Tight junctions of the blood-brain barrier: Development, composition and regulation

Vascular Pharmacology

Volumn 38, Issue 6, 2002, Pages 323-337

  Wolburg, Hartwig ^a   Lippoldt, Andrea ^b,c  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Blood brain barrier; Claudins; Freeze fracture; G proteins; Morphology; Occludin; Tight junction

Indexed keywords

CADHERIN; CATENIN; CELL ADHESION MOLECULE; CINGULIN; CLAUDIN; CLAUDIN 1; CLAUDIN 5; COLCHICINE; CYCLIC AMP; CYTOCHALASIN B; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANYLATE CYCLASE; JUNCTIONAL ADHESION MOLECULE A; MEMBRANE PROTEIN; OCCLUDIN; PHOSPHOTRANSFERASE; PROTEIN 7H6; PROTEIN JAM 2; PROTEIN JAM 3; PROTEIN P55; PROTEIN SERINE KINASE; PROTEIN TYROSINE KINASE; PROTEIN ZO 2; PROTEIN ZO 3; PROTEIN ZO1; THREONINE KINASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIMENTIN;

BLOOD BRAIN BARRIER; CALCIUM CELL LEVEL; CELL CONTACT; CELL MIGRATION; CELL STRUCTURE; CYTOSKELETON; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; MICROENVIRONMENT; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; SECOND MESSENGER; TIGHT JUNCTION; TRANSCYTOSIS;

EID: 0036627211     PISSN: 15371891     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1537-1891(02)00200-8     Document Type: Article

References (196)

1. Abbott N.J., Hughes C.C.W., Revest P.A., Greenwood J. Development and characterization of a rat capillary endothelial culture. Towards an in vitro BBB. J. Cell Sci. 103:1992;23-38.
2. Abrahamson D.R. Recent studies on the structure and pathology of basement membranes. J. Pathol. 149:1986;257-278.
3. Adamson P., Etienne S., Couraud P.O., Calder V., Greenwood J. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J. Immunol. 162:1999;2964-2973.
4. Ando-Akatsuka Y., Saitou M., Hirase T., Kishi M., Sakaqkibara 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;43-48.
5. Arthur F.E., Shivers R.R., Bowman P.D. Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Dev. Brain Res. 36:1987;155-159.
6. Aurrond-Lions M., Duncan L., Ballestrem C., Imhof B.A. JAM-2, a novel immunoglobulin superfamily molecule, expressed by endothelial and lymphatic cells. J. Biol. Chem. 276:2001;2733-2741.
7. Bacallao R., Garfinkel A., Monke S., Zampighi G., Mandel L.J. ATP-depletion: a novel method to study junctional properties in epithelial tissues: I. Rearrangement of the actin cytoskeleton. J. Cell Sci. 107:1994;3301-3313.
8. Balda M.S., Anderson J.M. Two classes of tight junctions are revealed by ZO-1 isoforms. Am. J. Physiol. 264:1993;C918-C924.
9. Balda M.S., Matter K. Transmembrane proteins of tight junctions. Semin. Cell Dev. Biol. 11:2000;281-289.
10. Balda M.S., Gonzáles-Mariscal L., Contreras R.G., Macias-Silva M., Torres-Marques 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.
11. Balda M.S., Gonzales-Mariscal L., Matter K., Cereijido M., Anderson J.M. Assembly of tight junction. The role of diacylglycerol. J. Cell Biol. 123:1993;293-302.
12. Balda M.S., Whitney J.A., Flores C., Gonzáles S., Cereijido M., Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol. 134:1996;1031-1049.
13. Balda M.S., Flores-Maldonado C., Cereijido M., Matter K. Multiple domains of occludin are involved in the regulation of paracellular permeability. J. Cell Biochem. 78:2000;85-96.
14. Barber A.J., Lieth E. Agrin accumulates in the brain microvascular basal lamina during development of the blood-brain barrier. Dev. Dyn. 208:1997;62-74.
15. Bauer H.C., Bauer H., Lamet-Schwandtner 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. Dev. Brain Res. 75:1993;269-278.
16. Bazzoni G., Martinez-Estrada O.M., Orsenigo F., Cordenonsi M., Citi S., Dejana E. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J. Biol. Chem. 275:2000;20520-20526.
17. Bentzel C.J., Hainau B., Ho S., Hui S.W., Edelman A., Anagnostopoulos T., Benedetti E.L. Cytoplasmic regulation of tight junction permeability: effect of plant cytokinins. Am. J. Physiol. 239:1980;C75-C89.
18. Berzin T.M., Zipser B.D., Rafii M.S., Kuo-Leblanc V., Yancopoulos G.D., Glass D.J., Fallon J.R., Stopa E.G. Agrin and microvascular damage in Alzheimer's disease. Neurobiol. Aging. 21:2000;349-355.
