Endothelial cell-cell junctions: Happy together

Nature Reviews Molecular Cell Biology

Volumn 5, Issue 4, 2004, Pages 261-270

  Dejana, Elisabetta ^a,b  

^a UNIVERSITY OF MILAN   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AFADIN; BINDING PROTEIN; CADHERIN; CALMODULIN; CD31 ANTIGEN; CELL ADHESION MOLECULE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GUANYLATE KINASE; IMMUNOGLOBULIN; MEMBRANE PROTEIN; NECTIN; PHOSPHATASE; PROTEIN DERIVATIVE; PROTEIN SERINE KINASE; STAT PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2; VINCULIN;

ANGIOGENESIS; APOPTOSIS; BLOOD FLOW; BLOOD VESSEL; CELL ACTIVITY; CELL ADHESION; CELL GROWTH; CELL JUNCTION; CELL PROLIFERATION; CELL PROTECTION; CELL STRUCTURE; COMPLEX FORMATION; DESMOSOME; DISULFIDE BOND; ENDOTHELIUM CELL; EPITHELIUM CELL; GENE EXPRESSION; GROWTH INHIBITION; HOMEOSTASIS; HUMAN; LEUKOCYTE; MESENCHYME CELL; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOLECULAR MECHANICS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; REVIEW; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ANIMALS; CELL ADHESION MOLECULES; CELL COMMUNICATION; CELL DIVISION; ENDOTHELIAL CELLS; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; HOMEOSTASIS; INTERCELLULAR JUNCTIONS; LEUKOCYTES;

EID: 1842632667     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1357     Document Type: Review

References (115)

1. Dvorak, A. et al. The vesiculo-vacuolar organelle (VVO): a distinct endothelial cell structure that provides a transcellular pathway for macromolecular extravasation. J. Leukocyte Biol. 59, 100-115 (1996).
2. Stevens, T., Garcia, J. G., Shasby, D. M., Bhattacharya, J. & Malik, A. B. Mechanisms regulating endothelial cell barrier function. Am. J. Physiol. Lung Cell Mol. Physiol. 279, L419-L422 (2000).
3. Matter, K. & Balda M. S. Signalling to and from tight junctions. Nature Rev. Mol. Cell Biol. 4, 225-236 (2003). A review on the mechanisms of bidirectional signalling to and from tight junctions.
4. Braga, V. M. Cell-cell adhesion and signaling. Curr. Opin. Cell Biol. 14, 546-556 (2002). A review on the role of small GTPases in the regulation of junction organization and signalling.
5. Wheelock, M. J. & Johnson, K. R. Cadherin-mediated cellular signaling. Curr. Opin. Cell Biol. 15, 509-514 (2003) This review describes the major intracellular signalling pathways that involve cadherins.
6. Bazzoni, G., Dejana, E. & Lampugnani, M. G. Endothelial adhesion molecules in the development of the vascular tree: the garden of forking paths. Curr. Opin. Cell Biol. 11, 573-581 (1999).
7. Simionescu, M. in Morphogenesis of endothelium Ch. 1 (eds Risau, W. & Rubanyi, G. M.) 1-21 (Harwood Academic, Amsterdam, 2000).
8. Dejana, E., Corada, M. & Lampugnani, M. G. Endothelial cell-to-cell junctions. FASEB J. 9, 910-918 (1995).
9. Schmelz, M. & Franke, W. W. Complexus adhaerentes, a new group of desmoplakin-containing junctions in endothelial cells: the syndesmos connecting retothelial cells of lymphnodes. Eur. J. Cell Biol. 61, 274-289 (1993).
10. Chitaev, N. A. & Troyanovsky, S. M. Adhesive but not lateral E-cadherin complexes require calcium and catenins for their formation. J. Cell Biol. 142, 837-846 (1998).
11. Gumbiner, B. M. Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-404 (2000).
12. Vleminckx, K. & Kemler, R. Cadherins and tissue formation: integrating adhesion and signaling. Bioessays 21, 211-220 (1999).
13. Takeichi, M. Cadherin in cancer: implications for invasion and metastasis. Curr. Opin. Cell Biol. 5, 806-811 (1993).
14. Cereijido, M., Shoshani, L. & Contreras, R. G. Molecular physiology and pathophysiology of tight junctions. I. Biogenesis of tight junctions and epithelial polarity. Am. J. Physiol. Gastrointest. Liver Physiol. 279, G477-G482 (2000).
