Roles of cadherins and catenins in cell-cell adhesion and epithelial cell polarity

Progress in Molecular Biology and Translational Science

Volumn 116, Issue , 2013, Pages 3-23

  Nelson, W James ^a   Dickinson, Daniel J ^a   Weis, William I ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Cadherin; Cytoskeleton; Epithelia; Polarity; Polarity complex; Vesicle trafficking

Indexed keywords

EID: 84875242939     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394311-8.00001-7     Document Type: Chapter

References (104)

1. C.M. Niessen, D. Leckband, and A.S. Yap Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation Physiol Rev 91 2011 691 731
2. A.M. Marchiando, W.V. Graham, and J.R. Turner Epithelial barriers in homeostasis and disease Annu Rev Pathol 5 2010 119 144
3. M. Cereijido, R.G. Contreras, and L. Shoshani Cell adhesion, polarity, and epithelia in the dawn of metazoans Physiol Rev 84 2004 1229 1262
4. D.M. Bryant, and K.E. Mostov From cells to organs: building polarized tissue Nat Rev Mol Cell Biol 9 2008 887 901
5. I. Mellman, and W.J. Nelson Coordinated protein sorting, targeting and distribution in polarized cells Nat Rev Mol Cell Biol 9 2008 833 845
6. B. Tanos, and E. Rodriguez-Boulan The epithelial polarity program: machineries involved and their hijacking by cancer Oncogene 27 2008 6939 6957
7. H. Folsch Regulation of membrane trafficking in polarized epithelial cells Curr Opin Cell Biol 20 2008 208 213
8. D. Gravotta, A. Deora, E. Perret, C. Oyanadel, A. Soza, and R. Schreiner AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells Proc Natl Acad Sci USA 104 2007 1564 1569
9. J.E. Casanova, P.P. Breitfeld, S.A. Ross, and K.E. Mostov Phosphorylation of the polymeric immunoglobulin receptor required for its efficient transcytosis Science 248 1990 742 745
10. K. Shin, V.C. Fogg, and B. Margolis Tight junctions and cell polarity Annu Rev Cell Dev Biol 22 2006 207 235
11. V. Bennett, and J. Healy Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin Trends Mol Med 14 2008 28 36
12. W.J. Nelson Adaptation of core mechanisms to generate cell polarity Nature 422 2003 766 774
13. L. Larue, M. Ohsugi, J. Hirchenhain, and R. Kemler E-cadherin null mutant embryos fail to form a trophectoderm epithelium Proc Natl Acad Sci USA 91 1994 8263 8267
14. F. Wang, K. Dumstrei, T. Haag, and V. Hartenstein The role of DE-cadherin during cellularization, germ layer formation and early neurogenesis in the Drosophila embryo Dev Biol 270 2004 350 363
15. C.T. Capaldo, and I.G. Macara Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells Mol Biol Cell 18 2007 189 200
16. Y. Takai, W. Ikeda, H. Ogita, and Y. Rikitake The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin Annu Rev Cell Dev Biol 24 2008 309 342
17. H. Togashi, K. Kominami, M. Waseda, H. Komura, J. Miyoshi, and M. Takeichi Nectins establish a checkerboard-like cellular pattern in the auditory epithelium Science 333 2011 1144 1147
18. L. Shapiro, and W.I. Weis Structure and biochemistry of cadherins and catenins Cold Spring Harb Perspect Biol 1 2009 a003053
19. W.I. Weis, and W.J. Nelson Re-solving the cadherin-catenin-actin conundrum J Biol Chem 281 2006 35593 35597
20. J.M. Benjamin, and W.J. Nelson Bench to bedside and back again: molecular mechanisms of alpha-catenin function and roles in tumorigenesis Semin Cancer Biol 18 2008 53 64