19. Blake D.J., Kröger S. The neurobiology of Duchenne muscular dystrophy: learning lessons from muscle? Trends Neurosci. 23:2000;92-99.
20. Boven L.A., Middel J., Verhoef J., De Groot C.J.A., Nottet H.S.L.M. Monocyte infiltration is highly associated with loss of the tight junction protein zonula occludens in HIV-1-associated dementia. Neuropathol. Appl. Neurobiol. 26:2000;354-360.
21. Brightman M.W., Reese T.S. Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40:1969;648-677.
22. Burns A.R., Bowden R.A., MacDonell S.D., Walker D.C., Odebunmi T.O., Donnachie E.M., Simon S.I., Entman M.L., Smith C.W. Analysis of tight junctions during neutrophil transendothelial migration. J. Cell Sci. 113:2000;45-57.
23. Butt A.M., Jones H.C., Abbott N.J. Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study. J. Physiol. 429:1990;47-62.
24. Cassella J.P., Lawrenson J.G., Firth J.A. Development of endothelial paracellular clefts and their tight junctions in the pial microvessels of the rat. J. Neurocytol. 26:1997;567-575.
25. Chen Y., Merzdorf C., Paul D.L., Goodenough D.A. COOH terminus of occludin is required for tight junction barrier function in early Xenopus embryos. J. Cell Biol. 138:1997;891-899.
26. Citi S., Sabanay H., Kendrick-Jones J., Geiger B. Cingulin: characterization and localization. J. Cell Sci. 93:1989;107-122.
27. Claude P. Morphologic factors influencing transepithelial permeability. A model for the resistance of the zonula occludens. J. Membr. Biol. 39:1978;219-232.
28. Claude P., Goodenough D.A. Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J. Cell Biol. 58:1973;390-400.
29. Conant K., McArthur J.C., Griffin D.E., Sjulson L., Wahl L.M., Irani D.N. Cerebrospinal fluid levels of MMP-2, -7 and -9 are elevated in association with human immunodeficiency virus dementia. Ann. Neurol. 46:1999;391-398.
30. Coomber B.L., Stewart P.A., Hayakawa K., Farrell C.L., Del Maestro R.F. Quantitative morphology of human glioblastoma multifome microvessels: structural basis of blood-brain barrier defect. J. Neuro-Oncol. 5:1987;299-307.
31. Dehouck B., Dehouck M.-P., Fruchart J.-C., Cecchelli R. Upregulation of the low density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary ECs and astrocytes. J. Cell Biol. 126:1994;465-474.
32. Dejana E., Lampugnani M.G., Martinez-Estrada O., Bazzoni G.F. The molecular organization of endothelial junctions and their functional role in vascular morphogenesis and permeability. Int. J. Dev. Biol. 44:2000;743-748.
33. DelMaschio A., Luigi A.D., Martin-Padura I., Brockhaus M., Bartfai T., Fruscella P., Adorini L., Martino G.V., Furlan R., De Simoni M.G., Dejana E. Leukocyte recruitment in the cerebrospinal fluid of mice with experimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J. Exp. Med. 190:1999;1351-1356.
34. DeMaio L., Chang Y.S., Gardner T.W., Tarbell J.M., Antonetti D. Shear stress regulates occludin content and phosphorylation. Am. J. Physiol. 281:2001;H105-H113.
35. Denker B.M., Nigam S.K. Molecular structure and assembly of the tight junction. Am. J. Physiol. 274:1998;F1-F9.
36. Denker B.M., Saha C., Khawaja S., Nigam S.K. Involvement of a heterotrimeric G protein alpha subunit in tight junction biogenesis. J. Biol. Chem. 271:1996;25750-25753.
37. De Vries L., Farquahr M.G. RGS proteins: more than just GAPs for heterotrimeric G proteins. Trends Cell Biol. 9:1999;138-144.
38. Dirnagl U., Iadecola C., Moskowitz M.A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999;391-397.
39. Dodane V., Kachar B. Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J. Membr. Biol. 149:1996;199-209.
40. Dombrowski S.M., Desai S.Y., Marroni M., Cucullo L., Goodrich K., Bingaman W., Mayberl L., Janigro D. Overexpression of multiple drug resistance gene in endothelial cells from patients with refractory epilepsy. Epilepsia. 42:2001;1501-1506.
41. Engelhardt B. The blood-brain barrier. Russell W.C. Molecular Biology of Multiple Sclerosis. 1997;137-160 Wiley, New York.
42. Essler M., Amano M., Kruse H.J., Kaibuchi K., Weber P.C., Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via rho and its target rho kinase in human endothelial cells. J. Biol. Chem. 273:1998;21867-21874.
