Paracellular tightness and claudin-5 expression is increased in the bcec/astrocyte blood-brain barrier model by increasing media buffer capacity during growth

AAPS Journal

Volumn 12, Issue 4, 2010, Pages 759-770

  Helms, Hans Christian ^a   Waagepetersen, Helle Sønderby ^a   Nielsen, Carsten Uhd ^a   Brodin, Birger ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Blood brain barrier; Buffer capacity; Drug delivery; In vitro model; Tight junction regulation

Indexed keywords

BUFFER; CLAUDIN 1; CLAUDIN 5; JUNCTIONAL ADHESION MOLECULE A; MESSENGER RNA; OCCLUDIN; PROTEIN ZO1;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CAPILLARY ENDOTHELIUM; CELL CULTURE; CELL DIFFERENTIATION; COCULTURE; CONTROLLED STUDY; COW; ENDOTHELIUM CELL; IN VITRO STUDY; NEWBORN; NONHUMAN; PH; PROTEIN EXPRESSION; RAT;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; CATTLE; COCULTURE TECHNIQUES; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; RATS; TIGHT JUNCTIONS;

EID: 78649646826     PISSN: 15507416     EISSN: None     Source Type: Journal    
DOI: 10.1208/s12248-010-9237-6     Document Type: Article

References (43)

