Expression of tight junction and drug efflux transporter proteins in an in vitro model of human blood-brain barrier

Frontiers in Psychiatry

Volumn 3, Issue MAY, 2012, Pages

  Cioni, Chiara ^a   Turlizzi, Elisa ^b   Zanelli, Ugo ^b   Oliveri, Giuseppe ^c   Annunziata, Pasquale ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b Siena Biotech SpA   (Italy)

^c Neurosurgery Unit   (Italy)

Author keywords

Blood brain barrier; Brain endothelium; Cell culture; Drug transporters; Glia; Tight junctions

Indexed keywords

CLAUDIN 5; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; OCCLUDIN; ORGANIC ANION TRANSPORTER 1; ORGANIC ANION TRANSPORTER 3; TIGHT JUNCTION PROTEIN; ZONULA OCCLUDENS PROTEIN;

ADULT; AGED; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CELL VIABILITY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; FEMALE; GENE; GLIA CELL; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; ORGANIC ANION TRANSPORTING POLYPEPTIDE 1 GENE; ORGANIC ANION TRANSPORTING POLYPEPTIDE 3 GENE; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; UPREGULATION;

EID: 84866882990     PISSN: None     EISSN: 16640640     Source Type: Journal    
DOI: 10.3389/fpsyt.2012.00047     Document Type: Article

References (43)

