The blood-brain barrier: An overview: Structure, regulation, and clinical implications

Neurobiology of Disease

Volumn 16, Issue 1, 2004, Pages 1-13

  Ballabh, Praveen ^a   Braun, Alex ^a   Nedergaard, Maiken ^a  

^a WESTCHESTER MEDICAL CENTER   (United States)

Author keywords

Astrocyte; Blood brain barrier; Germinal matrix; Pericyte; Tight junction

Indexed keywords

AQUAPORIN 4; CALCIUM ION; CELL ADHESION MOLECULE; CLAUDIN; GLIAL FIBRILLARY ACIDIC PROTEIN; OCCLUDIN; VIMENTIN;

ALZHEIMER DISEASE; ASTROCYTE; BLEEDING; BLOOD BRAIN BARRIER; BLOOD VESSEL; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; BRAIN TUMOR; CENTRAL NERVOUS SYSTEM DISEASE; CYTOPLASM; DEMENTIA; ENCEPHALITIS; ENDOTHELIUM CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HYPOXIA; IMMATURITY; INFLAMMATION; MULTIPLE SCLEROSIS; PATHOGENESIS; PATHOPHYSIOLOGY; PERICYTE; PERMEABILITY; PRECURSOR; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TIGHT JUNCTION;

ANIMALS; BLOOD-BRAIN BARRIER; HUMANS; INTRACRANIAL HEMORRHAGES; NERVOUS SYSTEM DISEASES;

EID: 2342471420     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2003.12.016     Document Type: Review

References (133)

