting regulatory element. J Neurochem 2002; 80(3)552–554
   PubMed Web of Science ®Google Scholar
• Boado RJ, Tsukamoto H, Pardridge WM. Evidence for translational control elements within the 5′-untranslated region of GLUT1 glucose transporter mRNA. J Neurochem 1996; 67(4)1335–1343
   PubMed Web of Science ®Google Scholar
• Boado RJ, Li JY, Nagaya M, Zhang C, Pardridge WM. Selective expression of the large neutral amino acid transporter at the blood–brain barrier. Proc Natl Acad Sci USA 1999; 96(21)12079–12084
   PubMed Web of Science ®Google Scholar
• Broadwell RD. Transcytosis of macromolecules through the blood–brain barrier: A cell biological perspective and critical appraisal. Acta Neuropathol (Berl) 1989; 79(2)117–128
   PubMed Web of Science ®Google Scholar
• Campbell L, Hollins AJ, Al-Eid A, Newman GR, von RC, Gumbleton M. Caveolin-1 expression and caveolae biogenesis during cell transdifferentiation in lung alveolar epithelial primary cultures. Biochem Biophys Res Commun 1999; 262(3)744–751
   PubMed Web of Science ®Google Scholar
• Chishty M, Reichel A, Begley DJ, Abbott NJ. Glial induction of blood–brain barrier-like l-system amino acid transport in the ECV304 cell line. Glia 2002; 39(2)99–104
   PubMed Web of Science ®Google Scholar
• Coomber BL, Stewart PA. Morphometric analysis of CNS microvascular endothelium. Microvasc Res 1985; 30(1)99–115
   PubMed Web of Science ®Google Scholar
• Duelli R, Enerson BE, Gerhart DZ, Drewes LR. Expression of large amino acid transporter LAT1 in rat brain endothelium. J Cereb Blood Flow Metab 2000; 20(11)1557–1562
   PubMed Web of Science ®Google Scholar
• Ek CJ, Dziegielewska KM, Stolp H, Saunders NR. Functional effectiveness of the blood–brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 2006; 496(1)13–26
   PubMed Web of Science ®Google Scholar
• Engelhardt B. Development of the blood–brain barrier. Cell Tissue Res 2003; 314(1)119–129
   PubMed Web of Science ®Google Scholar
• Forster C, Silwedel C, Golenhofen N, Burek M, Kietz S, Mankertz J, Drenckhahn D. Occludin as direct target for glucocorticoid-induced improvement of blood–brain barrier properties in a murine in vitro system. J Physiol 565 2005; 2: 475–486
   Google Scholar
• Franke H, Galla HJ, Beuckmann CT. An improved low-permeability in vitro-model of the blood–brain barrier: Transport studies on retinoids, sucrose, haloperidol, caffeine and mannitol. Brain Res 1999; 818(1)65–71
   PubMed Web of Science ®Google Scholar
• Franke H, Galla H, Beuckmann CT. 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 2000; 5(3)248–256
   PubMedGoogle Scholar
• Garberg P, Ball M, Borg N, Cecchelli R, Fenart L, Hurst RD, Lindmark T, Mabondzo A, Nilsson JE, Raub TJ, Stanimirovic D, Terasaki T, Oberg JO, Osterberg T. In vitro models for the blood–brain barrier. Toxicol in Vitro 2005; 19(3)299–334
   PubMed Web of Science ®Google Scholar
• Goh LB, Spears KJ, Yao D, Ayrton A, Morgan P, Roland WC, Friedberg T. Endogenous drug transporters in in vitro and in vivo models for the prediction of drug disposition in man. Biochem Pharmacol 2002; 64(11)1569–1578
   PubMed Web of Science ®Google Scholar
• Gumbleton M, Abulrob AG, Campbell L. Caveolae: An alternative membrane transport compartment. Pharm Res 2000; 17(9)1035–1048
   PubMed Web of Science ®Google Scholar
