Development of the Blood-Brain Interface

Blood-Brain Barriers: From Ontogeny to Artificial Interfaces

Volumn 1, Issue , 2007, Pages 9-39

  Engelhardt, Britta ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Blood brain barrier (BBB); Development of blood brain interface; Development of CNS vasculature; Differentiation; Maintenance; Ontogeny

Indexed keywords

BRAIN INTERFACES;

EID: 70449532747     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527611225.ch1     Document Type: Chapter

References (170)

1. Ehrlich P. 1904, Über die Beziehung chemischer Constitution, Vertheilung, und pharmakologischer Wirkung, Gesammelte Arbeiten zur Immunitätsforschung, Berlin.
2. Goldmann, E. E. 1913, Vitalfärbung am Zentralnervensystem, Abh. Preuss. Wissensch. Phys.-Math. 1, 1-60.
3. Bradbury, M. 1979, The Concept of a Blood-Brain Barrier, John Wiley & Sons, Chichester.
4. Lewandowsky, M. 1890, Zur Lehre der Zerebrospinalflüssigkeit, Z. Klin. Med. 40, 480-494.
5. Biedl, A., Kraus, R. 1898, Über eine bisher unbekannte toxische Wirkung der Gallensäure auf das Zentralnervensystem, Zentralbl. Inn. Med. 19, 1185-1200.
6. Reese, T. S., Karnovsky, M. J. 1967, Fine structural localization of a bloodbrain barrier to exogenous peroxidase, J. Cell Biol. 34, 207-217.
7. Karnovsky, M. J. 1967, The ultrastructural basis of capillary permeability studied with peroxidase as a tracer, J. Cell Biol. 35, 213-236.
8. Abbott, N. J. 1991, Permeability and transport of glial blood-brain barriers, Ann. N.Y. Acad. Sci. 633, 378-394.
9. Cserr, H. F., Bundgaard, M. 1984, Blood-brain interfaces in vertebrates: comparative approach, Am. J. Physiol. 246, 277-288.
10. Leonhardt, H. 1980, Ependym und circumventriculäre Organe, in Handbuch der mikroskopischen Anatomie des Menschen, ed. A. Oksche, L. Vollrath, Springer, Berlin, pp 177-666.
11. Bouchaud, C., Bosler, O. 1986, The circumventricular organs of the mammalian brain with special reference to monoaminergic innervation, Int. Rev. Cytol. 105, 283-327.
12. Engelhardt, B. 2001, The choroid plexus in health and disease, in Microcopy Research and Technique, vol. 52, ed. J. E. Johnson, Wiley-Liss, New York.
13. Johanson, C. E. 1980, Permeability and vascularity of the developing brain:cerebellum vs cerebral cortex, Brain Res. 190, 3-16.
14. Cohen, Z., et al. 1995, Ultrastructural analysis of tryptophan hydroxylase immunoreactive nerve terminals in the rat cerebral cortex and hippocampus:their associations with local blood vessels, Neuroscience 66, 555-569.
15. Paspalas, C. D., Papadopoulos, G. C. 1996, Ultrastructural relationships between noradrenergic nerve fibers and non-neuronal elements in the rat cerebral cortex, Glia 17, 1333-1346.
16. Crone, C., Olesen, S. P. 1982, Electrical resistance of brain microvascular endothelium, Brain Res. 241, 49-55.
17. Simionescu, M., et al. 1988, The cerebral microvasculature of the rat: structure and luminal surface properties during early development, J. Submicrosc. Cytol. 20, 243-261.
18. Mühleisen, H., Wolburg, H., Betz, E. 1989, Freeze-fracture analysis of endothelial cell membranes in rabbit carotid arteries subjected to short-term atherogenic stimuli, Virch. Arch. B Cell Pathol. 56, 413-417.
19. Kniesel, U., Risau, W., Wolburg, H. 1996, Development of blood-brain barrier tight junctions in the rat cortex, Brain Res. Dev. Brain Res. 96, 229-240.