1. The Boulder Committee Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166:1970;257-261
2. Abbott N.J. Inflammatory mediators and modulation of blood-brain barrier permeability. Cell. Mol. Neurobiol. 20:2000;131-147
3. Abbott N.J. Astrocyte-endothelial interactions and blood-brain barrier permeability. J. Anat. 200:2002;629-638
4. Akama K.T., Albanese C., Pestell R.G., Van Eldik L.J. Amyloid beta-peptide stimulates nitric oxide production in astrocytes through an NFkappaB-dependent mechanism. Proc. Natl. Acad. Sci. U.S.A. 95:1998;5795-5800
5. Allt G., Lawrenson J.G. Pericytes: cell biology and pathology. Cells Tissues Organs. 169:2001;1-11
6. Ando-Akatsuka Y., Saitou M., Hirase T., Kishi M., Sakakibara A., Itoh M., Yonemura S., Furuse M., Tsukita S. Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. J. Cell Biol. 133:1996;43-47
7. Annunziata P., Cioni C., Toneatto S., Paccagnini E. HIV-1 gp120 increases the permeability of rat brain endothelium cultures by a mechanism involving substance P. AIDS. 12:1998;2377-2385
8. Anstrom J.A., Brown W.R., Moody D.M., Thore C.R., Challa V.R., Block S.M. Anatomical analysis of the developing cerebral vasculature in premature neonates: absence of precapillary arteriole-to-venous shunts. Pediatr. Res. 52:2002;554-560
9. Antoniuk S., da Silva R.V. Periventricular and intraventricular hemorrhage in the premature infants. Rev. Neurol. 31:2000;238-243
10. Aurrand-Lions M., Johnson-Leger C., Wong C., Du Pasquier L., Imhof B.A. Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood. 98:2001;3699-3707
11. Balabanov R., Dore-Duffy P. Role of the CNS microvascular pericyte in the blood-brain barrier. J. Neurosci. Res. 53:1998;637-644
12. Balabanov R., Washington R., Wagnerova J., Dore-Duffy P. CNS microvascular pericytes express macrophage-like function, cell surface integrin alpha M, and macrophage marker ED-2. Microvasc. Res. 52:1996;127-142
13. Balda M.S., Gonzalez-Mariscal L., Contreras R.G., Macias-Silva M., Torres-Marquez M.E., Garcia-Sainz J.A., Cereijido M. Assembly and sealing of tight junctions: possible participation of G-proteins, phospholipase C, protein kinase C and calmodulin. J. Membr. Biol. 122:1991;193-202
14. Bandopadhyay R., Orte C., Lawrenson J.G., Reid A.R., De Silva S., Allt G. Contractile proteins in pericytes at the blood-brain and blood-retinal barriers. J. Neurocytol. 30:2001;35-44
15. Bass T., Singer G., Slusser J., Liuzzi F.J. Radial glial interaction with cerebral germinal matrix capillaries in the fetal baboon. Exp. Neurol. 118:1992;126-132
16. Bauer H.C., Bauer H., Lametschwandtner A., Amberger A., Ruiz P., Steiner M. Neovascularization and the appearance of morphological characteristics of the blood-brain barrier in the embryonic mouse central nervous system. Brain Res. Dev. Brain Res. 75:1993;269-278
17. Bazzoni G., Martinez-Estrada O.M., Mueller F., Nelboeck P., Schmid G., Bartfai T., Dejana E., Brockhaus M. Homophilic interaction of junctional adhesion molecule. J. Biol. Chem. 275:2000;30970-30976
18. Benagiano V., Virgintino D., Maiorano E., Rizzi A., Palombo S., Roncali L., Ambrosi G. VIP-like immunoreactivity within neurons and perivascular neuronal processes of the human cerebral cortex. Eur. J. Histochem. 40:1996;53-56
19. Bertossi M., Virgintino D., Errede M., Roncali L. Immunohistochemical and ultrastructural characterization of cortical plate microvasculature in the human fetus telencephalon. Microvasc. Res. 58:1999;49-61
20. Bolton S.J., Anthony D.C., Perry V.H. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience. 86:1998;1245-1257
21. Boven L.A., Gomes L., Hery C., Gray F., Verhoef J., Portegies P., Tardieu M., Nottet H.S. Increased peroxynitrite activity in AIDS dementia complex: implications for the neuropathogenesis of HIV-1 infection. J. Immunol. 162:1999;4319-4327