43. Essler M., Staddon J.M., Weber P.C., Aepfelbacher M. Cyclic AMP blocks bacterial lipopolysaccharide-induced myosin light chain phosphorylation in endothelial cells through inhibition of rho/rho kinase signaling. J. Immunol. 164:2000;6543-6549.
44. Etienne S., Adamson P., Greenwood J., Strosberg A.D., Cazaubon S., Couraud P.O. ICAM-1 signaling pathways associated with rho activation in microvascular brain endothelial cells. J. Immunol. 161:1998;5755-5761.
45. Fabian R.H., Hulsebosch C.E. Time course of penetration of xenogenic IgG into the central nervous system of the neonatal rat: an immunohistochemical and radionuclide tracer study. J. Neuroimmunol. 24:1989;183-189.
46. Fabian G., Szabo C.A., Bozo B., Greenwood J., Adamson P., Deli M.A., Joo F., Krizbai I.A., Szücs M. Expression of G-protein subtypes in cultured cerebral endothelial cells. Neurochem. Int. 33:1998;179-185.
47. Fallier-Becker P., Betz E., Wolburg-Buchholz K., Fotev Z. Fibromuscular proliferates induced in vitro using a trans-filter culture system. Res. Exp. Med. 191:1991;11-25.
48. Farquhar M.G., Palade G.E. Junctional complexes in various epithelial. J. Cell Biol. 17:1963;375-412.
49. 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.
50. Franke H., Galla H.-J., Beuckmann C.T. 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. Protoc. 5:2000;248-256.
51. Frigeri A., Nicchia G.P., Nico B., Quondamatteo F., Herken R., Roncali L., Svelto M. Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. FASEB J. 15:2001;90-98.
52. 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.
53. Furuse M., Itoh M., Hirase T., Nagafuchi A., Yonemura S., Tsukita S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 127:1994;1617-1626.
54. Furuse M., Fujita K., Hiiragi T., Fujimoto K., Tsukita S. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions. J. Cell Biol. 141:1998;1539-1550.
55. Furuse M., Sasaki H., Fujimoto K., Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J. Cell Biol. 143:1998;391-401.
56. Furuse M., Sasaki H., Tsukita S. Manner of interaction of heterogenous claudin species within and between tight junction strands. J. Cell Biol. 147:1999;891-903.
57. Furuse M., Furuse K., Sasaki H., Tsukita S. Conversion of Zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J. Cell Biol. 153:2001;263-272.
58. Gaillard P.J., Voorwinden L.H., Nielsen J.L., Ivanov A., Atsumi R., Engman H., Ringbom C., De Boer A.G., Breimer D.D. 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. Pharmacol. Sci. 12:2001;215-222.
59. Garcia J.G.N., Wang P., Liu F., Hershenson M.B., Borbiev T., Verin A.D. Pertussis toxin directly activates endothelial cell p42/p44 MAP kinases via a novel signaling pathway. Am. J. Physiol. 280:2001;C1233-C1241.
60. Gee S.H., Montanaro F., Lindenbaum M.H., Carbonetto S. Dystroglycan-α: a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell. 77:1994;675-686.
61. Gladson C.L. The extracellular matrix of gliomas: modulation of cell function. J. Neuropathol. Exp. Neurol. 58:1999;1029-1040.
62. Gonzáles-Mariscal L., Chavez de Ramirez B., Cereijido M. Tight junction formation in cultured epithelial cells (MDCK). J. Membr. Biol. 86:1985;113-121.
63. Gonzáles-Mariscal L., Betanzos A., Ávila-Flores A. MAGUK proteins: structure and role in the tight junction. Cell Dev. Biol. 11:2000;315-324.
64. Gow A., Southwood C.M., Li J.S., Pariali M., Riorsan G.P., Brodie S.E., Danias J., Bronstein J.M., Kachar B., Lazzarini R.A. CNS myelin and Sertzoli cell tight junction strands are absent in OSP/Claudin-11 null mice. Cell. 99:1999;649-659.
65. Granderath S., Stollewerk A., Greig S., Goodman C.S., O'Kane K.C. Loco encodes an RGS protein required for Drosophila glial differentiation. Development. 126:1999;1781-1791.
66. Grebenkämper K., Galla H.-J. Translational diffusion measurements of a fluorescent phospholipid between MDCK-1 cells support the lipid model of the tight junctions. Chem. Phys. Lipids. 71:1994;133-143.
67. Griepp E.B., Dolan W.J., Robbins E.S., Sabatini D.D. Participation of plasma membrane proteins in the formation of tight junctions by cultured epithelial cells. J. Cell Biol. 96:1983;693-702.
68. Gumbiner B., Simons K. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of an uvomorulin-like polypeptide. J. Cell Biol. 102:1986;457-468.
69. Hamann G.F., Okada Y., Fitridge R., del Zoppo G.J. Microvascular basal lamina antigens disappear during cerebral ischemia and reperfusion. Stroke. 26:1995;2120-2126.
