Artificial Blood-Brain Barriers

Blood-Brain Barriers: From Ontogeny to Artificial Interfaces

Volumn 1, Issue , 2007, Pages 375-401

  Cucullo, Luca ^a   Oby, Emily ^a   Hallene, Kerri ^a   Aumayr, Barbara ^a   Rapp, Ed ^b   Janigro, Damir ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b Cleveland Medical Devices Inc   (United States)

Author keywords

Artificial blood brain barriers; Cell culture based in vitro BBB models; Cell differentiation; Culturing blood brain barrier; Flow based in vitro BBB systems; Immobilized artificial membranes; Requirements for a good BBB model; Shear stress

Indexed keywords

BLOOD-BRAIN BARRIER;

EID: 84891035670     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527611225.ch17     Document Type: Chapter

References (95)

1. Bradbury, M.W. 1993, The blood-brain barrier, Exp. Physiol. 78, 453-472.
2. Dermietzel, R., Krause, D. 1991, Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry, Int. Rev. Cytol. 127, 57-109.
3. Rubin, L. L., Staddon, J.M. 1999, The cell biology of the blood-brain barrier, Annu. Rev. Neurosci. 22, 11-28.
4. Engelhardt, B. 2003, Development of the blood-brain barrier, Cell Tissue Res. 314, 119-129.
5. Grant, G. A., Abbott, N. J., Janigro, D. 1998, Understanding the physiology of the blood-brain barrier: in vitro models, News Physiol. Sci. 13, 287-293.
6. Grant, G. A., Janigro, D. 2004, The blood-brain barrier, in Youmans Neurological Surgery, vol. 1, ed. Winn, H.R., Saunders, Philadelphia, p. 153-174.
7. Virgintino, D., Errede, M., Robertson, D., Capobianco, C., Girolamo, F., Vimercati, A., Bertossi, M., Roncali, L. 2004, Immunolocalization of tight junction proteins in the adult and developing human brain, Histochem. Cell Biol. 122, 51-59.
8. Emmi, A., Wenzel, H.J., Schwartzkroin, P. A., Taglialatela, M., Castaldo, P., Bianchi, L., Nerbonne, J., Robertson, G. A., Janigro, D. 2000, Do glia have heart? Expression and functional role for ether-a-go-go currents in hippocampal astrocytes, J. Neurosci. 20, 3915-3925.
9. Liberto, C. M., Albrecht, P. J., Herx, L. M., Yong, V.W., Levison, S.W. 2004, Pro-regenerative properties of cytokine-activated astrocytes, J. Neurochem. 89, 1092-1100.
10. Stanness, K. A., Westrum, L. E., Fornaciari, E., Mascagni, P., Nelson, J. A., Stenglein, S. G., Myers, T., Janigro, D. 1997, Morphological and functional characterization of an in vitro blood-brain barrier model, Brain Res. 771, 329-342.
11. Mizuguchi, H., Utoguchi, N., Mayumi, T. 1997, Preparation of glial extracellular matrix: a novel method to analyze glial-endothelial cell interaction, Brain Res. Brain Res. Protocol 1, 339-343.
12. Hamm, S., Dehouck, B., Kraus, J., Wolburg-Buchholz, K., Wolburg, H., Risau, W., Cecchelli, R., Engelhardt, B., Dehouck, M.P. 2004, Astrocyte mediated modulation of blood-brain barrier permeability does not correlate with a loss of tight junction proteins from the cellular contacts, Cell Tissue Res. 315, 157-166.
13. Hori, S., Ohtsuki, S., Tachikawa, M., Kimura, N., Kondo, T., Watanabe, M., Nakashima, E., Terasaki, T. 2004, Functional expression of rat ABCG2 on the luminal side of brain capillaries and its enhancement by astrocyte-derived soluble factor(s), J. Neurochem. 90, 526-536.
14. Kramer, S. D., Schutz, Y. B., Wunderli-Allenspach, H., Abbott, N. J., Begley, D.J. 2002, Lipids in blood-brain barrier models in vitro II: influence of glial cells on lipid classes and lipid fatty acids, In Vitro Cell Dev. Biol. Anim. 38, 566-571.