22. Braet K., Paemeleire K., D'Herde K., Sanderson M.J., Leybaert L. Astrocyte-endothelial cell calcium signals conveyed by two signalling pathways. Eur. J. Neurosci. 13:2001;79-91
23. Broadwell R.D., Charlton H.M., Ebert P., Hickey W.F., Villegas J.C., Wolf A.L. Angiogenesis and the blood-brain barrier in solid and dissociated cell grafts within the CNS. Prog. Brain Res. 82:1990;95-101
24. Chao C.C., Hu S., Sheng W.S., Peterson P.K. Tumor necrosis factor-alpha production by human fetal microglial cells: regulation by other cytokines. Dev. Neurosci. 17:1995;97-105
25. Chen Y., McCarron R.M., Azzam N., Bembry J., Reutzler C., Lenz F.A., Spatz M. Endothelin-1 and nitric oxide affect human cerebromicrovascular endothelial responses and signal transduction. Acta Neurochir., Suppl. 76:2000;131-135
26. Clawson C.C., Hartmann J.F., Vernier R.L. Electron microscopy of the effect of gram-negative endotoxin on the blood-brain barrier. J. Comp. Neurol. 127:1966;183-198
27. Dehouck M.P., Vigne P., Torpier G., Breittmayer J.P., Cecchelli R., Frelin C. Endothelin-1 as a mediator of endothelial cell-pericyte interactions in bovine brain capillaries. J. Cereb. Blood Flow Metab. 17:1997;464-469
28. Deng X., Wang X., Andersson R. Endothelial barrier resistance in multiple organs after septic and nonseptic challenges in the rat. J. Appl. Physiol. 78:1995;2052-2061
29. de Vries H.E., Blom-Roosemalen M.C., van Oosten M., de Boer A.G., van Berkel T.J., Breimer D.D., Kuiper J. The influence of cytokines on the integrity of the blood-brain barrier in vitro. J. Neuroimmunol. 64:1996;37-43
30. DiSalvo D. The correlation between placental pathology and intraventricular hemorrhage in the preterm infant. The Developmental Epidemiology Network Investigators. Pediatr. Res. 43:1998;15-19
31. Ebnet K., Schulz C.U., Meyer Zu Brickwedde M.K., Pendl G.G., Vestweber D. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J. Biol. Chem. 275:2000;27979-27988
32. Elfont R.M., Sundaresan P.R., Sladek C.D. Adrenergic receptors on cerebral microvessels: pericyte contribution. Am. J. Physiol. 256:1989;R224-R230
33. Feuerstein G.Z., Liu T., Barone F.C. Cytokines, inflammation, and brain injury: role of tumor necrosis factor-alpha. Cerebrovasc. Brain Metab. Rev. 6:1994;341-360
34. Fischer S., Clauss M., Wiesnet M., Renz D., Schaper W., Karliczek G.F. Hypoxia induces permeability in brain microvessel endothelial cells via VEGF and NO. Am. J. Physiol. 276:1999;C812-C820
35. Fischer S., Wobben M., Kleinstuck J., Renz D., Schaper W. Effect of astroglial cells on hypoxia-induced permeability in PBMEC cells. Am. J. Physiol.: Cell Physiol. 279:2000;C935-C944
36. Fischer S., Wobben M., Marti H.H., Renz D., Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc. Res. 63:2002;70-80
37. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S. Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 123:1993;1777-1788
38. Furuse M., Fujita K., Hiiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141:1998;1539-1550
39. Furuse M., Sasaki H., Tsukita S. Manner of interaction of heterogeneous claudin species within and between tight junction strands. J. Cell Biol. 147:1999;891-903
40. Ghazi-Birry H.S., Brown W.R., Moody D.M., Challa V.R., Block S.M., Reboussin D.M. Human germinal matrix: venous origin of hemorrhage and vascular characteristics. AJNR Am. J. Neuroradiol. 18:1997;219-229
41. Giulian D., Haverkamp L.J., Li J., Karshin W.L., Yu J., Tom D., Li X., Kirkpatrick J.B. Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer brain. Neurochem. Int. 27:1995;119-137
42. Gould S.J., Howard S. An immunohistochemical study of the germinal layer in the late gestation human fetal brain. Neuropathol. Appl. Neurobiol. 13:1987;421-437
43. 2 indicator- dilution technique. J. Appl. Physiol. 58:1985;1929-1941
44. Groothuis D.R., Vriesendorp F.J., Kupfer B., Warnke P.C., Lapin G.D., Kuruvilla A., Vick N.A., Mikhael M.A., Patlak C.S. Quantitative measurements of capillary transport in human brain tumors by computed tomography. Ann. Neurol. 30:1991;581-588