70. Hamazaki Y., Itoh M., Sasaki H., Furuse M., Tsukita S. Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J. Biol. Chem. 277:2002;455-461.
71. 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.
72. 2+ , protamine and protons. Chem. Phys. Lipids. 63:1992;223-233.
73. Heiskala M., Peterson P.A., Yang Y. The roles of claudin superfamily proteins in paracellular transport. Traffic. 2:2001;92-98.
74. Hermansson M., Nister M., Betsholtz C., Heldin C.H., Westermark B., Funa K. Endothelial cell hyperplasia in human glioblastoma: coexpression of mRNA for platelet-derived growth factor (PDGF) B chain and PDGF receptor suggests autocrine growth stimulation. Proc. Natl. Acad. Sci. U. S. A. 85:1988;7748-7752.
75. 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 ECs. J. Cell Sci. 110:1997;1603-1613.
76. Hirase T., Kawashima S., Wong E.Y.M., Ueyama T., Rikitake Y., Tsukita S., Yokoyama M., Staddon J.M. Regulation of tight junction permeability and occludin phosphorylation by RhoA-p160ROCK-dependent and -independent mechanisms. J. Biol. Chem. 276:2001;10423-10431.
77. Hirata K.-I., Ishida T., Penta K., Rezaee M., Yang E., Wohlgemuth J., Quertermous T. Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J. Biol. Chem. 276:2001;16223-16231.
78. Holash J., Maisonpierre P.C., Compton D., Boland P., Alexander C.R., Zagzag D., Yancopoulos G.D., Wiegand S.J. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 284:1999;1994-1998.
79. Huber D., Balda M.S., Matter K. Occludin modulates transepithelial migration of neutrophils. J. Biol. Chem. 275:2000;5773-5778.
80. Huber J.D., Egleton R.D., Davis T.P. Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier. Trends Neurosci. 24:2001;719-725.
81. Igarashi Y., Utsumi H., Chiba H., Yamada-Sasamori Y., Tobioka H., Furuuchi K., Kokai Y., Nakagawa T., Mori M., Sawada N. Glial cell line-derived neurotrophic factor (GDNF) enhances barrier function of endothelial cells forming the blood-brain barrier. Biochem. Biophys. Res. Commun. 261:1999;108-112.
82. Inai T., Kobayashi J., Shibata Y. Claudin-1 contributes to the epithelial barrier function in MDCK cells. Eur. J. Cell Biol. 78:1999;849-855.
83. Itoh M., Nagafuchi A., Yonemura S., Kitaniyasuda T., Tsukita S. The 220 kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction associated protein in epithelial cells - cDNA cloning and immunoelectron microscopy. J. Cell Biol. 121:1993;491-502.
84. 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.
85. Jesaitis L.A., Goodenough D.A. Molecular characterization and tissue distribution of ZO-2, a tight junction protein homologous to ZO-1 and the Drosophila discs large tumor suppressor protein. J. Cell Biol. 124:1994;949-962.
86. Johanson C.E. Permeability and vascularity of the developing brain: cerebellum vs. cerebral cortex. Brain Res. 190:1980;3-16.
87. Johnson-Léger C., Aurrand-Lions M., Imhof B.A. The parting of the endothelium: miracle, or simply a junctional affair? J. Cell Sci. 113:2000;921-933.
88. Jones F.S., Jones P.L. The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev. Dyn. 218:2000;235-259.
89. Jones P.L., Crack J., Rabinovitch M. Regulation of tenascin-C, a vascular smooth muscle cell survival factor that interacts with the alpha V beta 3 integrin to promote epidermal growth factor receptor phosphorylation and growth. J. Cell Biol. 139:1997;279-293.
90. Jou T.S., Nelson W.J. Effects of regulated expression of mutant rhoA and rac1 small GTPases on the development of epithelial (MDCK) cell polarity. J. Cell Biol. 142:1998;85-100.
91. Jou T.S., Schneeberger E.E., Nelson W.J. Structural and functional regulation of tight junctions by rhoA and rac1 small GTPases. J. Cell Biol. 142:1998;101-115.
92. Kan F.W.K. Cytochemical evidence for the presence of phospholipids in epithelial tight junction strands. J. Histochem. Cytochem. 41:1993;649-656.
93. Ke C., Poon W.S., Ng H.K., Pang J.C.S., Chan Y. Heterogenous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci. Lett. 301:2001;21-24.
94. Kirsch T., Wellner M., Haller H., Lippoldt A. Altered gene expression in cerebral capillaries of stroke-prone spontaneously hypertensive rats. Brain Res. 910:2001;106-115.
95. Kniesel U., Wolburg H. Tight junction complexity in the retinal pigment epithelium of the chicken during development. Neurosci. Lett. 149:1993;71-74.
