Differential expression of endothelial β-catenin and plakoglobin during development and maturation of the blood-brain and blood-retina barrier in the chicken

Developmental Dynamics

Volumn 217, Issue 1, 2000, Pages 86-98

  Liebner, Stefan ^a   Gerhardt, Holger ^a   Wolburg, Hartwig ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

Author keywords

Blood brain barrier; Cell adhesion; Chicken; Pericytes; Tight junction

Indexed keywords

BETA CATENIN; PLAKOGLOBIN;

ANGIOGENESIS; ARTICLE; BLOOD BRAIN BARRIER; BLOOD RETINA BARRIER; CHICK EMBRYO; EMBRYO; EMBRYO DEVELOPMENT; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOGOLD STAINING; LASER MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; TIGHT JUNCTION; VASCULAR ENDOTHELIUM;

ANIMALS; BETA CATENIN; BLOOD-BRAIN BARRIER; BLOOD-RETINAL BARRIER; CELL DIFFERENTIATION; CHICK EMBRYO; CYTOSKELETAL PROTEINS; DESMOPLAKINS; EMBRYONIC AND FETAL DEVELOPMENT; ENDOTHELIUM, VASCULAR; GAMMA CATENIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; TRANS-ACTIVATORS;

AVES; EUKARYOTA; GALLUS GALLUS; VERTEBRATA;

EID: 0033987471     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(200001)217:1<86::AID-DVDY8>3.0.CO;2-E     Document Type: Article

References (39)