1. Abbott, N. J. (2000). Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol. 20, 131-147.
2. Annunziata, P. (2003). Blood-brain barrier changes during invasion of the central nervous system by HIV-1. Old and new insights into the mechanism. J. Neurol. 250, 901-906.
3. Annunziata, P., Cioni, C., Moschini, E, Riccucci, A., and Guazzi, G. C. (1995). Serum anti-brain endothe-lium antibodies and cognitive assessment in patients with Binswanger's encephalopathy. J. Neurol Sci. 128, 96-102.
4. Annunziata, P., Cioni, C., Toneatto, S., and Paccagnini, E. (1998). HIV-1 gp 120 increases the permeability of rat brain endothe-lium cultures by a mechanism involving substance P. AIDS 12, 2377-2385.
5. Arthur, F. E., Shivers, R. R., and Bowmann, P. D. (1987). Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Brain Res. 433, 155-159.
6. Ballabh, P., Braun, A., and Nedergaard, M. (2004). The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis.16, 1-13.
7. Bell, R. D., and Zlokovic, B. V. (2009). Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease. Acta Neuropathol. 118, 103-113.
8. Beuckmann, C., Hellwig, S., and Galla, H. J. (1995). Induction of the blood/brain- barrier-associated enzyme alkaline phosphatase in endothelial cells from cerebral capillaries is mediated via cAMP. Eur. J. Biochem. 229, 641-644.
9. Biegel, D., Spencer, D. D., and Pachter, J. S. (1995). Isolation and culture of human brain microvessel endothelial cells for the study of blood-brain barrier properties in vitro. Brain Res. 692, 183-189.
10. Blecharz, K. G., Haghikia, A., Stasi-olek, M., Kruse, N., Drenckhahn, D., Gold, R., Roewer, N., Chan, A., and Förster, C. Y. (2010). Gluco-corticoid effects on endothelial barrier function in the murine brain endothelial cell line cEND incubated with sera from patients with multiple sclerosis. Mult. Scler. 16, 293-302.
11. Bradbury, M. W. (1985). The blood-brain barrier. Transport across the cerebral endothelium. Circ. Res. 57, 213-222.
12. Bradbury, M. W. (1993). The blood-brain barrier. Exp. Physiol. 78, 453-472.
13. Brunet, J. F., Pellerin, L., Magistretti, P., and Villemure, J. G. (2003). Cryop-reservation of human brain tissue allowing timely production of viable adult human brain cells for autol-ogous transplantation. Cryobiology 47, 179-183.
14. Cecchelli, R., Dehouck, B., Descamps, L., Fenart, L., Bluée-Scherrer, V. V., Duhem, C., Lundquist, S., Rentfel, M., Torpier, G., and Dehouck, M. P. (1999). In vitro model for evaluating drug transport across the blood-brain barrier. Adv. Drug Deliv. Rev. 36, 165-178.
15. Cioni, C., Cantalupo, L., Turlizzi, E., Zanelli, U., and Annunziata, P. (2009). Expression of tight junction and drug efflux transporter proteins in a model of human blood-brain barrier. J. Neurol. 256(SUPPL 2), S190-S191.
16. Cordon-Cardo, C., O'Brien, J. P., Casals, D., Rittman-Grauer, L., Biedler, J. L., Melamed, M. R., and Bertino, J. R. (1989). Multidrug-resistance gene (P-glycoprotein) is expressed by endothelial cells at blood-brain barrier sites. Proc. Natl. Acad. Sci. U.S.A. 86, 695-698.
17. Culot, M., Lundquist, S., Vanuxeem, D., Nion, S., Landry, C., Delplace, Y., Dehouck, M. P., Berezowski, V., Fenart, L., and Cecchielli, R. (2008). An in vitro blood-brain barrier model for high throughput (HTS) toxicological screening. Toxi-col. In vitro 22, 799-811.
18. De Lange, E. C. M. (2004). Potential role of ABC transporters as a detoxification system at the blood-CSF barrier. Adv. DrugDeliv. Rev. 56, 1793-1809.
19. Dehouk, M. P., Meresse, S., Delorme, P., Fruchart, J. C., and Cecchelli, R. (1990). An easier, reproducible and mass-production method to study the blood-brain barrier in vitro. J. Neurochem. 54, 1798-1801.
20. Farshori, P., and Kachar, B. (1999). Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells. J. Membr. Biol. 170, 147-156.
21. Gao, B., Stieger, B., Noé, B., Fritschy, J. M., and Meier, P. J. (1999). Localization of the organic anion transporting polypeptide 2 (oatp2) in capillary endothelium and choroid plexus epithelium of rat brain. J. His-tochem. Cytochem. 47, 1255-1264.
22. Goldstein, G. W., and Betz, A. L. (1986). The blood-brain barrier. Sci. Am. 255, 74-83.
23. Hjelmeland, A. B., Lathia, J. D., Sathorn-sumetee, S., and Rich, J. N. (2011). Twisted tango: brain tumor neu-rovascular interactions. Nat. Neu-rosci. 14, 1375-1381.