96. Kniesel U., Wolburg H. Tight junctions of the blood-brain barrier. Cell. Mol. Neurobiol. 20:2000;57-76.
97. Kniesel U., Risau W., Wolburg H. Development of blood-brain barrier tight junctions in the rat cortex. Dev. Brain Res. 96:1996;229-240.
98. Lacaz-Vieira F., Jaeger M.M.M., Farshori P., Kachar B. Small synthetic peptides homologous to segments of the first loop of occludin impair tight junction resealing. J. Membr. Biol. 168:1999;289-297.
99. Lassmann H. Comparative Neuropathology of Chronic Experimental Allergic Encephalomyelitis and Multiple Sclerosis. 1983;Springer-Verlag, Berlin.
100. Li J.Y., Boado R.J., Pardridge W.M. Blood-brain barrier genomics. J. Cereb. Blood Flow Metab. 21:2001;61-68.
101. Liebner S., Fischmann A., Rascher G., Duffner F., Grote E.-H., Wolburg H. Claudin-1 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol. 100:2000;323-331.
102. 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.
103. Liedtke W., Edelmann W., Bieri P.L., Chiu F.-C., Cowan N.J., Kucherlapati R., Raine C.S. GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron. 17:1996;607-615.
104. 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.
105. Lippoldt A., Liebner S., Andbjer B., Kalbacher H., Wolburg H., Haller H., Fuxe K. Organization of choroid plexus epithelial and endothelial cell tight junctions and regulation of claudin-1, -2 and -5 expression by protein kinase C. NeuroReport. 11:2000;1427-1431.
106. Lippoldt, A., Kirsch, T., Rascher, G., Wegener, J., Reichel, M., Wellner, M., Kalbacher, H., Galla, H.-J., Wolburg, H., Haller, H. RGS5 is a new tight junction associated protein in endothelial and epithelial cells, submitted.
107. Liu F., Verin A.D., Borbiev T., Garcia J.G.N. Role of cAMP-dependent protein kinase A activity in endothelial cell cytoskeleton rearrangement. Am. J. Physiol. 280:2001;L1309-L1317.
108. Long D.M. Capillary ultrastructure and the blood-brain barrier in human malignant brain tumors. J. Neurosurg. 32:1970;127-144.
109. Lu R., Wang W., Uzzau S., Vigorito R., Zielke H.R., Fasano A. Affinity purification and partial characterization of the zonulin/zonula occludens toxin (Zot) receptor from human brain. J. Neurochem. 2000;320-326.
110. Lue R., Marfatia S.M., Branton D., Chishti A.H. Cloning and characterization of hdlg: the human homologue of the Drosophila disc large tumor suppressor binds to protein 4.1. Proc. Natl. Acad. Sci. U. S. A. 91:1994;9818-9822.
111. Lum H., Malik A.B. Mechanisms of increased endothelial permeability. Can. J. Physiol. Pharmacol. 74:1996;787-800.
112. Madara J.L. Regulation of the movement of solutes across tight junctions. Ann. Rev. Physiol. 60:1998;143-159.
113. Madara J.L., Dharmsathaphorn K. Occluding junction structure-function relationships in a cultured epithelial monolayer. J. Cell Biol. 101:1985;2124-2133.
114. Maisonpierre P.C., Suri C., Jones P.F., Bartunkova S., Wiegand S.J., Radziejewski C., Compton D., McClain J., Aldrich T.H., Papadopoulos N., Daly T.J., Davis S., Sato T.N., Yancopoulos G.D. Angiopoietin-2, a natural antagonist for tie2 that disrupts in vivo angiogenesis. Science. 277:1997;55-60.
115. Mandel L.J., Bacallao R., Zampighi G. Uncoupling of the molecular "fence" and paracellular "gate" functions in epithelial tight junctions. Nature. 361:1993;552-555.
116. Manley G.T., Fujimura M., Ma T., Noshita N., Fliz F., Bollen A.W., Chan P., Verkman A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 6:2000;159-163.
117. Marcial M.A., Carlson S.L., Madara J.L. Partitioning of paracellular conductance along the ileal crypt-villus axis: a hypothesis based on structural analysis with detailed consideration of tight junction structure-function relationship. J. Membr. Biol. 80:1984;59-70.
118. Martinez-Estrada M.O., Villa A., Breviario F., Orsenigo F., Dejana E., Bazzoni G. Association of junctional adhesion molecule with calcium/calmodulin-dependent serine protein kinase (CASK/LIN-2) in human epithelial Caco-2 cells. J. Biol. Chem. 276:2001;9291-9296.
119. Martinez-Palomo A., Meza I., Beaty G., Cereijido M. Experimental modulation of occluding junctions in a cultured transporting epithelium. J. Cell Biol. 87:1980;736-745.
120. Martin-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., Panzeri C., Stoppacciaro A., Ruco L., Villa A., Simmons D., Dejana E. 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.