21. P. Niewiadomska, D. Godt, and U. Tepass DE-Cadherin is required for intercellular motility during Drosophila oogenesis J Cell Biol 144 1999 533 547
22. R. Sarpal, M. Pellikka, R.R. Patel, F.Y. Hui, D. Godt, and U. Tepass Mutational analysis supports a core role for Drosophila alpha-catenin in adherens junction function J Cell Sci 125 2012 233 245
23. S. Yonemura, Y. Wada, T. Watanabe, A. Nagafuchi, and M. Shibata Alpha-catenin as a tension transducer that induces adherens junction development Nat Cell Biol 12 2010 533 542
24. S. Yamada, and W.J. Nelson Synapses: sites of cell recognition, adhesion, and functional specification Annu Rev Biochem 76 2007 267 294
25. M. Fukata, and K. Kaibuchi Rho-family GTPases in cadherin-mediated cell-cell adhesion Nat Rev Mol Cell Biol 2 2001 887 897
26. R.M. Shaw, A.J. Fay, M.A. Puthenveedu, M. von Zastrow, Y.N. Jan, and L.Y. Jan Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions Cell 128 2007 547 560
27. L.N. Nejsum, and W.J. Nelson A molecular mechanism directly linking E-cadherin adhesion to initiation of epithelial cell surface polarity J Cell Biol 178 2007 323 335
28. L.A. Ligon, and E.L. Holzbaur Microtubules tethered at epithelial cell junctions by dynein facilitate efficient junction assembly Traffic 8 2007 808 819
29. W.H. Lien, V.I. Gelfand, and V. Vasioukhin Alpha-E-catenin binds to dynamitin and regulates dynactin-mediated intracellular traffic J Cell Biol 183 2008 989 997
30. X. Chen, S. Kojima, G.G. Borisy, and K.J. Green p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions J Cell Biol 163 2003 547 557
31. C. Yeaman, K.K. Grindstaff, and W.J. Nelson Mechanism of recruiting Sec6/8 (exocyst) complex to the apical junctional complex during polarization of epithelial cells J Cell Sci 117 2004 559 570
32. K.K. Grindstaff, C. Yeaman, N. Anandasabapathy, S.C. Hsu, E. Rodriguez-Boulan, and R.H. Scheller Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells Cell 93 1998 731 740
33. C.C. Hazelett, D. Sheff, and C. Yeaman RalA and RalB differentially regulate development of epithelial tight junctions Mol Biol Cell 22 2011 4787 4800
34. J.T. Blankenship, M.T. Fuller, and J.A. Zallen The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity J Cell Sci 120 2007 3099 3110
35. D. St Johnston, and J. Ahringer Cell polarity in eggs and epithelia: parallels and diversity Cell 141 2010 757 774
36. P. Laprise, and U. Tepass Novel insights into epithelial polarity proteins in Drosophila Trends Cell Biol 21 2011 401 408
37. G. Tanentzapf, and U. Tepass Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization Nat Cell Biol 5 2003 46 52
38. S. Fan, T.W. Hurd, C.J. Liu, S.W. Straight, T. Weimbs, and E.A. Hurd Polarity proteins control ciliogenesis via kinesin motor interactions Curr Biol 14 2004 1451 1461
39. Y. Izumi, T. Hirose, Y. Tamai, S. Hirai, Y. Nagashima, and T. Fujimoto 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
40. D. Bilder, M. Schober, and N. Perrimon Integrated activity of PDZ protein complexes regulates epithelial polarity Nat Cell Biol 5 2003 53 58
41. J. Sfakianos, A. Togawa, S. Maday, M. Hull, M. Pypaert, and L. Cantley Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells J Cell Biol 179 2007 1133 1140
42. U. Tepass, G. Tanentzapf, R. Ward, and R. Fehon Epithelial cell polarity and cell junctions in Drosophila Annu Rev Genet 35 2001 747 784
43. D. Godt, and U. Tepass Drosophila oocyte localization is mediated by differential cadherin-based adhesion Nature 395 1998 387 391