20. Wolburg, H., et al. 1994, Modulation of tight junction structure in bloodbrain barrier endothelial cells: effects of tissue culture, second messengers and cocultured astrocytes, J. Cell Sci. 107, 1347-1357.
21. Shivers, R. R. 1979, The blood-brain barrier of a reptile, Anolis carolinensis:a freeze-fracture study, Brain Res. 169, 221-230.
22. Liebner, S., Gerhardt, H., Wolburg, H. 1997, Maturation of the blood-retina barrier in the pecten oculi of the developing chicken, Dev. Brain Res. 100, 205-219.
23. Liebner, S., et al. 2000, Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier endothelial cells, Eur. J. Cell Biol. 79, 707-717.
24. Morita, K., et al. 1999, Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells, J. Cell Biol. 147, 185-194.
25. Morita, K., et al. 1999, Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands, Proc. Natl Acad. Sci. USA 96, 511-516.
26. Saitou, M., et al. 1997, Mammalian occludin in epithelial cells: its expression and subcellular distribution, Eur. J. Cell Biol. 73, 222-231.
27. Furuse, M., et al. 1993, Occludin - a novel integral membrane-protein localizing at tight junctions, J. Cell Biol. 123, 1777-1788.
28. Saitou, M., et al. 2000, Complex phenotype of mice lacking occludin, a component of tight junction strands, Mol. Biol. Cell 11, 4131-4142.
29. Wolburg, H., et al. 2003, Localization of claudin-3 in tight junctions of the blood-brain barrier is selectively lost during experimental autoimmune encephalomyelitis and human glioblastoma multiforme, Acta Neuropathol. 105, 586-592.
30. Nitta, T., et al. 2003, Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice, J. Cell Biol. 161, 653-660.
31. Liebner, S., 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, 323-331.
32. Lee, S.W., et al. 2003, SSeCKS regulates angiogenesis and tight junction formation in blood-brain barrier, Nat. Med. 9, 900-906.
33. Furuse, M., Sasaki, H., Tsukita, S., 1999, Manner of interaction of heterogeneous claudin species within and between tight junction strands, J. Cell Biol. 147, 891-903.
34. Martin-Padura, I., et al. 1998, Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration, J. Cell Biol. 142, 117-127.
35. Nasdala, I., et al. 2002, A transmembrane tight junction protein selectively expressed on endothelial cells and platelets, J. Biol. Chem. 277, 16294-16303.
36. Cera, M.R., et al. 2004, Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice, J. Clin. Invest. 114, 719-728.
37. Bazzoni, G., et al. 2005, Expression of junctional adhesion molecule-A prevents spontaneous and random motility, J. Cell Sci. 118, 623-632.
38. Bolton, S. J., Anthony, D. C., Perry, V.H. 1998, Loss of tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo, Neuroscience 86, 1245-1257.
39. Tsukita, S., Furuse, M., Itoh, M. 1999, Structural and signalling molecules come together at tight junctions, Curr. Opin. Cell Biol. 11, 628-633.
40. Wolburg, H., Lippoldt, A. 2002, Tight junctions of the blood-brain barrier:development, composition and regulation, Vasc. Pharmacol. 28, 323-337.
41. Van Itallie, C. M., Anderson, J.M. 1997, Occludin confers adhesiveness when expressed in fibroblasts, J. Cell Sci. 110, 1113-1121.
42. Ruffer, C., Gerke, V. 2004, The C-terminal cytoplasmic tail of claudins 1 and 5 but not its PDZ-binding motif is required for apical localization at epithelial and endothelial tight junctions, Eur. J. Cell Biol. 83, 135-144.
43. Schulze, C., Firth, J. A. 1993, Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat, J. Cell Sci. 104, 773-782.
44. Corada, M., et al. 1999, Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo, Proc. Natl Acad. Sci. USA 96, 9815-9820.
45. Vleminckx, K., Kemler, R. 1999, Cadherins and tissue formation: integrating adhesion and signaling, Bioessays 21, 211-220.