15. De Boer, A. B., De Lange, E. L., Breimer, D.D. 1998, Transporters and the blood-brain barrier (BBB), Int. J. Clin. Pharmacol. Ther. 36, 14-15.
16. Hagenbuch, B., Gao, B., Meier, P. J. 2002, Transport of xenobiotics across the blood-brain barrier, News Physiol. Sci. 17, 231-234.
17. Abbott, N. J., Khan, E. U., Rollinson, C. M., Reichel, A., Janigro, D., Dombrowski, S. M., Dobbie, M.S., Begley, D. J. 2002, Drug resistance in epilepsy:the role of the blood-brain barrier, Novartis Found. Symp. 243, 38-47.
18. Cox, D.S., Scott, K. R., Gao, H., Raje, S., Eddington, N. D. 2001, Influence of multidrug resistance (MDR) proteins at the blood-brain barrier on the transport and brain distribution of enaminone anticonvulsants, J. Pharm. Sci. 90, 1540-1552.
19. Regina, A., Demeule, M., Laplante, A., Jodoin, J., Dagenais, C., Berthelet, F., Moghrabi, A., Beliveau, R. 2001, Multidrug resistance in brain tumors: roles of the blood-brain barrier, Cancer Metastasis Rev. 20, 13-25.
20. Mahar Doan, K. M., Humphreys, J. E., Webster, L. O., Wring, S. A., Shampine, L. J., Serabjit-Singh, C. J., Adkison, K. K., Polli, J.W. 2002, Passive permeability and P-glycoprotein-mediated efflux differentiate central nervous system (CNS) and non-CNS marketed drugs, J. Pharmacol. Exp. Ther. 303, 1029-1037.
21. Reichel, A., Begley, D. J. 1998, Potential of immobilized artificial membranes for predicting drug penetration across the blood-brain barrier, Pharm. Res. 15, 1270-1274.
22. Ong, S., Liu, H., Pidgeon, C. 1996, Immobilized-artificial-membrane chromatography: measurements of membrane partition coefficient and predicting drug membrane permeability, J. Chromatogr. A 728, 113-128.
23. Pidgeon, C., Ong, S., Liu, H., Qiu, X., Pidgeon, M., Dantzig, A. H., Munroe, J., Hornback, W. J., Kasher, J. S., Glunz, L. 1995, IAM chromatography: an in vitro screen for predicting drug membrane permeability, J. Med. Chem. 38, 590-594.
24. Wang, Q., Rager, J. D., Weinstein, K., Kardos, P. S., Dobson, G. L., Li, J., Hidalgo, I. J. 2005, Evaluation of the MDR-MDCK cell line as a permeability screen for the blood-brain barrier, Int. J. Pharm. 288, 349-359.
25. Reichel, A., Abbott, N. J., Begley, D. J. 2002, 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, 277-283.
26. Begley, D. J., Lechardeur, D., Chen, Z. D., Rollinson, C., Bardoul, M., Roux, F., Scherman, D., Abbott, N. J. 1996, Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4, J. Neurochem. 67, 988-995.
27. Chishty, M., Begley, D. J., Abbott, N. J., Reichel, A. 2003, Functional characterisation of nucleoside transport in rat brain endothelial cells, Neuroreport 14, 1087-1090.
28. Bendayan, R., Lee, G., Bendayan, M. 2002, Functional expression and localization of P-glycoprotein at the blood brain barrier, Microsc. Res. Tech. 57, 365-380.
29. Cestelli, A., Catania, C., D'Agostino, S., Di, L., Licata, L., Schiera, G., Pitarresi, G. L., Savettieri, G., De, C., Giandalia, G., Giannola, L. I. 2001, Functional feature of a novel model of blood brain barrier: studies on permeation of test compounds, J. Control Release 76, 139-147.