15. Balda, M. S. & Matter, K. Transmembrane proteins of tight junctions. Semin. Cell Dev. Biol. 11, 281-289 (2000).
16. Anderson, J. M. Molecular structure of tight junctions and their role in epithelial transport. News Physiol. Sci. 16, 126-130 (2001).
17. Tsukita, S., Furuse, M. & Itoh, M. Multifunctional strands in tight junctions. Nature Rev. Mol. Cell Biol. 2, 286-293 (2001).
18. Dejana, E., Bazzoni, G. & Lampugnani, M. G. Vascular endothelial (VE)-cadherin: only an intercellular glue? Exp. Cell Res. 252, 13-19 (1999).
19. Nitta, T. et al. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161, 653-660 (2003). The first direct evidence of the importance of claudin-5 in the control of endothelial permeability in the brain.
20. Dudek, S. M. & Garcia, J. G. Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91, 1487-1500 (2001).
21. Sheldon, R., Moy, A., Lindsley, K. & Shasby, S. Role of myosin light-chain phosphorylation in endothelial cell retraction. Am. J. Physiol. 265, L606-612 (1993).
22. Lampugnani, M. G. et al. VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol. Biol. Cell 13, 1175-1189 (2002).
23. Ben-Ze'ev, A. & Geiger, B. Differential molecular interactions of β-catenin and plakoglobin in adhesion, signaling and cancer. Curr. Opin. Cell Biol. 10, 629-639 (1998).
24. Bienz, M. & Clevers, H. Linking colorectal cancer to Wnt signaling. Cell 103, 311-320 (2000).
25. Stevenson, B. R., Siciliano, 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, 755-766 (1986).
26. Fanning, A. S. & Anderson, J. M. Protein modules as organizers of membrane structure. Curr. Opin. Cell Biol. 11, 432-439 (1999).
27. Itoh, M. et al. The 220-kD protein co-localizing 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, 491-502 (1993).
28. Ohsugi, M., Larue, L., Schwarz, H. & Kemler, R. Cell-junctional and cytoskeletal organization in mouse blastocysts lacking E-cadherin. Dev. Biol. 185, 261-271 (1997).
29. Behrens, J., Birchmeier, W., Goodman, S. L. & Imhof, B. A. Dissociation of Madin-Darby canine kidney epithelial cells by the monoclonal antibody anti-arc-1: mechanistic aspects and identification of the antigen as a component related to uvomorulin. J. Cell Biol. 101, 1307-1315 (1985).
30. Wolburg, H. & Lippoldt, A. Tight junctions of the blood-brain barrier: development, composition and regulation. Vascul. Pharmacol. 38, 323-337 (2002). A comprehensive review on the organization and functional role of tight junctions in the brain microvasculature.
31. Takahashi, K. et al. Nectin/PRR: an immunoglobulin-like cell adhesion molecule recruited to cadherin-based adherens junctions through interaction with afadin, a PDZ domain-containing protein. J. Cell Biol. 145, 539-549 (1999). A description of the nectin-afadin complex and its role in the assembly of adherens junctions.
32. Fukuhara, A. et al. Involvement of nectin in the localization of junctional adhesion molecule at tight junctions. Oncogene 21, 7642-7655 (2002).
33. Ilan, N. & Madri, J. A. PECAM: old friend, new partners. Curr. Opin. Cell Biol. 15, 515-524 (2003). A review on PECAM and its signalling properties.
34. Newman, P. J. The biology of PECAM-1. J. Clin. Invest. 99, 3-8 (1997).
35. Bardin, N. et al. Identification of CD146 as a component of the endothelial junction involved in the control of cell-cell cohesion. Blood 98, 3677-3684 (2001).
36. Fagotto, F. & Gumbiner, B. M. Cell contact-dependent signaling. Dev. Biol. 180, 445-454 (1996).
37. Vinals, F. & Pouyssegur, J. Confluence of vascular endothelial cells induces cell cycle exit by inhibiting p42/p44 mitogen-activated protein kinase activity. Mol. Cell Biol. 19, 2763-2772 (1999).
38. Pece, S. & Gutkind, J. S. Signaling from E-cadherins to the MAPK pathway by the recruitment and activation of epidermal growth factor receptors upon cell-cell contact formation. J. Biol. Chem. 275, 41227-41233 (2000).