46. Dejana, E. 1996, Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis, J. Clin. Invest. 98, 1949-1953.
47. Liebner, S., Gerhardt, H., Wolburg, H. 2000, Differential expression of endothelial beta-catenin and plakoglobin during development and maturation of the blood-brain and blood-retina barrier in the chicken, Dev. Dyn. 271, 86-98.
48. Breier, G., et al. 1995, Molecular cloning and expression of murine VE-cadherin in early developing cardiovascular system (in press).
49. Vorbrodt, A.W., Dobrogowska, D.H. 2004, Molecular anatomy of interendothelial junctions in human blood-brain barrier microvessels, Folia Histochem. Cytobiol. 42, 67-75.
50. Duncan, G. S., et al. 1999, Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions, J. Immunol. 162, 3022-3030.
51. Graesser, D., et al. 2002, Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice, J. Clin. Invest. 109, 383-392.
52. Nico, B., et al. 2003, Severe alterations of endothelial and glial cells in the blood-brain barrier of dystrophic mdx mice, Glia 42, 235-251.
53. Pardridge, W.M. 2005, Molecular biology of the blood-brain barrier, Mol. Biotechnol. 30, 57-70.
54. Bolz, S., et al. 1996, Subcellular distribution of glucose transporter (GLUT-1) during development of the blood-brain barrier in rats, Cell Tissue Res. 284, 355-365.
55. Kissel, K., et al. 1998, Immunohistochemical localization of the murine transferrin receptor (TfR) on blood-tissue barriers using a novel anti-TfR monoclonal antibody, Histochem. Cell Biol. (in press).
56. Schinkel, A. H., et al. 1994, Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs, Cell 77, 491-502.
57. Stewart, P. A. 2000, Development of the blood-brain barrier, in Morphogenesis of Endothelium, eds. W. Risau, G.M. Rubanyi, Harwood, Amsterdam, pp 109-122.
58. el-Bacha, R. S., Minn, A. 1999, Drug metabolizing enzymes in cerebrovascular endothelial cells afford a metabolic protection to the brain, Cell Mol. Biol. 45, 15-23.
59. Song, L., Pachter, J.S. 2003, Culture of murine brain microvascular endothelial cells that maintain expression and cytoskeletal association of tight junction-associated proteins, In Vitro Cell Dev. Biol. Anim. 39, 313-320.
60. Bär, T. 1980, The vascular system of the cerebral cortex, Adv. Anat. Embryol. Cell Biol. 59, 1-62.
61. Risau, W., Wolburg, H. 1990, Development of the blood-brain barrier, Trends Neurosci. 13, 174-178.
62. Dermietzel, R., Krause, D. 1991, Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry, Int. Rev. Cytol. 127, 57-109.
63. Stewart, P. A., Wiley, M. J. 1981, Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras, Dev. Biol. 84, 183-192.
64. Noden, D.M. 1991, Development of craniofacial blood vessels, in Development of the Vascular System, eds. R. N. Feinberg, G. K. Sherer, R. Auerbach, Karger, Basel, pp 1-24.
65. Risau, W. 1997, Mechanisms of angiogenesis, Nature 386, 671-674.
66. Roncali, L., et al. 1986, Microscopical and ultrastructural investigations on the development of the blood-brain barrier in the chick embryo optic tectum, Acta Neuropathol. 70, 193-201.
67. Kuban, K. C., Gilles, F.H. 1985, Human telencephalic angiogenesis, Ann. Neurol. 17, 539-548.
68. Risau, W., Gautschi-Sova, P., Bohlen, P. 1988, Endothelial cell growth factors in embryonic and adult chick brain are related to human acidic fibroblast growth factor, EMBO J. 7, 959-962.
69. Folkman, J., Klagsbrun, M. 1987, Vascular physiology: a family of angiogenic peptides (news), Nature 329, 671-672.
70. Folkman, J., et al. 1988, A heparin-binding angiogenic protein - basic fibroblast growth factor - is stored within basement membrane, Am. J. Pathol. 130, 393-400.
71. Risau, W., Gautschi-Sova, P., Böhlen, P. 1988, Endothelial cell growth factors in embryonic and adult chick brain are related to human acidic fibroblast growth factors, EMBO J. 7, 959-962.