1. TS Reese MJ Karnovsky 1967 Fine structural localization of a blood-brain barrier to exogenous peroxidase J Cell Biol 34 1 207 17 1:CAS:528: DyaF2sXksFWksr4%3D 10.1083/jcb.34.1.207 6033532
2. C Crone SP Olesen 1982 Electrical resistance of brain microvascular endothelium Brain Res 241 1 49 55 1:STN:280:DyaL383lvVehtQ%3D%3D 10.1016/0006-8993(82)91227-6 6980688 (Pubitemid 12124928)
3. MW Brightman TS Reese 1969 Junctions between intimately apposed cell membranes in the vertebrate brain J Cell Biol 40 3 648 77 1:STN:280: DyaF1M7hsVCitw%3D%3D 10.1083/jcb.40.3.648 5765759
4. AG de Boer PJ Gaillard DD Breimer 1999 The transference of results between blood-brain barrier cell culture systems Eur J Pharm Sci 8 1 1 4 10.1016/S0928-0987(99)00003-2 10072472 (Pubitemid 29117262)
5. RS el-Bacha A Minn 1999 Drug metabolizing enzymes in cerebrovascular endothelial cells afford a metabolic protection to the brain Cell Mol Biol (Noisy-le-grand) 45 1 15 23 1:CAS:528:DyaK1MXitVChtro%3D
6. R Cecchelli V Berezowski S Lundquist M Culot M Renftel MP Dehouck, et al. 2007 Modelling of the blood-brain barrier in drug discovery and development Nat Rev Drug Discov 6 8 650 61 1:CAS:528:DC%2BD2sXotl2qtLc%3D 10.1038/nrd2368 17667956 (Pubitemid 47202487)
7. MA Deli CS Abraham Y Kataoka M Niwa 2005 Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology Cell Mol Neurobiol 25 1 59 127 10.1007/s10571-004-1377-8 15962509 (Pubitemid 40558585)
8. AC Taylor 1962 Responses of cells to pH changes in the medium J Cell Biol 15 201 9 1:CAS:528:DyaF3sXmvVCisA%3D%3D 10.1083/jcb.15.2.201 13993539
9. CG Mackenzie JB Mackenzie P Beck 1961 The effect of pH on growth, protein synthesis, and lipid-rich particles of cultured mammalian cells J Biophys Biochem Cytol 9 141 56 1:CAS:528:DyaF3MXhtVKitb4%3D 10.1083/jcb.9.1.141 13764902
10. 2 incubators cause periodic changes in cell morphology Exp Cell Res 213 2 391 7 1:CAS:528:DyaK2cXlt12htb4%3D 10.1006/excr.1994.1214 8050495 (Pubitemid 24259484)
11. PA Dickinson JP Evans SJ Farr IW Kellaway TP Appelqvist AC Hann, et al. 1996 Putrescine uptake by alveolar epithelial cell monolayers exhibiting differing transepithelial electrical resistances J Pharm Sci 85 10 1112 6 1:CAS:528:DyaK28XlsVyhur8%3D 10.1021/js9504898 8897281 (Pubitemid 26338928)
12. PJ Gaillard AG de Boer 2008 2B-Trans technology: targeted drug delivery across the blood-brain barrier Methods Mol Biol 437 161 75 1:CAS:528: DC%2BD1cXkslOhtbw%3D 10.1007/978-1-59745-210-6-8 18369968
13. M Boveri V Berezowski A Price S Slupek AM Lenfant C Benaud, et al. 2005 Induction of blood-brain barrier properties in cultured brain capillary endothelial cells: comparison between primary glial cells and C6 cell line Glia 51 3 187 98 10.1002/glia.20189 15800928 (Pubitemid 41297425)
14. M Culot S Lundquist D Vanuxeem S Nion C Landry Y Delplace, et al. 2008 An in vitro blood-brain barrier model for high throughput (HTS) toxicological screening Toxicol In Vitro 22 3 799 811 1:CAS:528:DC%2BD1cXjtVemtLo%3D 10.1016/j.tiv.2007.12.016 18280105
15. H Franke HJ Galla CT Beuckmann 1999 An improved low-permeability in vitro-model of the blood-brain barrier: transport studies on retinoids, sucrose, haloperidol, caffeine and mannitol Brain Res 818 1 65 71 1:CAS:528: DyaK1MXmtVCrtg%3D%3D 10.1016/S0006-8993(98)01282-7 9914438 (Pubitemid 29227284)
16. PJ Gaillard LH Voorwinden JL Nielsen A Ivanov R Atsumi H Engman, et al. 2001 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 3 215 22 1:CAS:528:DC%2BD3cXoslGhtLs%3D 10.1016/S0928-0987(00)00123-8 11113640
17. S Nakagawa MA Deli S Nakao M Honda K Hayashi R Nakaoke, et al. 2007 Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells Cell Mol Neurobiol 27 6 687 94 1:CAS:528:DC%2BD2sXhtVOisb3F 10.1007/s10571-007-9195-4 17823866 (Pubitemid 47476613)
18. D Hoheisel T Nitz H Franke J Wegener A Hakvoort T Tilling, et al. 1998 Hydrocortisone reinforces the blood-brain properties in a serum free cell culture system Biochem Biophys Res Commun 247 2 312 5 1:STN:280: DyaK1czjsFGnuw%3D%3D 10.1006/bbrc.1997.8051 9679029 (Pubitemid 28419944)
19. KCK Malina I Cooper VI Teichberg 2009 Closing the gap between the in-vivo and in-vitro blood-brain barrier tightness Brain Res 1284 12 21 10.1016/j.brainres.2009.05.072
20. D Bratlid WJ Cashore W Oh 1984 Effect of acidosis on bilirubin deposition in rat brain Pediatrics 73 4 431 4 1:CAS:528:DyaL2cXktVGjsL4%3D 6709423
21. Z Nagy M Szabo I Huttner 1985 Blood-brain barrier impairment by low pH buffer perfusion via the internal carotid artery in rat Acta Neuropathol 68 2 160 3 1:STN:280:DyaL28%2Fntlejuw%3D%3D 10.1007/BF00688639 4072623 (Pubitemid 16242143)
22. M Asai K Takeuchi M Saotome T Urushida H Katoh H Satoh, et al. 2009 Extracellular acidosis suppresses endothelial function by inhibiting store-operated Ca2+ entry via non-selective cation channels Cardiovasc Res 83 1 97 105 1:CAS:528:DC%2BD1MXntlGhtL0%3D 10.1093/cvr/cvp105 19351743
23. Gueffroy DE, editor. Buffers a guide for preparation and use of buffers in biological systems. San Diego: Calbiochem-Novabiochem Corporation; 1993.