39. Pece, S., Chiariello, M., Murga, C. & Gutkind, J. S. Activation of the protein kinase Akt/PKB by the formation of E-cadherin-mediated cell-cell junctions. Evidence for the association of phosphatidylinositol 3-kinase with the E-cadherin adhesion complex. J. Biol. Chem. 274, 19347-19351 (1999).
40. Lampugnani, M. G. et al. Contact inhibition of VEGF-induced proliferation requires VE-cadherin, β-catenin and the phosphatase DEP-1/CD148. J. Cell Biol. 161, 79,3-804 (2003). References 40-43 describe the role of E-cadherin in mediating contact-induced inhibition of cell growth.
41. St Croix, B. et al. E-Cadherin-dependent growth suppression is mediated by the cyclin-dependent kinase inhibitor p27 (KIP1). J. Cell Biol. 142, 557-571 (1998).
42. Mueller, S., Cadenas, E. & Schönthal, A. H. p21WAF1 regulates anchorage-independent growth of HCT116 colon carcinoma cells via E-cadherin expression. Cancer Res. 60, 156-163 (2000).
43. Gottardi, C. J., Wong, E. & Gumbiner, B. M. E-cadherin suppresses cellular transformation by inhibiting β-catenin signaling in an adhesion-independent manner. J. Cell Biol. 153, 1049-1060 (2001).
44. Venkiteswaran, K. et al. Regulation of endothelial barrier function and growth by VE-cadherin, plakoglobin, and β-catenin. Am. J. Physiol. Cell Physiol. 283, C811-C821 (2002).
45. Gottardi, C. J. & Gumbiner, B. M. Adhesion signaling: how β-catenin interacts with its partners. Curr. Biol. 11, R792-R794 (2001).
46. Polakis, P. Wnt signaling and cancer. Genes Dev. 14, 1837-1851 (2000).
47. Van de Wetering, M., de Lau, W. & Clevers, H. WNT signaling and lymphocyte development. Cell 109 (Suppl.), S13-S19 (2002).
48. Suyama, K., Shapiro, I., Guttman, M. & Hazan, R. B. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2, 301-314 (2002).
49. Hoschuetzky, H., Aberle, H. & Kemler, R. β-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127, 1375-1380 (1994).
50. Schwartz, M. A. & Baron, V. Interactions between mitogenic stimuli, or, a thousand and one connections. Curr. Opin. Cell Biol. 11, 197-202 (1999).
51. Kim, J. B. et al. N-cadherin extracellular repeat 4 mediates epithelial to mesenchymal transition and increased mobility. J. Cell Biol. 151, 1193-1205 (2000).
52. Navarro, P., Ruco, L. & Dejana, E. 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 (1998).
53. Balsamo, J. et al. Regulated binding of PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of β-catenin. J. Cell Biol. 134, 801-813 (1996).
54. Brady-Kalnay, S. M., Rimm, D. L. & Tonks, N. K. Receptor protein tyrosine phosphatase PTPμ associates with cadherins and catenins in vivo. J. Cell Biol. 130, 977-986 (1995).
55. Kypta, R. M., Su, H. & Reichardt, L. F. Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex. J. Cell Biol. 134, 1519-1529 (1996).
56. Ukropec, J. A., Hollinger, M. K., Salva, S. M. & Woolkalis, M. J. SHP2 association with VE-cadherin complexesin human endothelial cells is regulated by thrombin. J. Biol. Chem. 275, 5983-5986 (2000).
57. Zanetti, A. et al. Vascular endothelial growth factor induces Shc association with vascular endothelial cadherin: a potential feedback mechanism to control vascular endothelial growth factor receptor-2 signaling. Arterioscler. Thromb. Vasc. Biol. 22, 617-622 (2002).
58. Balda, M. S., Garrett, M. D. & Matter, K. The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J. Cell Biol. 160, 423-432 (2003).
59. Rajasekaran, A. K., Hojo, M., Huima, T. & Rodriguez Boulan, E. Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol. 132, 451-463 (1996).
60. Reichert, M., Muller, T. & Hunziker, W. The PDZ domains of zonula occludens-1 induce an epithelial to mesenchymal transition of Madin-Darby canine kidney I cells. Evidence for a role of β-catenin/Tcf/Lef signaling. J. Biol. Chem. 275, 9492-9500 (2000).
61. Carmeliet, P. et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98, 147-157 (1999).
62. Gerber, H. et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 273, 30336-30343 (1998). A description of the key role of the P13K/AKT pathway in VEGFR2-mediated inhibition of endothelial apoptosis.