44. F. Drees, S. Pokutta, S. Yamada, W.J. Nelson, and W.I. Weis Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly Cell 123 2005 903 915
45. J.M. Benjamin, A.V. Kwiatkowski, C. Yang, F. Korobova, S. Pokutta, and T. Svitkina AlphaE-catenin regulates actin dynamics independently of cadherin-mediated cell-cell adhesion J Cell Biol 189 2010 339 352
46. A. Leibfried, R. Fricke, M.J. Morgan, S. Bogdan, and Y. Bellaiche Drosophila Cip4 and WASp define a branch of the Cdc42-Par6-aPKC pathway regulating E-cadherin endocytosis Curr Biol 18 2008 1639 1648
47. M. Georgiou, E. Marinari, J. Burden, and B. Baum Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability Curr Biol 18 2008 1631 1638
48. A. Suzuki, C. Ishiyama, K. Hashiba, M. Shimizu, K. Ebnet, and S. Ohno aPKC kinase activity is required for the asymmetric differentiation of the premature junctional complex during epithelial cell polarization J Cell Sci 115 2002 3565 3573
49. K. Ebnet, M. Aurrand-Lions, A. Kuhn, F. Kiefer, S. Butz, and K. Zander The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity J Cell Sci 116 2003 3879 3891
50. K. Takekuni, W. Ikeda, T. Fujito, K. Morimoto, M. Takeuchi, and M. Monden Direct binding of cell polarity protein PAR-3 to cell-cell adhesion molecule nectin at neuroepithelial cells of developing mouse J Biol Chem 278 2003 5497 5500
51. S.Y. Wei, L.M. Escudero, F. Yu, L.H. Chang, L.Y. Chen, and Y.H. Ho Echinoid is a component of adherens junctions that cooperates with DE-cadherin to mediate cell adhesion Dev Cell 8 2005 493 504
52. M.A. McGill, R.F. McKinley, and T.J. Harris Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions J Cell Biol 185 2009 787 796
53. M. Sebbagh, M.J. Santoni, B. Hall, J.P. Borg, and M.A. Schwartz Regulation of LKB1/STRAD localization and function by E-cadherin Curr Biol 19 2009 37 42
54. D. Cohen, P.J. Brennwald, E. Rodriguez-Boulan, and A. Musch Mammalian PAR-1 determines epithelial lumen polarity by organizing the microtubule cytoskeleton J Cell Biol 164 2004 717 727
55. D. Cohen, E. Rodriguez-Boulan, and A. Musch Par-1 promotes a hepatic mode of apical protein trafficking in MDCK cells Proc Natl Acad Sci USA 101 2004 13792 13797
56. M. Elbert, G. Rossi, and P. Brennwald The yeast par-1 homologs kin1 and kin2 show genetic and physical interactions with components of the exocytic machinery Mol Biol Cell 16 2005 532 549
57. M.H. Roh, and B. Margolis Composition and function of PDZ protein complexes during cell polarization Am J Physiol Renal Physiol 285 2003 F377 F387
58. C. Lemmers, D. Michel, L. Lane-Guermonprez, M.H. Delgrossi, E. Medina, and J.P. Arsanto CRB3 binds directly to Par6 and regulates the morphogenesis of the tight junctions in mammalian epithelial cells Mol Biol Cell 15 2004 1324 1333
59. Z. Li, L. Wang, T.S. Hays, and Y. Cai Dynein-mediated apical localization of crumbs transcripts is required for Crumbs activity in epithelial polarity J Cell Biol 180 2008 31 38
60. T.J. Harris, and M. Peifer The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila J Cell Biol 170 2005 813 823
61. S. Horne-Badovinac, and D. Bilder Dynein regulates epithelial polarity and the apical localization of stardust A mRNA PLoS Genet 4 2008 e8
62. V.C. Fogg, C.J. Liu, and B. Margolis Multiple regions of Crumbs3 are required for tight junction formation in MCF10A cells J Cell Sci 118 2005 2859 2869