1. Behrens J, von Kries JP, Kühl M, Bruhn L, Wedlich D, Grosschedl R, Birchmeier W. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 382:638-642.
2. Bierkamp C, McLaughlin KJ, Schwarz H, Huber O, Kemler R. 1996. Embryonic heart and skin defects in mice lacking plakoglobin. Dev Biol 180:780-785.
3. Bowman PD, Betz AL, Ar D, Wolinsky JS, Penney JB, Shivers RR, Goldstein GW. 1981. Primary culture of capillary endothelium from rat brain. In Vitro 17:353-362.
4. Bowman PD, Ennis SR, Rarey KE, Betz AL, Goldstein GW. 1983. Brain microvessel endothelial cells in tissue culture: a model for study of blood-brain barrier permeability. Ann Neurol 14:396-402.
5. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E. 1999. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98:147-157.
6. Engelhardt B, Risau W. 1995. Development of the blood-brain barrier. In: Greenwood Jea, Editor. New Concepts of a blood-brain barrier. New York: Plenum Press, p 11-31.
7. Fagotto F, Gluck U, Gumbiner BM. 1998. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr Biol 8:181-190.
8. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita SA, Tsukita SH. 1993. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777-1788.
9. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita SH. 1998. Claudin-1 and -2: novel integral membrane proteines localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141: 1539-1550.
10. 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 Tiss Res 285:91-100.
11. Gerhardt H, Liebner S, Redies C, Wolburg H. 1999. N-cadherin expression in endothelial cells during early angiogenesis in the eye and brain of the chicken: relation to blood-retina/blood-brain barrier development. Eur J Neurosci 11:1191-1201.
12. Gory-Fauré S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P. 1999. Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126:2093-2102.
13. Gumbiner B, Simons K. 1986. A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J Cell Biol 102:457-468.
14. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R. 1995. Lack of beta-catenin affects mouse development at gastrulation. Development 121: 3529-3537.
15. Herrenknecht K, Ozawa M, Eckerskorn C, Lottspeich F, Leuter M, Kemler R. 1991. The uvomorulin-anchorage protein alpha-catenin is a vinculin homologue. Proc Natl Acad Sci USA 88:9156-9160.
16. Huber O, Krohn M, Kemler R. 1997. A specific domain in alpha-catenin mediates binding to beta-catenin or plakoglobin. J Cell Sci 110:1759-1765.
17. Knudsen KA, Frankowski C, Johnson KR, Wheelock MJ. 1998. A role for cadherins in cellular signaling and differentiation. J Cell Biochem Suppl 30-31:168-176.
18. Kowalczyk AP, Navarro P, Dejana E, Bornslaeger EA, Green KJ, Kopp DS, Borgwardt JE. 1998. VE-cadherin and desmoplakin are assembled into dermal microvascular endothelial intercellular junctions: a pivotal role for plakoglobin in the recruitment of desmoplakin to intercellular junctions. J Cell Sci 111:3045-3057.
19. Lampugnani MG, Corada M, Caveda L, Breviario F, Ayalon O, Geiger B, Dejana E. 1995. The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, beta-catenin and alpha-catenin with vascular endothelial cadherin (VE-cadherin). J Cell Biol 129:203-217.
20. 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.
21. Lindahl P, Johansson BR, Leveen P, Betsholtz C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242-245.
22. McCrea PD, Gumbiner BM. 1991. Purification of a 92-kDa cytoplasmic protein tightly associated with the cell-cell adhesion molecule E-cadherin (uvomorulin). Characterization and extractability of the protein complex from the cell cytostructure. J Biochem Chem 266: 4514-4520.
23. Miller JR, Moon RT. 1996. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Gen Dev 10:2527-2539.
24. Miskevich F, Zhu Y, Ranscht B, Sanes JR. 1998. Expression of multiple cadherins and catenins in the chick optic tectum. Mol Cell Neurosci 12:240-255.
25. Morita K, Furuse M, Fujimoto K, Tsukita S. 1999. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96:511-516.
26. Munemitsu S, Albert I, Souza B, Rubinfeld B, Polakis P. 1995. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc Natl Acad Sci USA 92:3046-3050.
27. Nagafuchi A, Takeichi M. 1989. Transmembrane control of cadherin-mediated cell adhesion: a 94-kD protein functionally associates with a specific region of the cytoplasmic domain of E-cadherin. Cell Reg 1:37-44.
28. Navarro P, Ruco L, Dejana E. 1998. Differential localization of VE-and N-cadherin in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol 140:1475-1484.
29. Nelson W. 1992. Regulation of cell surface polarity from bacteria to mammals. Science 258:948-955.
30. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO. 1997. Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64-78.
31. Risau W, Engelhardt B, Wekerle H. 1990. Immune function of the blood-brain barrier: incomplete presentation of protein (auto-)antigens by rat brain microvascular endothelium in vitro. J Cell Biol 110:1757-1766.
32. Rodriguez-Boulan E, Nelson WJ. 1989. Morphogenesis of the polarized epithelial cell phenotype. Science 245:718-725.
33. Sacco PA, McGranahan TM, Wheelock MJ, Johnson KR. 1995. Identification of plakoglobin domains required for association with N-cadherin and alpha-catenin. J Biol Chem 270:20201-20206.
34. Schnittler H-J, Püschel B, Drenckhahn D. 1997. Role of cadherins and plakoglobin in interendothelial adhesion under resting conditions and shear stress. Am J Physiol 273:2396-2405.
35. Schulze C, Firth JA. 1993. Immunohistochemical localization of adherens junction components in blood-brain barrier microvessels of the rat. J Cell Sci 104:773-782.
36. Vleminckx K, Kemler R. 1999. Cadherins and tissue formation: integrating adhesion and signaling. Bioessays 21:211-220.
37. Voorhout W. 1991. Preservation and immunogold localization of lipids by freeze-substitution and low temperature embedding. Scan Microsc Suppl 5:S17-S25.
38. Wolburg H, Liebner S, Reichenbach A, Gerhardt H. 1999. The pecten oculi of the chicken: a model system for differentiation and barrier maturation. Int Rev Cytol 187:111-159.
39. Yost C, Torres M, Miller JR, Huang E, Kimelman D, Moon RT. 1996. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3. Genes Dev 10:1443-1454.