• Gumbleton M, Audus KL. 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 2001; 90(11)1681–1698
   PubMed Web of Science ®Google Scholar
• Hoffmann K, Gastens AM, Volk HA, Loscher W. Expression of the multidrug transporter MRP2 in the blood–brain barrier after pilocarpine-induced seizures in rats. Epilepsy Res 2006; 69(1)1–14
   PubMed Web of Science ®Google Scholar
• Hoheisel D, Nitz T, Franke H, Wegener J, Hakvoort A, Tilling T, Galla HJ. Hydrocortisone reinforces the blood–brain barrier properties in a serum free cell culture system. Biochem Biophys Res Commun 1998; 244(1)312–316
   PubMed Web of Science ®Google Scholar
• Iqbal J, Pompolo S, Murakami T, Grouzmann E, Sakurai T, Meister B, Clarke IJ. Immunohistochemical characterization of localization of long-form leptin receptor (OB-Rb) in neurochemically defined cells in the ovine hypothalamus. Brain Res 2001; 920(1–2)55–64
   PubMed Web of Science ®Google Scholar
• 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 2000; 879(1–2)115–121
   PubMed Web of Science ®Google Scholar
• 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 2001; 53(4)497–503
   PubMed Web of Science ®Google Scholar
• Lee WJ, Peterson DR, Sukowski EJ, Hawkins RA. Glucose transport by isolated plasma membranes of the bovine blood–brain barrier. Am J Physiol 1997; 1(5 Pt 1)C1552–C1557
   Google Scholar
• Merino B, ez-Fernandez C, Ruiz-Gayo M, Somoza B. Choroid plexus epithelial cells co-express the long and short form of the leptin receptor. Neurosci Lett 2006; 393(2–3)269–272
   PubMed Web of Science ®Google Scholar
• Moos T, Mollgard K. Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages. Neuropathol Appl Neurobiol 1993; 19(2)120–127
   PubMed Web of Science ®Google Scholar
• Newman GR, Campbell L, von RC, 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 1999; 295(1)111–120
   PubMed Web of Science ®Google Scholar
• Ohtsuki S. New aspects of the blood–brain barrier transporters; its physiological roles in the central nervous system. Biol Pharm Bull 2004; 27(10)1489–1496
   PubMed Web of Science ®Google Scholar
• Omidi Y, Campbell L, Barar J, Connell D, Akhtar S, Gumbleton M. 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 Res 2003; 990(1–2)95–112
   PubMed Web of Science ®Google Scholar
• Pinkofsky HB, Dwyer DS, Bradley RJ. The inhibition of GLUT1 glucose transport and cytochalasin B binding activity by tricyclic antidepressants. Life Sci 2000; 66(3)271–278
   PubMed Web of Science ®Google Scholar
• Raub TJ, Kuentzel SL, Sawada GA. Permeability of bovine brain microvessel endothelial cells in vitro: Barrier tightening by a factor released from astroglioma cells. Exp Cell Res 1992; 199(2)330–340
   PubMed Web of Science ®Google Scholar
• Regina A, Roux F, Revest PA. Glucose transport in immortalized rat brain capillary endothelial cells in vitro: Transport activity and GLUT1 expression. Biochim Biophys Acta 1997; 1335(1–2)135–143
   PubMed Web of Science ®Google Scholar
• Rist RJ, Romero IA, Chan MW, Couraud PO, Roux F, Abbott NJ. F-actin cytoskeleton and sucrose permeability of immortalised rat brain microvascular endothelial cell monolayers: Effects of cyclic AMP and astrocytic factors. Brain Res 1997; 768(1–2)10–18
   PubMed Web of Science ®Google Scholar
• Rossier G, Meier C, Bauch C, Summa V, Sordat B, Verrey F, Kuhn LC. LAT2, a new basolateral 4F2hc/CD98-associated amino acid transporter of kidney and intestine. J Biol Chem 1999; 274(49)34948–34954