72. Schnurch, H., Risau, W. 1991, Differentiating and mature neurons express the acidic fibroblast growth factor gene during chick neural development, Development 111, 1143-1154.
73. Emoto, N., et al. 1989, Basic fibroblast growth factor (FGF) in the central nervous system: identification of specific loci of basic FGF expression in the rat brain, Growth Factors 2, 21-29.
74. Claus, P., Grothe, C. 2001, Molecular cloning and developmental expression of rat fibroblast growth factor receptor 3, Histochem. Cell Biol. 115, 147-155.
75. Ferrara, N., Henzel, W. J. 1989, Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells, Biochem. Biophys. Res. Commun. 161, 851-858.
76. Gale, N.W., Yancopoulos, G. D. 1999, Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development, Genes Dev. 13, 1055-1066.
77. Engelhardt, B., Risau, W. 1995, The development of the blood-brain barrier, in New Concepts of a Blood-Brain Barrier, eds. J. Greenwood, D. Begley, M. Segal, Plenum, London.
78. Bass, T., et al. 1992, Radial glial interaction with cerebral germinal matrix capillaries in the fetal baboon, Exp. Neurol. 118, 126-132.
79. Fruttiger, M., et al. 1996, PDGF mediates a neuron-astrocyte interaction in the developing retina, Neuron 17, 1117-1131.
80. Gerhardt, H., et al. 2003, VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia, J. Cell Biol. 161, 1163-1177.
81. Stone, J., Dreher, Z. 1987, Relationship between astrocytes, ganglion cells and vasculature of the retina, J. Comp. Neurol. 255, 35-49.
82. Houck, K. A., et al. 1992, Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms, J. Biol. Chem. 267, 26031-26037.
83. Ruhrberg, C., et al. 2002, Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis, Genes Dev. 16, 2684-2698.
84. Fischer, A., et al. 2004, The notch target genes Hey1 and Hey2 are required for embryonic vascular development, Genes Dev. 18, 901-911.
85. Adams, R.H. 2002, Vascular patterning by Eph receptor tyrosine kinases and ephrins, Semin. Cell Dev. Biol. 13, 55-60.
86. Shawber, C. J., Kitajewski, J. 2004, Notch function in the vasculature: insights from zebrafish, mouse and man, Bioessays 26, 225-234.
87. Park, K.W., et al. 2003, Robo4 is a vascular-specific receptor that inhibits endothelial migration, Dev. Biol. 261, 251-267.
88. Eichmann, A., Makinen, T., Alitalo, K. 2005, Neural guidance molecules regulate vascular remodeling and vessel navigation, Genes Dev. 19, 1013-1021.
89. Deutsch, U. 2004, Semaphorins guide PerPlexeD endothelial cells, Dev. Cell. 7, 1-2.
90. Davis, S., Yancopoulos, G. D. 1999, The angiopoietins: yin and yang in angiogenesis, Curr. Top. Microbiol. Immunol. 237, 173-185.
91. Lindahl, P., et al. 1997, Pericyte loss and microaneurysm formation in PDGF-B-deficient mice, Science 277, 242-245.
92. Goumans, M.J., Lebrin, F., Valdimarsdottir, G. 2003, Controlling the angiogenic switch: a balance between two distinct TGF-α receptor signaling pathways, Trends Cardiovasc Med. 13, 301-307.
93. Papkoff, J., Brown, A. M., Varmus, H.E. 1987, The int-1 proto-oncogene products are glycoproteins that appear to enter the secretory pathway, Mol. Cell Biol. 7, 3978-3984.
94. Papkoff, J., Schryver, B. 1990, Secreted int-1 protein is associated with the cell surface, Mol. Cell Biol. 10, 2723-2730.
95. Gumbiner, B.M. 1995, Signal transduction by β-catenin, Curr. Opin. Cell Biol. 7, 634-640.
96. Behrens, J., et al. 1996, Functional interaction of β-catenin with the transcription factor LEF-1, Nature 382, 638-642.