30. Regina, A., Koman, A., Piciotti, M., El Hafny, B., Center, M. S., Bergmann, R., Couraud, P. O., Roux, F. 1998, Mrp1 multidrug resistance-associated protein and P-glycoprotein expression in rat brain microvessel endothelial cells, J. Neurochem. 71, 705-715.
31. Chat, M., Bayol-Denizot, C., Suleman, G., Roux, F., Minn, A. 1998, Drug metabolizing enzyme activities and superoxide formation in primary and immortalized rat brain endothelial cells, Life Sci. 62, 151-163.
32. El Hafny, B., Cano, N., Piciotti, M., Regina, A., Scherrmann, J. M., Roux, F. 1997, Role of P-glycoprotein in colchicine and vinblastine cellular kinetics in an immortalized rat brain microvessel endothelial cell line, Biochem. Pharmacol. 53, 1735-1742.
33. Rist, R. J., Romero, I. A., Chan, M.W., Couraud, P. O., Roux, F., Abbott, N. J. 1997, F-actin cytoskeleton and sucrose permeability of immortalised rat brain microvascular endothelial cell monolayers: effects of cyclic AMP and astrocytic factors, Brain Res. 768, 10-18.
34. Desai, S.Y., Marroni, M., Cucullo, L., Krizanac-Bengez, L., Mayberg, M.R., Hossain, M.T., Grant, G. G., Janigro, D. 2002, Mechanisms of endothelial survival under shear stress, Endothelium 9, 89-102.
35. Smith, B. J., Doran, A. C., McLean, S., Tingley, F.D. III, O'Neill, B.T., Kajiji, S.M. 2001, P-glycoprotein efflux at the blood-brain barrier mediates differences in brain disposition and pharmacodynamics between two structurally related neurokinin-1 receptor antagonists, J. Pharmacol. Exp. Ther. 298, 1252-1259.
36. 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., Osterberg, T. 2005, In vitro models for the blood-brain barrier, Toxicol. In Vitro 19, 299-334.
37. Wang, Q., Rager, J. D., Weinstein, K., Kardos, P. S., Dobson, G. L., Li, J., Hidalgo, I. J. 2005, Evaluation of the MDR-MDCK cell line as a permeability screen for the blood-brain barrier, Int. J. Pharm. 288, 349-359.
38. Zhu, Z. B., Makhija, S. K., Lu, B., Wang, M., Rivera, A. A., Preuss, M., Zhou, F., Siegal, G. P., Alvarez, R. D., Curiel, D.T. 2004, Transport across a polarized monolayer of Caco-2 cells by transferrin receptor-mediated adenovirus transcytosis, Virology 325, 116-128.
39. Lohmann, C., Huwel, S., Galla, H.J. 2002, Predicting blood-brain barrier permeability of drugs: evaluation of different in vitro assays, J. Drug Target. 10, 263-276.
40. Dallaire, L., Tremblay, L., Beliveau, R. 1991, Purification and characterization of metabolically active capillaries of the blood-brain barrier, Biochem. J. 276, 745-752.
41. Biegel, D., Spencer, D. D., 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.
42. Franke, H., Galla, H., Beuckmann, C.T. 2000, 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. Protocol 5, 248-256.
43. Dombrowski, S., Desai, S., Marroni, M., Cucullo, L., Bingaman, W., Mayberg, M.R., Bengez, L., Janigro, D. 2001, Overexpression of multiple drug resistance genes in endothelial cells from patients with refractory epilepsy, Epilepsia 42, 1504-1507.
44. Marroni, M., Marchi, N., Cucullo, L., Abbott, N. J., Signorelli, K., Janigro, D. 2003, Vascular and parenchymal mechanisms in multiple drug resistance:a lesson from human epilepsy, Curr. Drug Target. 4, 297-304.
45. Berezowski, V., Landry, C., Lundquist, S., Dehouck, L., Cecchelli, R., Dehouck, M.P., Fenart, L. 2004, Transport screening of drug cocktails through an in vitro blood-brain barrier: is it a good strategy for increasing the throughput of the discovery pipeline? Pharm. Res. 21, 756-760.