121. Mayhan W.G. Leukocyte adherence contributes to disruption of the blood-brain barrier during activation of mast cells. Brain Res. 869:2000;112-120.
122. McMahon U.J. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55:1990;407-418.
123. Méresse S., Dehonk M.-P., Delorme P., Bensaid M., Tauber J.-P., Delbart C., Fruchart J.-C., Cecchelli R. Bovine brain ECs express tight junctions and monoamine oxidase activity in long-term culture. J. Neurochem. 53:1989;1363-1371.
124. Mies G., Hermann D., Ganten U., Hossmann K.A. Hemodynamics and metabolism in stroke-prone spontaneously hypertensive rats before manifestation of brain infarcts. J. Cereb. Blood Flow Metab. 19:1999;1238-1246.
125. Mitic L.C., 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. 279:2000;G250-G254.
126. Miyamori H., Takino T., Kobayashi Y., Tokai H., Itoh Y., Seiki M., Sato H. Claudin promotes activation of Pro-MMP-2 mediated by membrane-type matrix metalloproteinases. J. Biol. Chem. 276:2001;28204-28211.
127. Mollgard K., Saunders N.R. The development of the human blood-brain and blood-CSF barriers. Neuropathol. Appl. Neurobiol. 12:1986;337-358.
128. Moolenaar W.H. Lysophosphatidic acid: a multifunctional phospholipid messenger. J. Biol. Chem. 270:1995;12949-12952.
129. Morita K., Furuse M., Fujimoto K., Tsukita S. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. U. S. A. 96:1999;511-516.
130. Morita K., Sasaki H., Fujimoto K., Furuse M., Tsukita M. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J. Cell Biol. 145:1999;579-588.
131. 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.
132. Mühleisen H., Wolburg H., Betz E. Freeze-fracture analysis of endothelial cell membranes in rabbit carotid arteries subjected to short-term atherogenic stimuli. Virchows Arch., B Pathol. 56:1989;413-417.
133. Nabeshima S., Reese T.S., Landis D.M., Brightman M.W. Junctions in the meninges and marginal glia. J. Comp. Neurol. 164:1975;127-170.
134. Nag S. Role of the endothelial cytoskeleton in blood-brain barrier permeability to protein. Acta Neuropathol. 90:1995;454-460.
135. Nagy Z., Peters H., Hüttner I. Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab. Invest. 50:1984;313-322.
136. Nasdala I., Wolburg-Buchholz K., Wolburg H., Kuhn A., Ebnet K., Brachtendorf T., Samulowitz U., Kuster B., Engelhardt B., Vestweber D., Butz S. A transmembrane tight junction protein selectively expressed on endothelial cells and platelets. J. Biol. Chem. 277:2002;16294-16303.
137. Neely J.D., Amiry-Moghaddam M., Ottersen O.P., Froehner S.C., Agre P., Adams M.E. Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc. Natl. Acad. Sci. U. S. A. 98:2001;14108-14113.
138. 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.
139. Nielsen S., Nagelhus E.A., Amiry-Moghaddam M., Bourque C., Agre P., Ottersen O.P. Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17:1997;171-180.
140. Noske W., Hirsch M. Morphology of tight junctions in the ciliary epithelium of rabbits during arachidonic acid-induced breakdown of the blood-aqueous barrier. Cell Tissue Res. 245:1986;405-412.
141. Nusrat A., Giry M., Turner J.R., Colgan S.P., Parkos D., Lemichez E., Boquet P., Madara J.L. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc. Natl. Acad. Sci. U. S. A. 92:1995;10629-10633.
142. Palmeri D., van Zante A., Huang C.C., Hemmerich S., Rosen S.D. Vascular endothelial junction-associated molecule, a novel member of the immunoglobulin superfamily, is localized to intercellular boundaries of endothelial cells. J. Biol. Chem. 275:2000;19139-19145.
143. Patterson C.E., Stasek J.E., Schaphorst K.L., Davis H.W., Gaercia J.G.N. Mechanisms of pertussis toxin induced barrier dysfunction in bovine pulmonary artery endothelial cell monolayers. Am. J. Physiol. 268:1995;L926-L934.
144. Pekny M., Stanness K.A., Eliasson C., Betsholtz C., Janigro D. Impaired induction of blood-brain barrier properties in aortic endothelial cells by astrocytes from GFAP-deficient mice. Glia. 22:1998;390-400.
145. Pekny M., Johannson C.B., Eliasson C., Stakeberg J., Wallén A., Perlmann T., Lendahl U., Betsholtz C., Berthold C.-H., Frisén J. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J. Cell Biol. 145:1999;503-514.
146. Plate K.H., Breier G., Farrell C.L., Risau W. Platelet-derived growth factor receptor-beta is induced during tumor development and upregulated during tumor progression in endothelial cells in human gliomas. Lab. Invest. 67:1992;529-534.