63. C.D. Wells, J.P. Fawcett, A. Traweger, Y. Yamanaka, M. Goudreault, and K. Elder A Rich1/Amot complex regulates the Cdc42 GTPase and apical-polarity proteins in epithelial cells Cell 125 2006 535 548
64. H. Lu, and D. Bilder Endocytic control of epithelial polarity and proliferation in Drosophila Nat Cell Biol 7 2005 1232 1239
65. S. Audebert, C. Navarro, C. Nourry, S. Chasserot-Golaz, P. Lecine, and Y. Bellaiche Mammalian Scribble forms a tight complex with the betaPIX exchange factor Curr Biol 14 2004 987 995
66. A.G. Tian, and W.M. Deng Lgl and its phosphorylation by aPKC regulate oocyte polarity formation in Drosophila Development 135 2008 463 471
67. A. Musch, D. Cohen, C. Yeaman, W.J. Nelson, E. Rodriguez-Boulan, and P.J. Brennwald Mammalian homolog of Drosophila tumor suppressor lethal (2) giant larvae interacts with basolateral exocytic machinery in Madin-Darby canine kidney cells Mol Biol Cell 13 2002 158 168
68. O. Klezovitch, T.E. Fernandez, S.J. Tapscott, and V. Vasioukhin Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice Genes Dev 18 2004 559 571
69. J. Betschinger, F. Eisenhaber, and J.A. Knoblich Phosphorylation-induced autoinhibition regulates the cytoskeletal protein Lethal (2) giant larvae Curr Biol 15 2005 276 282
70. J. Betschinger, K. Mechtler, and J.A. Knoblich The Par complex directs asymmetric cell division by phosphorylating the cytoskeletal protein Lgl Nature 422 2003 326 330
71. J. Behrens, and W. Birchmeier Cell-cell adhesion in invasion and metastasis of carcinomas Cancer Treat Res 71 1994 251 266
72. G. Berx, K.F. Becker, H. Hofler, and F. van Roy Mutations of the human E-cadherin (CDH1) gene Hum Mutat 12 1998 226 237
73. M.R. Silvis, B.T. Kreger, W.H. Lien, O. Klezovitch, G.M. Rudakova, and F.D. Camargo Alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1 Sci Signal 4 2011 ra33
74. R. Fodde, and T. Brabletz Wnt/beta-catenin signaling in cancer stemness and malignant behavior Curr Opin Cell Biol 19 2007 150 158
75. V. Vasioukhin, C. Bauer, L. Degenstein, B. Wise, and E. Fuchs Hyperproliferation and defects in epithelial polarity upon conditional ablation of alpha-catenin in skin Cell 104 2001 605 617
76. G. Berx, and F. van Roy Involvement of members of the cadherin superfamily in cancer Cold Spring Harb Perspect Biol 1 2009 a003129
77. B.D. White, A.J. Chien, and D.W. Dawson Dysregulation of Wnt/beta-catenin signaling in gastrointestinal cancers Gastroenterology 142 2012 219 232
78. H. Eagle, E.M. Levine, and C.W. Boone Cellular growth, contact inhibition, and macromolecular synthesis Science 148 1965 665
79. F. Fagotto, and B.M. Gumbiner Cell contact-dependent signaling Dev Biol 180 1996 445 454
80. W.H. Lien, O. Klezovitch, T.E. Fernandez, J. Delrow, and V. Vasioukhin alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway Science 311 2006 1609 1612
81. W.J. Nelson, and R. Nusse Convergence of Wnt, beta-catenin, and cadherin pathways Science 303 2004 1483 1487
82. J.C. Boggiano, and R.G. Fehon Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling Dev Cell 22 2012 695 702
83. K. Schlegelmilch, M. Mohseni, O. Kirak, J. Pruszak, J.R. Rodriguez, and D. Zhou Yap1 acts downstream of alpha-catenin to control epidermal proliferation Cell 144 2011 782 795
84. M.S. Balda, and K. Matter Tight junctions and the regulation of gene expression Biochim Biophys Acta 1788 2009 761 767