45. Hambleton G., Wigglesworth J.S. Origin of intraventricular haemorrhage in the preterm infant. Arch. Dis. Child. 51:1976;651-659
46. Haskins J., Gu L., Wittchen E.S., Hibbard J., Stevenson B.R. ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin. J. Cell Biol. 141:1998;199-208
47. Healy D.P., Wilk S. Localization of immunoreactive glutamyl aminopeptidase in rat brain. II. Distribution and correlation with angiotensin II. Brain Res. 606:1993;295-303
48. Hippenstiel S., Krull M., Ikemann A., Risau W., Clauss M., Suttorp N. VEGF induces hyperpermeability by a direct action on endothelial cells. Am. J. Physiol. 274:1998;L678-L684
49. Hirase T., Staddon J.M., Saitou M., Ando-Akatsuka Y., Itoh M., Furuse M., Fujimoto K., Tsukita S., Rubin L.L. Occludin as a possible determinant of tight junction permeability in endothelial cells. J. Cell. Sci. 110:1997;1603-1613
50. Hirschi K.K., D'Amore P.A. Control of angiogenesis by the pericyte: molecular mechanisms and significance. EXS. 79:1997;419-428
51. Hoheisel D., Nitz T., Franke H., Wegener J., Hakvoort A., Tilling T., Galla H.J. Hydrocortisone reinforces the blood-brain properties in a serum free cell culture system. Biochem. Biophys. Res. Commun. 247:1998;312-315
52. Holash J.A., Noden D.M., Stewart P.A. Re-evaluating the role of astrocytes in blood-brain barrier induction. Dev. Dyn. 197:1993;14-25
53. Itoh M., Furuse M., Morita K., Kubota K., Saitou M., Tsukita S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J. Cell Biol. 147:1999;1351-1363
54. Izumi Y., Hirose T., Tamai Y., Hirai S., Nagashima Y., Fujimoto T., Tabuse Y., Kemphues K.J., Ohno S. An atypical PKC directly associates and colocalizes at the epithelial tight junction with ASIP, a mammalian homologue of Caenorhabditis elegans polarity protein PAR-3. J. Cell Biol. 143:1998;95-106
55. Jacobson M. Developmental Neurobiology. third ed. 1991;Plenum, New York
56. Janzer R.C., Raff M.C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature. 325:1987;253-257
57. Jeppsson B., Freund H.R., Gimmon Z., James J.H., von Meyenfeldt M.F., Fischer J.E. Blood-brain barrier derangement in sepsis: cause of septic encephalopathy? Am. J. Surg. 141:1981;136-142
58. Johnson R.T., McArthur J.C., Narayan O. The neurobiology of human immunodeficiency virus infections. FASEB J. 2:1988;2970-2981
59. Kenny J.D., Garcia-Prats J.A., Hilliard J.L., Corbet A.J., Rudolph A.J. Hypercarbia at birth: a possible role in the pathogenesis of intraventricular hemorrhage. Pediatrics. 62:1978;465-467
60. Kern T.S., Engerman R.L. Capillary lesions develop in retina rather than cerebral cortex in diabetes and experimental galactosemia. Arch. Ophthalmol. 114:1996;306-310
61. Kis B., Abraham C.S., Deli M.A., Kobayashi H., Niwa M., Yamashita H., Busija D.W., Ueta Y. Adrenomedullin, an autocrine mediator of blood-brain barrier function. Hypertens. Res. 26:2003;S61-S70. (supplement)
62. Klegeris A., McGeer P.L. Beta-amyloid protein enhances macrophage production of oxygen free radicals and glutamate. J. Neurosci. Res. 49:1997;229-235
63. Klegeris A., Walker D.G., McGeer P.L. Interaction of Alzheimer beta-amyloid peptide with the human monocytic cell line THP-1 results in a protein kinase C-dependent secretion of tumor necrosis factor-alpha. Brain Res. 747:1997;114-121
64. Kondo T., Kinouchi H., Kawase M., Yoshimoto T. Astroglial cells inhibit the increasing permeability of brain endothelial cell monolayer following hypoxia/reoxygenation. Neurosci. Lett. 208:1996;101-104
65. Krum J.M., Kenyon K.L., Rosenstein J.M. Expression of blood-brain barrier characteristics following neuronal loss and astroglial damage after administration of anti-Thy-1 immunotoxin. Exp. Neurol. 146:1997;33-45