   PubMed Web of Science ®Google Scholar
• Schinkel AH, Wagenaar E, van DL, Mol CA, Borst P. Absence of the mdr1a p-Glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporin A. J Clin Invest 1995; 96(4)1698–1705
   PubMed Web of Science ®Google Scholar
• Siawrys G, Przala J, Kaminski T, Smolinska N, Gajewska A, Kochman K, Skowronski M, Staszkiewicz J. Long form leptin receptor mRNA expression in the hypothalamus and pituitary during early pregnancy in the pig. Neuro Endocrinol Lett 2005; 26(4)305–309
   PubMed Web of Science ®Google Scholar
• Smith MW, Gumbleton M. Endocytosis at the blood–brain barrier: From basic understanding to drug delivery strategies. J Drug Target 2006; 14(4)191–214
   PubMed Web of Science ®Google Scholar
• Sobue K, Yamamoto N, Yoneda K, Hodgson ME, Yamashiro K, 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 1999; 35(2)155–164
   PubMed Web of Science ®Google Scholar
• Stewart PA. Endothelial vesicles in the blood–brain barrier: Are they related to permeability?. Cell Mol Neurobiol 2000; 20(2)149–163
   PubMed Web of Science ®Google Scholar
• Stewart PA, Hayakawa K, Hayakawa E, Farrell CL, Del Maestro RF. A quantitative study of blood–brain barrier permeability ultrastructure in a new rat glioma model. Acta Neuropathol (Berl) 1985; 67(1–2)96–102
   PubMed Web of Science ®Google Scholar
• Stewart PA, Magliocco M, Hayakawa K, Farrell CL, Del Maestro RF, Girvin J, Kaufmann JC, Vinters HV, Gilbert J. A quantitative analysis of blood–brain barrier ultrastructure in the aging human. Microvasc Res 1987; 33(2)270–282
   PubMed Web of Science ®Google Scholar
• Stewart PA, Farrell CR, Farrell CL, Hayakawa E. Horseradish peroxidase retention and washout in blood–brain barrier lesions. J Neurosci Methods 1992; 41(1)75–84
   PubMed Web of Science ®Google Scholar
• Su Y, Sinko PJ. Drug delivery across the blood–brain barrier: Why is it difficult? How to measure and improve it?. Expert Opin Drug Deliv 2006; 3(3)419–435
   PubMed Web of Science ®Google Scholar
• Tilling T, Korte D, Hoheisel D, Galla HJ. Basement membrane proteins influence brain capillary endothelial barrier function in vitro. J Neurochem 1998; 71(3)1151–1157
   PubMed Web of Science ®Google Scholar
• Verrey F, Meier C, Rossier G, Kuhn LC. Glycoprotein-associated amino acid exchangers: Broadening the range of transport specificity. Pflugers Arch 2000; 440(4)503–512
   PubMed Web of Science ®Google Scholar
• Virgintino D, Robertson D, Errede M, Benagiano V, Tauer U, Roncali L, Bertossi M. Expression of caveolin-1 in human brain microvessels. Neuroscience 2002; 115(1)145–152
   PubMed Web of Science ®Google Scholar
• Wagner CA, Lang F, Broer S. Function and structure of heterodimeric amino acid transporters. Am J Physiol Cell Physiol 2001; 281(4)C1077–C1093
   PubMed Web of Science ®Google Scholar
• Zhang Y, Schuetz JD, Elmquist WF, Miller DW. Plasma membrane localization of multidrug resistance-associated protein homologs in brain capillary endothelial cells. J Pharmacol Exp Ther 2004; 311(2)449–455
   PubMed Web of Science ®Google Scholar
• Zhou R, Vander Heiden MG, Rudin CM. Genotoxic exposure is associated with alterations in glucose uptake and metabolism. Cancer Res 2002; 62(12)3515–3520
   PubMed Web of Science ®Google Scholar