24. Hollò, Z., Homolya, L., Davis, C. W., and Sarkadi, B. (1994). Calcein accumulation as a fluorometric functional assay of the multidrug transporter. Biochim. Biophys. Acta 1191, 384-388.
25. Janzer, R. C., and Raff, M. C. (1987). Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325, 253-257.
26. Kalback, W., Esh, C., Castaño, E. M., Rahman, A., Kokjohn, T., Luehrs, D. C., Sue, L., Cisneros, R., Gerber, E, Richardson, C., Bohrmann, B., Walker, D. G., Beach, T. G., and Roher, A. E. (2004). Atherosclerosis, vascular amyloidosis and brain hypoperfusion in the pathogene-sis of sporadic Alzheimer's disease. Neurol Res. 26, 525-539.
27. Kermode, A. G., Thompson, A. J., Tofts, P., MacManus, D. G., Kendall, B. E., Kingsley, D. P., Mosely, I. F., Rudge, P., and McDonald, W. I. (1990). Breakdown of the blood-brain barrier precedes symptoms and other MRI signs of new lesions in multiple sclerosis. Pathogenetic and clinical implications. Brain 113, 1477-1489.
28. Kuo, Y. C., and Lu, C. H. (2011). Effect of human astrocytes on the characteristics of human brain- microvascular endothelial cells in the blood-brain barrier. Colloids Surf. B Biointerfaces 86, 225-231.
29. Kusahara, H., He, Z., Nagata, Y., Nozaki, Y., Ito, T., Masuda, H., Meyer, P. J., Abe, T., and Sugiyama, Y (2003). Expression and functional involvement of organic anion transporting polypeptide subtype 3 (Slc21a7) in rat choroids plexus. Pharm. Res. 20, 720-727.
30. Megard, I., Garrigues, A., Orlowski, S., Jorajuria, S., Clayette, P., Ezan, E., and Mabondzo, A. (2002). 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, 153-167.
31. Meyer, J., Mischeck, U., Veyhl, M., Henzel, K.,andGalla, H.J.(1990).Blood-brain barrier characteristic enzymatic properties in cultured brain capillary endothelial cells. Brain Res. 514, 305-309.
32. Meyer, J., Rauh, J., and Galla, H. J. (1991). The susceptibility of cerebral endothelial cells to astroglial induction of blood-brain barrier enzymes depends on their proliferative state. J. Neurochem. 57,1971-1977.
33. Minagar, A., and Alexander, J.S. (2003). Blood-brain barrier disruption in multiple sclerosis. Mult. Scler. 9, 540-549.
34. Mitic, L. L., Van Itallie, C. M., and Anderson, J. M. (2000). Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins. Am. J. Physiol. Gastrointest. LiverPhysiol. 279, 250-254.
35. Morita, K., Sasaki, H., Furuse, M., and Tsukita, S. (1999). Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J. Cell Biol. 147, 185-194.
36. Mrsulja, B. B., Mrsulja, B. J, Fujimoto, T., Klatzo, I., and Spatz, M. (1976). Isolation of brain capillaries: a simplified technique. Brain Res. 110, 361-365.
37. Perrière, N., Yousif, S., Cazaubon, S., Chaverot, N., Bourasset, F., Cis-ternino, S., Declèves, X., Hori, S., Terasaki, T., Deli, M., Scherrmann, J. M., Temsamani, J., Roux, F., and Couraud, P. O. (2007). A functional in vitro model of rat blood-brain barrier for molecular analysis of efflux transporters. Brain Res. 1150, 1-13.
38. Rubin, L. L., Hall, D. F., Porter, S., Barbu, K., Cannon, C., Horner, H. C., Janat-pour, M., Liaw, C. W., Manning, K., Morales, J., Tanner, L. I., Tomaselli, K. J., and Bard, E (1991). A cell culture model for the blood-brain barrier.J. Cell Biol. 115, 1725-1735.
39. Siddharthan, V., Kim, Y. V., Liu, S., and Kim, K. S. (2007). Human astrocytes/astrocyte-conditioned medium and shear stress enhance the barrier properties of human brain microvascular endothelial cells. Brain Res. 1147, 39-50.
40. Smith, T. W., De Girolami, U., Hénin, D., Bolgert, F., and Hauw, J. J. (1990). Human immunodeficiency virus (HIV) leuken-cephalopathy and the microcircula-tion. J. Neuropathol Exp. Neurol. 49, 357-370.
41. Teifel, M., and Friedl, P. (1996). Establishement of the permanent microvascular endothelial cell line PBMEC/C1-2 from porcine brains. Exp. Cell Res. 228, 50-57.
42. Weksler, B. B., Subileau, A., Perrière, N., Charneau, P., Holloway, K., Lev-eque, M., Tricoire-Leignel, H., Nico-tra,A.,Bourdoulous,S.,Turowski, P., Male, D. K., Roux, F., Greenwood, J., Romero, I. A., and Couraud, P. O. (2005). Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 19, 1872-1874.
43. Willott, E., Balda, M. S., Heintzelman, M., Jameson, B., and Anderson, J. M. (1992). Localization and differential expression of two isoforms of tight junction protein ZO-1. Am. J. Physiol. 262, C1119-C1124.