97. Zhurinsky, J., Shutman, M., Ben-Ze'ev, A. 2000, Plakoglobin and beta-catenin:protein interactions, regulation and biological roles, J. Cell Sci. 113, 3127-3139.
98. Miller, J. R., Moon, R.T. 1996, Signal transduction through β-catenin and specification of cell fate during embryogenesis, Genes Dev. 10, 2527-2539.
99. Liebner, S., et al. 2004, Beta-catenin is required for TGF-beta-mediated endothelial to mesenchymal transformation during heart cushion development in the mouse, J. Cell Biol. (in press).
100. Cattelino, A., et al. 2003, The conditional inactivation of the β-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility, J. Cell Biol. 162, 1111-1122.
101. Wright, M., et al. 1999, Identification of a Wnt-responsive signal transduction pathway in primary endothelial cells, Biochem. Biophys. Res. Commun. 263, 384-388.
102. Maretto, S., et al. 2003, Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors, Proc. Natl Acad. Sci. USA 100, 3299-3304.
103. Robitaille, J., et al. 2002, Mutant frizzled-4 disrupts retinal angiogenesis in familial exudative vitreoretinopathy, Nat. Genet. 32, 326-330.
104. Xu, Q., et al. 2004, Vascular development in the retina and inner ear: control by norrin and frizzled-4, a high-affinity ligand-receptor pair, Cell 116, 883-895.
105. Cassella, J. P., Lawrenson, J. G., Firth, J. A. 1997, Development of endothelial paracellular clefts and their tight junctions in the pial microvessels of the rat, J. Neurocytol. 26, 567-575.
106. Stewart, P. A., Hayakawa, E.M. 1994, Early ultrastructural changes in bloodbrain barrier vessels of the rat embryo, Dev. Brain Res. 78, 25-34.
107. Schulze, C., Firth, J. A. 1992, Interendothelial junctions during blood-brain barrier development in the rat: morphological changes at the level of individual tight junctional contacts, Dev. Brain Res. 1-11.
108. Saunders, N. R., Dziegielewska, K. M., Mollgard, K. 1991, Letter to the editor:the importance of the blood-brain barrier in fetuses and embryos, Trends Neurosci. 14, 14.
109. Risau, W., Wolburg, H. 1991, The importance of the blood-brain barrier in fetuses and embryos - reply, Trends Neurosci. 14, 15.
110. Risau, W. 1991, Induction of blood-brain barrier endothelial cell differentiation, Ann. NY Acad. Sci. 633, 405-419.
111. Wakai, S., Hirokawa, N. 1978, Development of the blood-brain barrier to horseradish peroxidase in the chick embryo, Cell Tissue Res. 195, 195-203.
112. Stewart, P. A., Hayakawa, E.M. 1987, Interendothelial junctional changes underlie the developmental 'tightening' of the blood-brain barrier, Dev. Brain Res. 32, 271-281.
113. Olsson, Y., et al. 1968, Blood-brain barrier to albumin in embryonic new born and adult rats, Acta Neuropathol. 10, 117-122.
114. Risau, W., Hallmann, R., Albrecht, U. 1986, Differentiation-dependent expression of protein in brain endothelium during development of the bloodbrain barrier, Dev. Biol. 117, 537-545.
115. Mollgard, K., et al. 1988, Synthesis and localization of plasma proteins in the developing human brain. Integrity of the fetal blood-brain barrier to endogenous proteins of hepatic origin, Dev. Biol. 128, 207-221.
116. Stonestreet, B. S., et al. 1996, Ontogeny of blood-brain barrier function in ovine fetuses, lambs, and adults, Am. J. Physiol. 271, R1594-R1601.
117. Dziegielewska, K. M., et al. 2001, Development of the choroid plexus, Microsc. Res. Tech. 52, 5-20.
118. Tuor, U. I., Simone, C., Bascaramurty, S. 1992, Local blood-brain barrier in the newborn rabbit: postnatal changes in alpha-aminoisobutyric acid transfer within medulla, cortex, and selected brain areas, J. Neurochem. 59, 999-1007.