46. Hori, S., Ohtsuki, S., Hosoya, K., Nakashima, E., Terasaki, T. 2004, A pericyte-derived angiopoietin-1 multimeric complex induces occludin gene expression in brain capillary endothelial cells through Tie-2 activation in vitro, J. Neurochem. 89, 503-513.
47. Hamm, S., Dehouck, B., Kraus, J., Wolburg-Buchholz, K., Wolburg, H., Risau, W., Cecchelli, R., Engelhardt, B., Dehouck, M.P. 2004, Astrocyte mediated modulation of blood-brain barrier permeability does not correlate with a loss of tight junction proteins from the cellular contacts, Cell Tissue Res. 315, 157-166.
48. Toimela, T., Maenpaa, H., Mannerstrom, M., Tahti, H. 2004, Development of an in vitro blood-brain barrier model: cytotoxicity of mercury and aluminum, Toxicol. Appl. Pharmacol. 195, 73-82.
49. Berezowski, V., Landry, C., Dehouck, M.P., Cecchelli, R., Fenart, L. 2004, 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, 1-9.
50. Grabb, P. A., Gilbert, M.R. 1995, Neoplastic and pharmacological influence on the permeability of an in vitro blood-brain barrier, J. Neurosurg. 82, 1053-1058.
51. Hoheisel, D., Nitz, T., Franke, H., Wegener, J., Hakvoort, A., Tilling, T., Galla, H.J. 1998, Hydrocortisone reinforces the blood-brain barrier properties in a serum free cell culture system, Biochem. Biophys. Res. Commun. 244, 312-316.
52. Betz, A. L., Goldstein, G.W. 1978, Polarity of the blood-brain barrier: neutral amino acid transport into isolated brain capillaries, Science 202, 225-227.
53. Betz, A. L., Firth, J. A., Goldstein, G.W. 1980, Polarity of the blood-brain barrier:distribution of enzymes between the luminal and antiluminal membranes of brain capillary endothelial cells, Brain Res. 192, 17-28.
54. Farrell, C. L., Pardridge, W.M. 1991, Blood-brain barrier glucose transporter is asymmetrically distributed on brain capillary endothelial lumenal and ablumenal membranes: an electron microscopic immunogold study, Proc. Natl Acad. Sci. USA 88, 5779-5783.
55. Pardridge, W. M., Golden, P. L., Kang, Y. S., Bickel, U. 1997, Brain microvascular and astrocyte localization of P-glycoprotein, J. Neurochem. 68, 1278-1285.
56. Cucullo, L., McAllister, M. S., Kight, K., Krizanac-Bengez, L., Marroni, M., Mayberg, M.R., Stanness, K. A., Janigro, D. 2002, A new dynamic in vitro model for the multidimensional study of astrocyte-endothelial cell interactions at the blood-brain barrier, Brain Res. 951, 243-254.
57. Ziegler, T., Nerem, R.M. 1994, Effect of flow on the process of endothelial cell division, Arterioscler. Thromb. 14, 636-643.
58. Goldstein, G.W. 1988, Endothelial cell-astrocyte interactions. A cellular model of the blood-brain barrier, Ann. NY Acad. Sci. 529, 31-39.
59. Hori, S., Ohtsuki, S., Tachikawa, M., Kimura, N., Kondo, T., Watanabe, M., Nakashima, E., Terasaki, T. 2004, Functional expression of rat ABCG2 on the luminal side of brain capillaries and its enhancement by astrocyte-derived soluble factor(s), J. Neurochem. 90, 526-536.
60. Cucullo, L., Hallene, K., Dini, G., Dal Toso, R., Janigro, D. 2004, Glycerophosphoinositol and dexamethasone improve transendothelial electrical resistance in an in vitro study of the blood-brain barrier, Brain Res. 997, 147-151.
61. Cucullo, L., Marchi, N., Marroni, M., Fazio, V., Namura, S., Janigro, D. 2003, Blood-brain barrier damage induces release of α2-macroglobulin, Mol. Cell Proteomics 2, 234-241.