63. Takahashi, T., Yamaguchi, S., Chida, K. & Shibuya, M. A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLCγ and DNA synthesis in vascular endothelial cells. EMBO J. 20, 2768-2778 (2001). Analysis of the auto-phosphorylation sites that are responsible for the activation of PLCγ and the induction of endothelial cell proliferation by VEGFR2.
64. Gao, C. et al. PECAM-1 functions as a specific and potent inhibitor of mitochondrial-dependent apoptosis. Blood 102, 169-179(2003).
65. Zondag, G. et al. Oncogenic Ras downregulates Rac activity, which leads to increased Rho activity and epithelial-mesenchymal transition. J. Cell Biol. 149, 775-782 (2000).
66. Noren, N. K., Liu, B. P., Burridge, K. & Kreft, B. p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-580 (2000).
67. Michels, F., Habets, G. G. M., Stam, J. C., Van der Kammen, R. A. & Collard, J. G. A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature 375, 338-340 (1995).
68. Noren, N. K., Arthur, W. T. & Burridge, K. Cadherin engagement inhibits RhoA via p190RhoGAP. J. Biol. Chem. 278, 13615-13618 (2003).
69. Shay-Salit, A. et al. VEGF receptor 2 and the adherens junction as a mechanical transducer in vascular endothelial cells. Proc. Natl Acad. Sci. USA 99, 9462-9467 (2002).
70. Osawa, M., Masuda, M., Kusano, K. & Fujiwara, K. Evidence for a role of platelet endothelial cell adhesion molecule-1 in endothelial cell mechanosignal transduction: is it a mechanoresponsive molecule? J. Cell Biol. 158, 773-785 (2002).
71. Corada, M. et al. A monoclonal antibody to vascular endothelial-cadherin inhibits tumor angiogenesis without side effects on endothelial permeability. Blood 100, 905-911 (2002).
72. Carmeliet, P. & Jain, R. K. Angiogenesis in cancer and other diseases. Nature 407, 249-257 (2000).
73. Dvorak, H. F., Nagy, J. A., Feng, D., Brown, L. F. & Dvorak, A. M. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr. Top. Microbiol. Immunol. 237, 97-132 (1999).
74. Esser, S., Lampugnani, M. G., Corada, M., Dejana, E. & Risau, W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111, 1853-1865 (1998).
75. Paul, R. et al. Src deficiency or blockade of Src activity in mice provides cerebral protection following stroke. Nature Med. 7, 222-227 (2001)
76. Cattelino, A. et al. The conditional inactivation of β-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J. Cell Biol. 162, 1111-1122 (2003).
77. Takahashi, T. et al. A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development. Mol. Cell Biol. 23, 1817-1831 (2003).
78. Saitou, M. et al. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol. Biol. Cell 11, 4131-4142 (2000).
79. Connolly, J. O., Simpson, N., Hewlett, L. & Hall, A. Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 13, 2474-2485 (2002)
80. Ebnet, K. et al. The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J. 20, 3738-3748 (2001).
81. Itoh, M. et al. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J. Cell Biol. 154, 491-497 (2001).
82. Lubarsky, B. & Krasnow, M. A. Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28 (2003).
83. Hogan, B. L. & Kolodziej, P. A. Organogenesis: molecular mechanisms of tubulogenesis. Nature Rev. Genet. 3, 513-523 (2002).
84. + ATPase is required for septate junction function and epithelial tube-size control in the Drosophila tracheal system. Development 130, 4963-4974 (2003).
85. Feng, D., Nagy, J. I., Pyne, K., Dvorak, H. F. & Dvorak, A. M. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med. 187, 903-915 (1998).
86. Muller, W. A. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24, 326-333 (2003).
87. Huang, A. J. et al. Endothelial cell cytosolic free calcium regulates neutrophil migration across monolayers of endothelial cells. J. Cell Biol. 120, 1371-1380 (1993).
88. Van Wetering, S. et al. VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leukocyte transmigration. Am. J. Physiol. Cell Physiol. 285, C343-C352 (2003).
89. 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, 150-165 (1998).
90. Vouret-Craviari, V., Boquet, P., Pouyssegur, J. & Van Obberghen-Schilling, E. Regulation of the actin cytoskeleton by thrombin in human endothelial cells: role of Rho proteins in endothelial barrier function. Mol. Biol. Cell 9, 2639-2653 (1998).