119. Butt, A. M., Jones, H.C., Abbott, N. J. 1990, Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study, J. Physiol. 429, 47-62.
120. Keep, R. F., et al. 1995, Developmental changes in blood-brain barrier potassium permeability in the rat: relation to brain growth, J. Physiol. 488, 439-448.
121. Robertson, P. L., et al. 1985, Angiogenesis in developing rat brain: an in vivo and in vitro study, Dev. Brain Res. 23, 219-223.
122. Betz, A. L., Goldstein, G.W. 1986, Specialized properties and solute transport in brain capillaries, Annu. Rev. Physiol. 48, 241-250.
123. Broadwell, R. D. 1989, Transcytosis of macromolecules through the bloodbrain barrier: a cell biological perspective and critical appraisal, Acta Neuropathol. 79, 117-128.
124. Pardridge, W.M. 1988, Recent advances in blood-brain barrier transport, Annu. Rev. Pharmacol. Toxicol. 28, 25-39.
125. Dermietzel, R., et al. 1992, Pattern of glucose transporter (Glut 1) expression in embryonic brains is related to maturation of blood-brain barrier tightness, Dev. Dyn. 193, 152-163.
126. Qin, Y., Sato, T. N. 1995, Mouse multidrug resistance 1a/3 gene is the earliest known endothelial cell differentiation marker during blood-brain barrier development, Dev. Dyn. 202, 172-180.
127. Stewart, P. A., Beliveau, R., Rogers, K. A. 1996, Cellular localization of P-glycoprotein in brain versus gonadal capillaries, J. Histochem. Cytochem. 44, 679-685.
128. Golden, P. L., Pardridge, W.M. 2000, Brain microvascular P-glycoprotein and a revised model of multidrug resistance in brain, Cell Mol. Neurobiol. 20, 165-181.
129. Achen, M.G., et al. 1995, The non-receptor tyrosine kinase Lyn is localised in the developing murine blood-brain barrier, Differentiation 59, 15-24.
130. Albrecht, U., et al. 1990, Correlation of blood-brain barrier function and HT7 protein distribution in chick brain circumventricular organs, Brain Res. 535, 49-61.
131. Gerhardt, H., Liebner, S., Wolburg, H. 1996, The pecten oculi of the chicken as a new in vivo model of the blood-brain barrier, Cell Tissue Res. 285, 91-100.
132. Bertossi, M., et al. 2002, Developmental changes of HT7 expression in the microvessels of the chick embryo brain, Anat. Embryol. 205, 229-233.
133. Hallmann, R., et al. 1995, Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood-brain barrier, Dev. Dyn. 202, 325-332.
134. Stan, R.V., et al. 1999, Isolation, cloning, and localization of rat PV-1, a novel endothelial caveolar protein, J. Cell Biol. 145, 1189-1198.
135. Stan, R.V., Kubitza, M., Palade, G. E. 1999, PV-1 is a component of the fenestral and stomatal diaphragms in fenestrated endothelia, Proc. Natl Acad. Sci. USA 96, 13203-13207.
136. Leppink, D.M., et al. 1989, Inducible expression of an endothelial cell antigen on murine myocardial vasculature in association with interstitial cellular infiltration, Transplantation 48, 874-877.
137. Barber, A. J., Lieth, E. 1997, Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier, Dev. Dyn. 208, 62-74.
138. Ikeda, E., Flamme, I., Risau, W. 1996, Developing brain cells produce factors capable of inducing the HT7 antigen, a blood-brain barrier-specific molecule, in chick endothelial cells, Neurosci. Lett. 209, 149-152.
139. Phelps, C.H. 1972, The development of glio-vascular relationships in the rat spinal cord, Z. Zellforsch. 128, 555-563.
140. Goldstein, G.W. 1988, Endothelial cell-astrocyte interactions: a cellular model of the blood-brain barrier, Ann. NY Acad. Sci. 529, 31-39.
141. Janzer, R. C., Raff, M.C. 1987, Astrocytes induce blood-brain barrier properties in endothelial cells, Nature 325, 253-257.