62. Terasaki, T., Ohtsuki, S., Hori, S., Takanaga, H., Nakashima, E., Hosoya, K. 2003, New approaches to in vitro models of blood-brain barrier drug transport, Drug Discov. Today 8, 944-954.
63. Salvetti, F., Cecchetti, P., Janigro, D., Lucacchini, A., Benzi, L., Martini, C. 2002, Insulin permeability across an in vitro dynamic model of endothelium, Pharm. Res. 19, 445-450.
64. McAllister, M. S., Krizanac-Bengez, L., Macchia, F., Naftalin, R. J., Pedley, K. C., Mayberg, M.R., Marroni, M., Leaman, S., Stanness, K. A., Janigro, D. 2001, Mechanisms of glucose transport at the blood-brain barrier: an in vitro study, Brain Res. 904, 20-30.
65. Janigro, D., Leaman, S. M., Stanness, K. A. 1999, Dynamic modeling of the blood-brain barrier: a novel tool for studies of drug delivery to the brain, News Physiol. Sci. 12, 7-12.
66. Stanness, K. A., Neumaier, J. F., Sexton, T. J., Grant, G. A., Emmi, A., Maris, D.O., Janigro, D. 1999, A new model of the blood-brain barrier: co-culture of neuronal, endothelial and glial cells under dynamic conditions, Neuroreport 10, 3725-3731.
67. Krizanac-Bengez, L., Kapural, M., Parkinson, F., Cucullo, L., Hossain, M., Mayberg, M.R., Janigro, D. 2003, Effects of transient loss of shear stress on blood-brain barrier endothelium: role of nitric oxide and IL-6, Brain Res. 977, 239-246.
68. Ballermann, B. J., Dardik, A., Eng, E., Liu, A. 1998, Shear stress and the endothelium, Kidney Int. Suppl. 67, S100-S108.
69. Haidekker, M. A., L'Heureux, N., Frangos, J. A. 2000, Fluid shear stress increases membrane fluidity in endothelial cells: a study with DCVJ fluorescence, Am. J. Physiol. Heart Circ. Physiol. 278, H1401-H1406.
70. Wasserman, S. M., Topper, J.N. 2004, Adaptation of the endothelium to fluid flow: in vitro analyses of gene expression and in vivo implications, Vasc. Med. 9, 35-45.
71. Krizanac-Bengez, L., Mayberg, M.R., Janigro, D. 2004, The cerebral vasculature as a therapeutic target for neurological disorders and the role of shear stress in vascular homeostasis and pathophysiology, Neurol. Res. 26, 846-853.
72. Brooks, A. R., Lelkes, P. I., Rubanyi, G.M. 2004, Gene expression profiling of vascular endothelial cells exposed to fluid mechanical forces: relevance for focal susceptibility to atherosclerosis, Endothelium 11, 45-57.
73. Ott, M.J., Ballermann, B. J. 1995, Shear stress-conditioned, endothelial cellseeded vascular grafts: improved cell adherence in response to in vitro shear stress, Surgery 117, 334-339.
74. Ballermann, B. J., Ott, M.J. 1995, Adhesion and differentiation of endothelial cells by exposure to chronic shear stress: a vascular graft model, Blood Purif. 13, 125-134.
75. Ando, J., Kamiya, A. 1996, Flow-dependent regulation of gene expression in vascular endothelial cells, Jpn Heart J. 37, 19-32.
76. Lin, K., Hsu, P. P., Chen, B. P., Yuan, S., Usami, S., Shyy, J.Y., Li, Y. S., Chien, S. 2000, Molecular mechanism of endothelial growth arrest by laminar shear stress, Proc. Natl. Acad. Sci. USA 97, 9385-9389.
77. Davies, P. F., Remuzzi, A., Gordon, E. J., Dewey, C.F. Jr., Gimbrone, M.A. Jr. 1986, Turbulent fluid shear stress induces vascular endothelial cell turnover in vitro, Proc. Natl. Acad. Sci. USA 83, 2114-2117.
78. Grabowski, E. F., Jaffe, E. A., Weksler, B.B. 1985, Prostacyclin production by cultured endothelial cell monolayers exposed to step increases in shear stress, J. Lab. Clin. Med. 105, 36-43.