91. Essler, M. et al. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J. Biol. Chem. 273, 21867-21874 (1998).
92. 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, 2964-2973 (1999). One of the first reports of leukocyte signalling through an endothelial cell adhesion molecule.
93. Greenwood, J. et al. Intracellular domain of brain endothelial intercellular adhesion molecule-1 is essential for T lymphocyte-mediated signaling and migration. J. Immunol. 171, 2099-2108 (2003).
94. Allport, J. R., Ding, H., Collins, T., Gerritsen, M. E. & Luscinskas, F. W. Endothelial-dependent mechanisms regulate leukocyte transmigration: a process involving the proteasome and disruption of the vascular endothelial-cadherin complex at endothelial cell-to-cell junctions. J. Exp. Med. 186, 517-527 (1997).
95. Mamdouh, Z., Chen, X., Pierini, L. M., Maxfield, F. R. & Muller, W. A. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 421, 748-753 (2003).
96. Su, W., Chen, H. & Jen, C. J. Differential movements of VE-cadherin and PECAM-1 during transmigration of polymorphonuclear leukocytes through human umbilical vein endothelium. Blood 100, 3597-3603 (2002).
97. Ma, S. et al. Dynamics of junctional adhesion molecule 1 (JAM1) during leukocyte transendothelial migration under flow in vitro. FASEB J. A1189 (2003).
98. Schenkel, A. R., Mamdouh, Z., Chen, X., Liebman, R. M. & Muller, W. A. CD99 plays a major role in the migration of monocytes through endothelial junctions. Nature Immunol. 3, 143-150 (2002).
99. Johnson-Leger, C., Aurrand-Lions, M. & Imhof, B. A. The parting of the endothelium: miracle, or simply a junctional affair? J. Cell Sci. 113, 921-933 (2000).
100. Vestweber, D. Regulation of endothelial cell contacts during leukocyte extravasation. Curr. Opin. Cell Biol. 14, 587-593 (2002). A review on the mechanisms of leukocyte diapedesis.
101. Martin-Padura, I. 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, 117-127 (1998).
102. Del Maschio, A. et al. 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, 1351-1356 (1999).
103. Lechner, F. et al. Antibodies to the junctional adhesion molecule cause disruption of endothelial cells and do not prevent leukocyte influx into the meninges after viral or bacterial infection. J. Infect. Dis. 182, 978-982 (2000).
104. 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, 3699-3707 (2001).
105. Bazzoni, G. & Dejana, E. Pores in the sieve and channels in the wall: control of paracellular permeability by junctional proteins in endothelial cells. Microcirculation 8, 143-152 (2001).
106. Nawroth, R. et al. VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 21, 4885-4895 (2002).
107. Radice, G. L. et al. Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78 (1997).
108. Gallicano, G. I. & Bauer, C. Rescuing desmoplakin function in extra-embryonic ectoderm reveals the importance of this protein in embryonic heart, neuroepithelium, skin and vasculature. Development 128, 929-941 (2001).
109. Saitou, M. et al. Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J. Cell Biol. 141, 397-408 (1998).
110. Duncan, G. S. et al. 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 (1999).
111. Solowiej, A., Biswas, P., Graesser, D. & Madri, J. A. Lack of platelet endothelial cell adhesion molecule-1 attenuates foreign body inflammation because of decreased angiogenesis. Am. J. Pathol. 162, 953-962 (2003).
112. Huelsken, J. & Behrens, J. The Wnt signaling pathway. J. Cell Sci. 115, 3977-3978 (2002).
113. Daniel, J. M., Spring, C. M., Crawford, H. C., Reynolds, A. B. & Baig, A. The p120(ctn)-binding partner Kaiso is a bi-modal DNA-binding protein that recognizes both a sequence-specific consensus and methylated CpG dinucleotides. Nucleic Acid Res. 30, 2911-2919 (2002).
114. Williams, B. O., Barish, G. D., Klymkowsky, M. W. & Varmus, H. E. A comparative evaluation of β-catenin and plakoglobin signalling activity. Oncogene 19, 5720-5728 (2000).
115. Nakamura, T. et al. HuASH1 protein, a putative transcription factor encoded by a human homologue of the Drosophila ash 1 gene, localizes to both nuclei and cell-cell tight junctions. Proc. Natl Acad. Sci. USA 97, 7284-7289 (2000).