142. Small, R. K., et al. 1993, Functional properties of retinal Muller cells following transplantation to the anterior eye chamber, Glia 7, 158-169.
143. Rubin, L. L., et al. 1991, A cell culture model of the blood-brain barrier, J. Cell Biol. 115, 1725-1735.
144. Meresse, S., et al. 1989, Bovine brain endothelial cells express tight junctions and monoamine oxidase activity in long-term culture, J. Neurochem. 53, 1363-1371.
145. Coats, S. R., et al. 2002, Ligand-specific control of src-suppressed C kinase substrate gene expression, Biochem. Biophys. Res. Commun. 297, 1112-1120.
146. Bjarnegard, M., et al. 2004, Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities, Development 131, 1847-1857.
147. Mi, H., Haeberle, H., Barres, B. A. 2001, Induction of astrocyte differentiation by endothelial cells, J. Neurosci. 21, 1538-1547.
148. Sims, D.E. 1986, The pericyte - a review, Tissue Cell 18, 153-174.
149. Lindblom, P., et al. 2003, Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall, Genes Dev. 17, 1835-1840.
150. Suri, C., et al. 1996, Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis, Cell 87, 1171-1180.
151. Oh, S. P., et al. 2000, Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis, Proc. Natl Acad. Sci. USA 97, 2626-2631.
152. Yang, X., et al. 1999, Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5, Development 126, 1571-1580.
153. Larsson, J., et al. 2001, Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice, EMBO J. 20, 1663-1673.
154. Oshima, M., Oshima, H., Taketo, M.M. 1996, TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis, Dev. Biol. 179, 297-302.
155. Li, D.Y., et al. 1999, Defective angiogenesis in mice lacking endoglin, Science 284, 1534-1537.
156. Dickson, M.C., et al. 1995, Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice, Development 121, 1845-1854.
157. Gerhardt, H., Wolburg, H., Redies, C. 2000, N-cadherin mediates pericyticendothelial interaction during brain angiogenesis in the chicken, Dev. Dyn. 218, 472-479.
158. Gerhardt, H., et al. 1999, N-cadherin expression in endothelial cells during early angiogenesis in the eye and brain of the chicken: relation to bloodretina and blood-brain barrier development, Eur. J. Neurosci. 11, 1191-1201.
159. Miwa, N., et al. 2000, Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers, Oncol. Res. 12, 469-476.
160. Bauer, H. C., Bauer, H. 2000, Neural induction of the blood-brain barrier:still an enigma, Cell Mol. Neurobiol. 20, 13-28.
161. McCarty, J. H., et al. 2002, Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking alpha integrins, Mol. Cell Biol. 22, 7667-7777.
162. Zhu, J., et al. 2002, Abstract beta integrins are required for vascular morphogenesis in mouse embryos, Development 129, 2891-2903.
163. Engelhardt, B., Conley, F. K., Butcher, E.C. 1994, Cell adhesion molecules on vessels during inflammation in the mouse central nervous system, J. Neuroimmunol. 51, 199-208.
164. Barber, A. J., Lieth, E. 1997, Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier, Dev. Dyn. 208, 62-74.
165. Rascher, G., et al. 2002, Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin, Acta Neuropathol. 104, 85-91.
166. Kniesel, U., Wolburg, H. 2000, Tight junctions of the blood-brain barrier, Cell Mol. Neurobiol. 20, 57-76.
167. Coisne, C., et al. 2005, Mouse syngeneic in vitro blood-brain barrier model:a new tool to examine inflammatory events in cerebral endothelium, Lab. Invest. 85, 734-746.
168. Farrell, C. L., Risau, W. 1994, Normal and abnormal development of the blood-brain barrier, Microsc. Res. Tech. 27, 495-506.
169. Alt, C., et al. 2005, Gene and protein expression profiling of the microvascular compartment in experimental autoimmune encephalomyelitis in C57Bl/6 and SJL mice, Brain Pathol. 15, 1-16.
170. Engelhardt, B. 2003, Development of the blood-brain barrier, Cell Tissue Res. 314, 119-129.