66. Kustova Y., Grinberg A., Basile A.S. Increased blood-brain barrier permeability in LP-BM5 infected mice is mediated by neuroexcitatory mechanisms. Brain Res. 839:1999;153-163
67. Lamszus K., Laterra J., Westphal M., Rosen E.M. Scatter factor/hepatocyte growth factor (SF/HGF) content and function in human gliomas. Int. J. Dev. Neurosci. 17:1999;517-530
68. Lang H.L., Jacobsen H., Ikemizu S., Andersson C., Harlos K., Madsen L., Hjorth P., Sondergaard L., Svejgaard A., Wucherpfennig K., Stuart D.I., Bell J.I., Jones E.Y., Fugger L. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol. 3:2002;940-943
69. Liebner S., Fischmann A., Rascher G., Duffner F., Grote E.H., Kalbacher H., Wolburg H. Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol. (Berl.). 100:2000;323-331
70. Liebner S., Kniesel U., Kalbacher H., Wolburg H. Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier endothelial cells. Eur. J. Cell Biol. 79:2000;707-717
71. Lindahl P., Johansson B.R., Leveen P., Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 277:1997;242-245
72. Lippoldt A., Kniesel U., Liebner S., Kalbacher H., Kirsch T., Wolburg H., Haller H. Structural alterations of tight junctions are associated with loss of polarity in stroke-prone spontaneously hypertensive rat blood-brain barrier endothelial cells. Brain Res. 885:2000;251-261
73. Liu Y., Wu Y., Lee J.C., Xue H., Pevny L.H., Kaprielian Z., Rao M.S. Oligodendrocyte and astrocyte development in rodents: an in situ and immunohistological analysis during embryonic development. Glia. 40:2002;25-43
74. Long D.M. Capillary ultrastructure and the blood-brain barrier in human malignant brain tumors. J. Neurosurg. 32:1970;127-144
75. Long D.M. Capillary ultrastructure in human metastatic brain tumors. J. Neurosurg. 51:1979;53-58
76. Lou J., Chofflon M., Juillard C., Donati Y., Mili N., Siegrist C.A., Grau G.E. Brain microvascular endothelial cells and leukocytes derived from patients with multiple sclerosis exhibit increased adhesion capacity. NeuroReport. 8:1997;629-633
77. Louissaint A. Jr., Rao S., Leventhal C., Goldman S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron. 34:2002;945-960
78. Magistretti P.J., Pellerin L., Rothman D.L., Shulman R.G. Energy on demand. Science. 283:1999;496-497
79. Mark K.S., Davies T.P. Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am. J. Physiol.: Heart Circ. Physiol. 282:2002;H1485-H1494
80. Martin-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., Panzeri C., Stoppacciaro A., Ruco L., Villa A., et al. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142:1998;117-127
81. Matter K., Balda M.S. Signalling to and from tight junctions. Nat. Rev., Mol. Cell Biol. 4:2003;225-236
82. Ment L.R., Oh W., Philip A.G., Ehrenkranz R.A., Duncan C.C., Allan W., Taylor K.J., Schneider K., Katz K.H., Makuch R.W. Risk factors for early intraventricular hemorrhage in low birth weight infants. J. Pediatr. 121:1992;776-783
83. Ment L.R., Stewart W.B., Ardito T.A., Madri J.A. Germinal matrix microvascular maturation correlates inversely with the risk period for neonatal intraventricular hemorrhage. Brain Res. Dev. Brain Res. 84:1995;142-149
84. Merrill J.E., Ignarro L.J., Sherman M.P., Melinek J., Lane T.E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151:1993;2132-2141
85. Mi H., Haeberle H., Barres B.A. Induction of astrocyte differentiation by endothelial cells. J. Neurosci. 21:2001;1538-1547
86. Minagar A., Shapshak P., Fujimura R., Ownby R., Heyes M., Eisdorfer C. The role of macrophage/microglia and astrocytes in the pathogenesis of three neurologic disorders: HIV-associated dementia, Alzheimer disease, and multiple sclerosis. J. Neurol. Sci. 202:2002;13-23
87. Mitic L.L., Van Itallie C.M., Anderson J.M. Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins. Am. J. Physiol.: Gastrointest. Liver Physiol. 279:2000;G250-G254