24. BM Altura A Carella BT Altura 1980 Adverse effects of Tris. HEPES and MOPS buffers on contractile responses of arterial and venous smooth muscle induced by prostaglandins Prostaglandins Med 5 2 123 30 1:CAS:528: DyaL3cXmtlWlu7s%3D 10.1016/0161-4630(80)90099-3 6251495
25. IH Lelong G Rebel 1998 pH drift of "physiological buffers" and culture media used for cell incubation during in vitro studies J Pharmacol Toxicol Methods 39 4 203 10 1:CAS:528:DyaK1MXhtlanu74%3D 10.1016/S1056-8719(98) 00019-7 9845299 (Pubitemid 28535162)
26. Luo S, Pal D, Shah SJ, Kwatra D, Paturi KD, Mitra AK. Effect of HEPES buffer on the uptake and transport of P-glycoprotein substrates and large neutral amino acids. Mol Pharm. Apr 5;7(2):412-20
27. CA Poole HC Reilly MH Flint 1982 The adverse effects of HEPES, TES, and BES zwitterion buffers on the ultrastructure of cultured chick embryo epiphyseal chondrocytes In Vitro 18 9 755 65 1:CAS:528:DyaL38XmtFajsL4%3D 10.1007/BF02796499 6293964
28. K Morita H Sasaki M Furuse S Tsukita 1999 Endothelial claudin: Claudin-5/TMVCF constitutes tight junction strands in endothelial cells J Cell Biol 147 1 185 94 1:CAS:528:DyaK1MXmsVCltbk%3D 10.1083/jcb.147.1.185 10508865 (Pubitemid 30211806)
29. T Nitta M Hata S Gotoh Y Seo H Sasaki N Hashimoto, et al. 2003 Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice J Cell Biol 161 3 653 60 1:CAS:528:DC%2BD3sXjvVeqsb8%3D 10.1083/jcb.200302070 12743111 (Pubitemid 36578587)
30. Z Chen M Zandonatti D Jakubowski HS Fox 1998 Brain capillary endothelial cells express MBEC1, a protein that is related to the Clostridium perfringens enterotoxin receptors Lab Investig 78 3 353 63 1:CAS:528:DyaK1cXit1arsrw%3D 9520948
31. T Ishizaki H Chiba T Kojima M Fujibe T Soma H Miyajima, et al. 2003 Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain-barrier endothelial cells via protein kinase A-dependent and -independent pathways Exp Cell Res 290 2 275 88 1:CAS:528:DC%2BD3sXotVCitLs%3D 10.1016/S0014-4827(03)00354-9 14567987 (Pubitemid 37272172)
32. T Koto K Takubo S Ishida H Shinoda M Inoue K Tsubota, et al. 2007 Hypoxia disrupts the barrier function of neural blood vessels through changes in the expression of claudin-5 in endothelial cells Am J Pathol 170 4 1389 97 1:CAS:528:DC%2BD2sXkvFymtr0%3D 10.2353/ajpath.2007.060693 17392177 (Pubitemid 47339345)
33. T Soma H Chiba Y Kato-Mori T Wada T Yamashita T Kojima, et al. 2004 Thr(207) of claudin-5 is involved in size-selective loosening of the endothelial barrier by cyclic AMP Exp Cell Res 300 1 202 12 1:CAS:528:DC%2BD2cXnslKrs70%3D 10.1016/j.yexcr.2004.07.012 15383327 (Pubitemid 39286229)
34. S Liebner A Fischmann G Rascher F Duffner EH Grote H Kalbacher, et al. 2000 Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme Acta Neuropathol 100 3 323 31 1:CAS:528:DC%2BD3cXmtFSnu74%3D 10.1007/s004010000180 10965803
35. S Amasheh T Schmidt M Mahn P Florian J Mankertz S Tavalali, et al. 2005 Contribution of claudin-5 to barrier properties in tight junctions of epithelial cells Cell Tissue Res 321 1 89 96 1:CAS:528:DC%2BD2MXlvVynsbk%3D 10.1007/s00441-005-1101-0 16158492 (Pubitemid 40984842)
36. H Wen DD Watry MC Marcondes HS Fox 2004 Selective decrease in paracellular conductance of tight junctions: role of the first extracellular domain of claudin-5 Mol Cell Biol 24 19 8408 17 1:CAS:528:DC%2BD2cXnvVakt74%3D 10.1128/MCB.24.19.8408-8417.2004 15367662 (Pubitemid 39245063)
37. G Krause L Winkler SL Mueller RF Haseloff J Piontek IE Blasig 2008 Structure and function of claudins Biochim Biophys Acta 1778 3 631 45 1:CAS:528:DC%2BD1cXjtVSqt70%3D 18036336
38. CJ Favre M Mancuso K Maas JW McLean P Baluk DM McDonald 2003 Expression of genes involved in vascular development and angiogenesis in endothelial cells of adult lung Am J Physiol Heart Circ Physiol 285 5 H1917 38 1:CAS:528:DC%2BD3sXpt1Olu7Y%3D 12842817
39. F Wang B Daugherty LL Keise Z Wei JP Foley RC Savani, et al. 2003 Heterogeneity of claudin expression by alveolar epithelial cells Am J Respir Cell Mol Biol 29 1 62 70 1:CAS:528:DC%2BD3sXlt1KqsLg%3D 10.1165/rcmb.2002-0180OC 12600828 (Pubitemid 36783317)
40. M Gumbleton KL Audus 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 11 1681 98 1:CAS:528:DC%2BD3MXosVKltrw%3D 10.1002/jps.1119 11745727 (Pubitemid 33062590)
41. P Garberg M Ball N Borg R Cecchelli L Fenart RD Hurst, et al. 2005 In vitro models for the blood-brain barrier Toxicol In Vitro 19 3 299 334 1:CAS:528:DC%2BD2MXhtlCrurg%3D 10.1016/j.tiv.2004.06.011 15713540 (Pubitemid 40248750)
42. AR Calabria EV Shusta 2008 A genomic comparison of in vivo and in vitro brain microvascular endothelial cells J Cereb Blood Flow Metab 28 1 135 48 1:CAS:528:DC%2BD1cXhtF2rug%3D%3D 10.1038/sj.jcbfm.9600518 17565361
43. R Lyck N Ruderisch AG Moll O Steiner CD Cohen B Engelhardt, et al. 2009 Culture-induced changes in blood-brain barrier transcriptome: implications for amino-acid transporters in vivo J Cereb Blood Flow Metab 29 9 1491 502 1:CAS:528:DC%2BD1MXhtVKnurrF 10.1038/jcbfm.2009.72 19491922