85. M.S. Balda, M.D. Garrett, and K. Matter The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density J Cell Biol 160 2003 423 432
86. J. Zeitler, C.P. Hsu, H. Dionne, and D. Bilder Domains controlling cell polarity and proliferation in the Drosophila tumor suppressor Scribble J Cell Biol 167 2004 1137 1146
87. C.D. Hough, D.F. Woods, S. Park, and P.J. Bryant Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK Discs large Genes Dev 11 1997 3242 3253
88. L. Zhan, A. Rosenberg, K.C. Bergami, M. Yu, Z. Xuan, and A.B. Jaffe Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma Cell 135 2008 865 878
89. A.A. Mailleux, M. Overholtzer, and J.S. Brugge Lumen formation during mammary epithelial morphogenesis: insights from in vitro and in vivo models Cell Cycle 7 2008 57 62
90. M. Zhao, P. Szafranski, C.A. Hall, and S. Goode Basolateral junctions utilize warts signaling to control epithelial-mesenchymal transition and proliferation crucial for migration and invasion of Drosophila ovarian epithelial cells Genetics 178 2008 1947 1971
91. B.V. Reddy, and K.D. Irvine The Fat and Warts signaling pathways: new insights into their regulation, mechanism and conservation Development 135 2008 2827 2838
92. S.A. Nichols, B.W. Roberts, D.J. Richter, S.R. Fairclough, and N. King Origin of metazoan cadherin diversity and the antiquity of the classical cadherin/beta-catenin complex Proc Natl Acad Sci USA 109 2012 13046 13051
93. S.A. Nichols, W. Dirks, J.S. Pearse, and N. King Early evolution of animal cell signaling and adhesion genes Proc Natl Acad Sci USA 103 2006 12451 12456
94. B. Fahey, and B.M. Degnan Origin of animal epithelia: insights from the sponge genome Evol Dev 12 2010 601 617
95. D.J. Dickinson, W.J. Nelson, and W.I. Weis An epithelial tissue in Dictyostelium and the origin of metazoan multicellularity BioEssays 34 2012 833 840
96. B. Baum, J. Settleman, and M.P. Quinlan Transitions between epithelial and mesenchymal states in development and disease Semin Cell Dev Biol 19 2008 294 308
97. D.J. Dickinson, W.J. Nelson, and W.I. Weis A polarized epithelium organized by beta- and alpha-catenin predates cadherin and metazoan origins Science 331 2011 1336 1339
98. A.V. Kwiatkowski, S.L. Maiden, S. Pokutta, H.J. Choi, J.M. Benjamin, and A.M. Lynch In vitro and in vivo reconstitution of the cadherin-catenin-actin complex from Caenorhabditis elegans Proc Natl Acad Sci USA 107 2010 14591 14596
99. M.J. Grimson, J.C. Coates, J.P. Reynolds, M. Shipman, R.L. Blanton, and A.J. Harwood Adherens junctions and beta-catenin-mediated cell signalling in a non-metazoan organism Nature 408 2000 727 731
100. H. Urushihara Developmental biology of the social amoeba: history, current knowledge and prospects Dev Growth Differ 50 Suppl. 1 2008 S277 S281
101. K.B. Raper, and D.I. Fennell Stalk formation in Dictyostelium Bull Torrey Bot Club 19 1952 1421 1428
102. D.J. Dickinson, W.J. Nelson, and W.I. Weis α-Catenin and IQGAP regulate myosin localization to control epithelial tube morphogenesis in Dictyostelium Dev Cell 23 2012 533 546
103. J. Faix, and W. Dittrich DGAP1, a homologue of rasGTPase activating proteins that controls growth, cytokinesis, and development in Dictyostelium discoideum FEBS Lett 394 1996 251 257
104. J. Faix, M. Steinmetz, H. Boves, R.A. Kammerer, F. Lottspeich, and U. Mintert Cortexillins, major determinants of cell shape and size, are actin-bundling proteins with a parallel coiled-coil tail Cell 86 1996 631 642