88. Morita K., Sasaki H., Fujimoto K., Furuse M., Tsukita S. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J. Cell Biol. 145:1999;579-588
89. Morita K., Sasaki H., Furuse M., Tsukita S. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells. J. Cell Biol. 147:1999;185-194
90. Neuhaus J., Risau W., Wolburg H. Induction of blood-brain barrier characteristics in bovine brain endothelial cells by rat astroglial cells in transfilter coculture. Ann. N.Y. Acad. Sci. 633:1991;578-580
91. Nico B., Frigeri A., Nicchia G.P., Quondamatteo F., Herken R., Errede M., Ribatti D., Svelto M., Roncali L. Role of aquaporin-4 water channel in the development and integrity of the blood-brain barrier. J. Cell Sci. 114:2001;1297-1307
92. Nielsen S., King L.S., Christensen B.M., Agre P. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am. J. Physiol. 273:1997;C1549-C1561
93. Norenberg M.D. Astrocyte responses to CNS injury. J. Neuropathol. Exp. Neurol. 53:1994;213-230
94. Paemeleire K. The cellular basis of neurovascular metabolic coupling. Acta Neurol. Belg. 102:2002;153-157
95. Palmer T.D., Willhoite A.R., Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425:2000;479-494
96. Pan W., Kastin A.J., Gera L., Stewart J.M. Bradykinin antagonist decreases early disruption of the blood-spinal cord barrier after spinal cord injury in mice. Neurosci. Lett. 307:2001;25-28
97. Papadopoulos M.C., Lamb F.J., Moss R.F., Davies D.C., Tighe D., Bennett E.D. Faecal peritonitis causes oedema and neuronal injury in pig cerebral cortex. Clin. Sci. (Lond.). 96:1999;461-466
98. Papadopoulos M.C., Davies D.C., Moss R.F., Tighe D., Bennett E.D. Pathophysiology of septic encephalopathy: a review. Crit. Care Med. 28:2000;3019-3024
99. Papadopoulos M.C., Saadoun S., Woodrow C.J., Davies D.C., Costa-Martins P., Moss R.F., Krishna S., Bell B.A. Occludin expression in microvessels of neoplastic and non-neoplastic human brain. Neuropathol. Appl. Neurobiol. 27:2001;384-395
100. Pardridge W.M., Eisenberg J., Yang J. Human blood-brain barrier insulin receptor. J. Neurochem. 44:1985;1771-1778
101. Rakic P. Guidance of neurons migrating to the fetal monkey neocortex. Brain Res. 33:1971;471-476
102. Ramsauer M., Krause D., Dermietzel R. Angiogenesis of the blood-brain barrier in vitro and the function of cerebral pericytes. FASEB J. 16:2002;1274-1276
103. Rash J.E., Yasumura T., Hudson C.S., Agre P., Nielsen S. Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc. Natl. Acad. Sci. U.S.A. 95:1998;11981-11986
104. Rubin L.L., Barbu K., Bard F., Cannon C., Hall D.E., Horner H., Janatpour M., Liaw C., Manning K., Morales J., et al. Differentiation of brain endothelial cells in cell culture. Ann. N.Y. Acad. Sci. 633:1991;420-425
105. Saadoun S., Papadopoulos M.C., Davies D.C., Krishna S., Bell B.A. Aquaporin-4 expression is increased in oedematous human brain tumours. J. Neurol. Neurosurg. Psychiatry. 72:2002;262-265
106. Sasaki A., Hirato J., Nakazato Y., Ishida Y. Immunohistochemical study of the early human fetal brain. Acta Neuropathol. 76:1988;128-134
107. Schroeter M.L., Mertsch K., Giese H., Muller S., Sporbert A., Hickel B., Blasig I.E. Astrocytes enhance radical defence in capillary endothelial cells constituting the blood-brain barrier. FEBS Lett. 449:1999;241-244
108. Sharer L.R. Pathology of HIV-1 infection of the central nervous system. A review. J. Neuropathol. Exp. Neurol. 51:1992;3-11
109. Sobue K., Yamamoto N., Yoneda K., Hodgson M.E., 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. 35:1999;155-164
110. Sonoda N., Furuse M., Sasaki H., Yonemura S., Katahira J., Horiguchi Y., Tsukita S. Clostridium perfringens enterotoxin fragment removes specific claudins from tight junction strands: evidence for direct involvement of claudins in tight junction barrier. J. Cell Biol. 147:1999;195-204
111. St'astny F., Skultetyova I., Pliss L., Jezova D. Quinolinic acid enhances permeability of rat brain microvessels to plasma albumin. Brain Res. Bull. 53:2000;415-420