79. Buga, G. M., Gold, M.E., Fukuto, J. M., Ignarro, L. J. 1991, Shear stressinduced release of nitric oxide from endothelial cells grown on beads, Hypertension 17, 187-193.
80. Sharefkin, J. B., Diamond, S. L., Eskin, S. G., McIntire, L.V., Dieffenbach, C.W. 1991, Fluid flow decreases preproendothelin mRNA levels and suppresses endothelin-1 peptide release in cultured human endothelial cells, J. Vasc. Surg. 14, 1-9.
81. Akimoto, S., Mitsumata, M., Sasaguri, T., Yoshida, Y. 2000, Laminar shear stress inhibits vascular endothelial cell proliferation by inducing cyclin-dependent kinase inhibitor p21(Sdi1/Cip1/Waf1), Circ. Res. 86, 185-190.
82. Arisaka, T., Mitsumata, M., Kawasumi, M., Tohjima, T., Hirose, S., Yoshida, Y. 1995, Effects of shear stress on glycosaminoglycan synthesis in vascular endothelial cells, Ann. NY Acad. Sci. 748, 543-554.
83. Yoshida, Y., Okano, M., Wang, S., Kobayashi, M., Kawasumi, M., Hagiwara, H., Mitsumata, M. 1995, Hemodynamic-force-induced difference of interendothelial junctional complexes, Ann. NY Acad. Sci. 748, 104-120.
84. Johnson, R.M. 1994, Membrane stress increases cation permeability in red cells, Biophys. J. 67, 1876-1881.
85. Kroll, M.H., Hellums, J. D., McIntire, L.V., Schafer, A. I., Moake, J. L. 1996, Platelets and shear stress, Blood 88, 1525-1541.
86. Moazzam, F., DeLano, F. A., Zweifach, B.W., Schmid-Schonbein, G.W. 1997, The leukocyte response to fluid stress, Proc. Natl Acad. Sci. USA 94, 5338-5343.
87. Janigro, D., Nguyen, T. S., Gordon, E. L., Winn, H.R. 1996, Physiological properties of ATP-activated cation channels in rat brain microvascular endothelial cells, Am. J. Physiol. 270, H1423-H1434.
88. Stanness, K. A., Guatteo, E., Janigro, D. 1996, A dynamic model of the bloodbrain barrier "in vitro", Neurotoxicology 17, 481-496.
89. Marroni, M., Marchi, N., Cucullo, L., Abbott, N. J., Signorelli, K., Janigro, D. 2003, Vascular and parenchymal mechanisms in multiple drug resistance:a lesson from human epilepsy, Curr. Drug Target. 4, 297-304.
90. Parkinson, F. E., Friesen, J., Krizanac-Bengez, L., Janigro, D. 2003, Use of a three-dimensional in vitro model of the rat blood-brain barrier to assay nucleoside efflux from brain, Brain Res. 980, 233-241.
91. Salvetti, F., Cecchetti, P., Janigro, D., Lucacchini, A., Benzi, L., Martini, C. 2002, Insulin permeability across an in vitro dynamic model of endothelium, Pharm. Res. 19, 445-450.
92. Sinclair, C. J., Krizanac-Bengez, L., Stanness, K. A., Janigro, D., Parkinson, F. E. 2001, Adenosine permeation of a dynamic in vitro blood-brain barrier inhibited by dipyridamole, Brain Res. 898, 122-125.
93. Strelow, L., Janigro, D., Nelson, J. A. 2002, Persistent SIV infection of a blood-brain barrier model, J. Neurovirol. 8, 270-280.
94. Pekny, M., Stanness, K. A., Eliasson, C., Betsholtz, C., Janigro, D. 1998, Impaired induction of blood-brain barrier properties in aortic endothelial cells by astrocytes from GFAP-deficient mice, Glia 22, 390-400.
95. Stanness, K. A., Guatteo, E., Janigro, D. 1996, A dynamic model of the bloodbrain barrier "in vitro", Neurotoxicology 17, 481-496.