147. Rahner C., Mitic L.L., Anderson J.M. Heterogeneity in expression and subcellular localization of claudins 2, 3, 4, and 5 in rat liver, pancreas, and gut. Gastroenterology. 120:2001;411-422.
148. Rascher G., Wolburg H. The tight junctions of the leptomeningeal blood-cerebrospinal fluid barrier during development. J. Brain Res. 38:1997;525-540.
149. Rascher G., Fischmann A., Kröger S., Duffner F., Grote E.-H., Wolburg H. Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin. Acta Neuropathol. 104:2002;85-91.
150. 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.
151. Reese T.S., Karnovsky M.J. Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol. 34:1967;207-217.
152. Rubin L.L., Staddon J.M. The cell biology of the blood-brain barrier. Ann. Rev. Neurosci. 22:1999;11-28.
153. Rubin L.L., Hall D.E., Porter S., Barbu K., Cannon C., Horner H.C., Janatpour M., Liaw C.W., Manning K., Morales J., Tanner L.J., Tomaselli K.J., Bard F. A cell culture model of the blood-brain barrier. J. Cell Biol. 115:1991;1725-1736.
154. Saha C., Nigam S.K., Denker B.M. Involvement of Gαi2 in the maintenance and biogenesis of epithelial cell tight junctions. Biol. Chem. 273:1998;21629-21633.
155. Saitou M., Furuse M., Sasaki H., Schulzke J.-D., Fromm M., Takano H., Noda T., Tsukita S. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell. 11:2000;4131-4142.
156. Sakakibara A., Furuse M., Saitou M., Ando-Akatsuka Y., Tsukita S. Possible involvement of phosphorylation of occludin in tight junction formation. J. Cell Biol. 137:1997;1393-1401.
157. Savettieri G., Di Liegro I., Catania C., Licata L., Pitarresi G.L., D'Agostino S., Schiera G., De Caro V., Giandalia L.I., Giannola L.I., Cestelli A. Neurons and ECM regulate occludin localization in brain endothelial cells. NeuroReport. 11:2000;1081-1084.
158. Schulze C., Firth J.A. Interendothelial junctions during blood-brain barrier development in the rat. Morphological changes at the level of individual tight junctional contacts. Dev. Brain Res. 69:1992;85-96.
159. Schulze C., Firth J.A. Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. J. Cell Sci. 104:1993;773-782.
160. Schulze C., Smales C., Rubin L.L., Staddon J.M. Lysophosphatidic acid increases tight junctional permeability in cultured brain ECs. J. Neurochem. 68:1997;991-1000.
161. Sears C.L. Molecular physiology and pathophysiology of tight junctions: V. Assault of the tight junction by enteric pathogens. Am. J. Physiol. 279:2000;G1129-G1134.
162. Shivers R.R., Arthur F.E., Bowman P.D. Induction of gap junctions and brain endothelium-like tight junctions in cultured bovine endothelial cells. Local control of cell specialization. J. Submicrosc. Cytol. Pathol. 20:1988;1-14.
163. Simionescu M., Simionescu N., Palade G.E. Segmental differentiations of cell junctions in the vascular endothelium. Arteries and veins. J. Cell Biol. 68:1976;705-723.
164. 2+ resorption. Science. 285:1999;103-106.
165. 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.
166. Stanimirovic D., Satoh K. Inflammatory mediators of cerebral endothelium: a role in ischemic brain inflammation. Brain Pathol. 10:2000;113-126.
167. Stanness K.A., Neumaier J.F., Sexton T.J., Grant G.A., Emmi A., Maris D.O., Janigro D. A new model of the blood-brain barrier: coculture of neuronal, endothelial and glial cells under dynamic conditions. NeuroReport. 10:1999;3725-3731.
168. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 103:1986;755-766.
169. Stewart P.A., Hayakawa E.M. Interendothelial junctional changes underlie the developmental "tightening" of the blood-brain barrier. Dev. Brain Res. 32:1987;271-281.
170. Stewart P.A., Hayakawa K. Early ultrastructural changes in blood-brain barrier vessels of the rat embryo. Dev. Brain Res. 78:1994;25-34.
171. Tagami M., Yamagata K., Fujino H., Kubota A., Nara Y., Yamori Y. Morphological differentiation of endothelial cells co-cultured with astrocytes on type-I or type-IV collagen. Cell Tissue Res. 268:1992;225-232.
172. Tao-Cheng J.-H., Nagy Z., Brightman M.W. Tight junctions of brain endothelium in vitro are enhanced by astroglia. J. Neurosci. 7:1987;3293-3299.
173. Tontsch U., Bauer H.C. Glial cells and neurons induce blood brain barrier related enzymes in cultured cerebral ECs. Brain Res. 539:1991;247-253.