112. Stevenson B.R., Begg D.A. Concentration-dependent effects of cytochalasin D on tight junctions and actin filaments in MDCK epithelial cells. J. Cell Sci. 107:1994;367-375
113. Stewart P.A., Hayakawa K. Early ultrastructural changes in blood-brain barrier vessels of the rat embryo. Brain Res. Dev. Brain Res. 78:1994;25-34
114. Stewart P.A., Wiley M.J. Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev. Biol. 84:1981;183-192
115. Szymonowicz W., Schafler K., Cussen L.J., Yu V.Y. Ultrasound and necropsy study of periventricular haemorrhage in preterm infants. Arch. Dis. Child. 59:1984;637-642
116. Taniguchi M., Yamashita T., Kumura E., Tamatani M., Kobayashi A., Yokawa T., Maruno M., Kato A., Ohnishi T., Kohmura E., et al. Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain Res. Mol. Brain Res. 78:2000;131-137
117. Tarkowski E., Rosengren L., Blomstrand C., Wikkelso C., Jensen C., Ekholm S., Tarkowski A. Intrathecal release of pro- and anti-inflammatory cytokines during stroke. Clin. Exp. Immunol. 110:1997;492-499
118. Tighe D., Moss R., Bennett D. Cell surface adrenergic receptor stimulation modifies the endothelial response to SIRS. Systemic inflammatory response syndrome. New Horiz. 4:1996;426-442
119. Tran N.D., Correale J., Schreiber S.S., Fisher M. Transforming growth factor-beta mediates astrocyte-specific regulation of brain endothelial anticoagulant factors. Stroke. 30:1999;1671-1678
120. Tsukamoto T., Nigam S.K. Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins. Am. J. Physiol. 276:1999;F737-F750
121. Utsumi H., Chiba H., Kamimura Y., Osanai M., Igarashi Y., Tobioka H., Mori M., Sawada N. Expression of GFRalpha-1, receptor for GDNF, in rat brain capillary during postnatal development of the BBB. Am. J. Physiol.: Cell Physiol. 279:2000;C361-C368
122. van Zwieten E.J., Ravid R., Swaab D.F., Van de Woude T. Immunocytochemically stained vasopressin binding sites on blood vessels in the rat brain. Brain Res. 474:1988;369-373
123. Verbeek M.M., de Waal R.M., Schipper J.J., Van Nostrand W.E. Rapid degeneration of cultured human brain pericytes by amyloid beta protein. J. Neurochem. 68:1997;1135-1141
124. Vizuete M.L., Venero J.L., Vargas C., Ilundain A.A., Echevarria M., Machado A., Cano J. Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema. Neurobiol. Dis. 6:1999;245-258
125. Volpe J.J. Intraventricular hemorrhage in the premature infant-current concepts. Part I. Ann. Neurol. 25:1989;3-11
126. Volpe J.J. Intraventricular hemorrhage in the premature infant-current concepts. Part II. Ann. Neurol. 25:1989;109-116
127. Wekerle H., Hohlfeld R. Molecular mimicry in multiple sclerosis. N. Engl. J. Med. 349:2003;185-186
128. Wolburg H., Wolburg-Buchholz K., Liebner S., Engelhardt B. Claudin-1, claudin-2 and claudin-11 are present in tight junctions of choroid plexus epithelium of the mouse. Neurosci. Lett. 307:2001;77-80
129. Yoder E.J. Modifications in astrocyte morphology and calcium signaling induced by a brain capillary endothelial cell line. Glia. 38:2002;137-145
130. Zhang Y., Pardridge W.M. Rapid transferrin efflux from brain to blood across the blood-brain barrier. J. Neurochem. 76:2001;1597-1600
131. Zhang W., Smith C., Shapiro A., Monette R., Hutchison J., Stanimirovic D. Increased expression of bioactive chemokines in human cerebromicrovascular endothelial cells and astrocytes subjected to simulated ischemia in vitro. J. Neuroimmunol. 101:1999;148-160
132. Zhang W., Smith C., Howlett C., Stanimirovic D. Inflammatory activation of human brain endothelial cells by hypoxic astrocytes in vitro is mediated by IL-1beta. J. Cereb. Blood Flow Metab. 20:2000;967-978
133. Zonta M., Angulo M.C., Gobbo S., Rosengarten B., Hossmann K.A., Pozzan T., Carmignoto G. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat. Neurosci. 6:2003;43-50