174. Tsukita S., Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol. 9:1999;268-273.
175. Tsukita S., Furuse M. Pores in the wall: claudins constitute tight junction strands containing aqueous pores. J. Cell Biol. 149:2000;13-16.
176. Tsukita S., Furuse M., Itoh M. Multifunctional strands in tight junctions. Nat. Rev., Mol. Cell Biol. 2:2001;285-293.
177. Utsumi H., Chiba H., Kamimura Y., Osanai M., Igarashi Y., Tobioka H., Mori M., Sawada N. Expression of GFRa-1, receptor for GDNF, in rat brain capillary during postnatal development of the BBB. Am. J. Physiol. 279:2000;C361-C368.
178. Van Deurs B., Koehler J.K. Tight junctions in the choroid plexus epithelium. A freeze-fracture study including complementary replicas. J. Cell Biol. 80:1979;662-673.
179. Venero J.L., Vizuete M.L., Machado A., Cano J. Aquaporins in the central nervous system. Prog. Neurobiol. 63:2001;321-336.
180. Verin A.D., Liu F., Bogatcheva N., Borbiev T., Hershenson M.B., Wang P., Garcia J.G. Role of ras-dependent ERK activation in phorbol ester-induced endothelial cell barrier dysfunction. Am. J. Physiol. 279:2000;L360-L370.
181. Vorbrodt A.W., Dobrogowska D.H., Kim Y.S., Lossinsky A.S., Wisniewski H.M. Ultrastructural studies of glycoconjugates in brain micro-blood vessels and amyloid plaques of scrapie-infected mice. Acta Neuropathol. (Berl.). 75:1988;277-287.
182. Wakai S., Hirokawa N. Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tissue Res. 195:1978;195-203.
183. Westermark J., Kahari V.M. Regulation of matrix metalloproteinase expression in tumor invasion. FASEB J. 13:1999;781-792.
184. Wojciak-Stothard B., Entwistle A., Garg R., Ridley A.J. Regulation of TNF-α-induced reorganization of the actin cytoskeleton and cell-cell junctions by rho, rac, and cdc42 in human endothelial cells. J. Cell Physiol. 176:1998;150-165.
185. Wolburg H. Orthogonal arrays of intramembranous particles. A review with special reference to astrocytes. J. Brain Res. 36:1995;239-258.
186. Wolburg H. Glia-neuronal and glia-vascular interrelations in blood-brain barrier formation and axon regeneration in vertebrates. Vernadakis A., Roots B. Neuro-Glial Interactions during Phylogeny. 1995;479-510 Humana Press, Totowa, NJ.
187. Wolburg H., Risau W. Formation of the blood-brain barrier. Kettenmann H., Ransom B.R. Neuroglia. 1995;763-776 Oxford Univ. Press, New York, Oxford.
188. Wolburg H., Neuhaus J., Kniesel U., Krauss B., Schmid E.-M., Öcalan M., Farrell C., Risau W. Modulation of tight junction structure in blood-brain barrier ECs. Effects of tissue culture, second messengers and cocultured astrocytes. J. Cell Sci. 107:1994;1347-1357.
189. 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.
190. Wong V., Gumbiner B.M. A synthetic peptide corresponding to the extracellular domain of occludin perturbs the tight junction permeability barrier. J. Cell Biol. 136:1997;399-409.
191. Yagi T., Jikihara I., Fukumura M., Watabe K., Ohashi T., Eto Y., Hara M., Maeda M. Rescue of ischemic brain injury by adenoviral gene transfer of glial cell line-derived factor after transient global ischemia in gerbils. Brain Res. 885:2000;273-282.
192. Yoshida Y., Okano M., Wang S., Kobayashi M., Kawasumi M., Hagiwara H., Mitsumata M. Hemodynamic-force-induced difference of interendothelial junctional complexes. Ann. NY Acad. Sci. 748:1995;104-120.
193. Yurchenko P.D., Schittny J.C. Molecular architecture of basement membranes. FASEB J. 4:1990;1577-1590.
194. Zagzag D., Hooper A., Friedlander D.R., Chan W., Holash J., Wiegand S.J., Yancopoulus G.D., Grumet M. In situ expression of angiopoietins in astrocytomas identifies angiopoietin-2 as an early marker of tumor angiogenesis. Exp. Neurol. 159:1999;391-400.
195. Zampighi G., Bacallao R., Mandel L., Cereijido M. Structural differences of the tight junction between low and high resistance MDCK monolayers. J. Cell Biol. 115:1991;479a.
196. Zhong Y., Enomoto K., Isomura H., Sawada N., Minase T., Oyamada M., Konishi Y., Mori M. Localization of the 7H6 antigen at tight junctions correlates with the paracellular barrier function of MDCK cells. Exp. Cell Res. 214:1994;614-620.