Advertisement

Classical Cadherins

  • Barry M. GumbinerEmail author
Chapter

Abstract

Classical cadherins mediate a wide range of cellular functions important for morphogenesis, tissue homeostasis and physiology, and disease conditions. Their core adhesive functions, in association with the contractile actomyosin cytoskeleton allow cells to sort into domains and exert forces in order to separate from their neighbors, rearrange relative to their neighbors, or cause a change in tissue shape. The diversity of classical cadherins underlies cell recognition specificity and also provides for more specialized tissue-specific functions and signaling events. Cadherin-mediated adhesion is regulated in a variety of ways to allow them to perform this diversity of physiological and developmental functions in different tissues. Regulatory mechanisms include control of cadherin gene expression and cadherin switching, cadherin membrane trafficking, cytoskeletal remodeling, and the control of the state of the adhesive bond itself. Signaling mechanisms are essential to classical cadherin functions, contributing to both their intrinsic adhesive and force generating functions as well as communicating the state of the tissue to mediate changes in growth and differentiation.

Keywords

Cell adhesion Catenins Morphogenesis Actomyosin Cell sorting Signal transduction Barrier function Regulation Selectivity Structure 

References

  1. Abe K, Takeichi M (2008) EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt. Proc Natl Acad Sci U S A 105(1):13–19PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akhmanova A, Stehbens SJ, Yap AS (2009) Touch, grasp, deliver and control: functional cross-talk between microtubules and cell adhesions. Traffic 10(3):268–274PubMedCrossRefGoogle Scholar
  3. Alanne MH, Pummi K, Heape AM, Grenman R, Peltonen J, Peltonen S (2009) Tight junction proteins in human Schwann cell autotypic junctions. J Histochem Cytochem 57(6):523–529PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alberts B, Johnson A, Lewis J, et al (2002) Molecular biology of the cell (4th edn). New York: Garland ScienceGoogle Scholar
  5. Anastasiadis PZ, Reynolds AB (2001) Regulation of Rho GTPases by p120-catenin. Curr Opin Cell Biol 13(5):604–610PubMedCrossRefGoogle Scholar
  6. Anderson JM, Van Itallie CM (2009) Physiology and function of the tight junction. Cold Spring Harbor Perspect Biol 1(2):a002584CrossRefGoogle Scholar
  7. Aono S, Nakagawa S, Reynolds AB, Takeichi M (1999) p120(ctn) acts as an inhibitory regulator of cadherin function in colon carcinoma cells. J Cell Biol 145(3):551–562PubMedPubMedCentralCrossRefGoogle Scholar
  8. Astick M, Tubby K, Mubarak WM, Guthrie S, Price SR (2014) Central topography of cranial motor nuclei controlled by differential cadherin expression. Curr Biol 24(21):2541–2547PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bauer R, Weimbs A, Lechner H, Hoch M (2006) DE-cadherin, a core component of the adherens junction complex modifies subcellular localization of the Drosophila gap junction protein innexin2. Cell Commun Adhes 13(1–2):103–114PubMedCrossRefGoogle Scholar
  10. Baum B, Georgiou M (2011) Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192(6):907–917PubMedPubMedCentralCrossRefGoogle Scholar
  11. Boggon TJ, Murray J, Chappuis-Flament S, Wong E, Gumbiner BM, Shapiro L (2002) C-cadherin ectodomain structure and implications for cell adhesion mechanisms. Science 296(5571):1308–1313PubMedCrossRefGoogle Scholar
  12. Borrmann CM, Grund C, Kuhn C, Hofmann I, Pieperhoff S, Franke WW (2006) The area composita of adhering junctions connecting heart muscle cells of vertebrates. II. Colocalizations of desmosomal and fascia adhaerens molecules in the intercalated disk. Eur J Cell Biol 85(6):469–485PubMedCrossRefGoogle Scholar
  13. Brasch J, Harrison OJ, Ahlsen G, Carnally SM, Henderson RM, Honig B, Shapiro L (2011) Structure and binding mechanism of vascular endothelial cadherin: a divergent classical cadherin. J Mol Biol 408(1):57–73PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brasch J, Harrison OJ, Honig B, Shapiro L (2012) Thinking outside the cell: how cadherins drive adhesion. Trends Cell Biol 22(6):299–310PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brieher WM, Gumbiner BM (1994) Regulation of C-cadherin function during activin induced morphogenesis of Xenopus animal caps. J Cell Biol 126(2):519–527PubMedCrossRefGoogle Scholar
  16. Bulgakova NA, Klapholz B, Brown NH (2012) Cell adhesion in Drosophila: versatility of cadherin and integrin complexes during development. Curr Opin Cell Biol 24(5):702–712PubMedCrossRefGoogle Scholar
  17. Cai D, Chen SC, Prasad M, He L, Wang X, Choesmel-Cadamuro V, Sawyer JK, Danuser G, Montell DJ (2014) Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 157(5):1146–1159PubMedPubMedCentralCrossRefGoogle Scholar
  18. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E et al (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98(2):147–157PubMedCrossRefGoogle Scholar
  19. Cavey M, Rauzi M, Lenne PF, Lecuit T (2008) A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453(7196):751–756PubMedCrossRefGoogle Scholar
  20. Chazeau A, Garcia M, Czondor K, Perrais D, Tessier B, Giannone G, Thoumine O (2015) Mechanical coupling between transsynaptic N-cadherin adhesions and actin flow stabilizes dendritic spines. Mol Biol Cell 26(5):859–873PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chen X, Gumbiner BM (2006) Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J Cell Biol 174(2):301–313PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chen X, Koh E, Yoder M, Gumbiner BM (2009) A protocadherin-cadherin-FLRT3 complex controls cell adhesion and morphogenesis. PLoS One 4(12):e8411PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chen XL, Nam JO, Jean C, Lawson C, Walsh CT, Goka E, Lim ST, Tomar A, Tancioni I, Uryu S, Guan JL, Acevedo LM, Weis SM, Cheresh DA, Schlaepfer DD (2012) VEGF-induced vascular permeability is mediated by FAK. Dev Cell 22(1):146–157PubMedPubMedCentralCrossRefGoogle Scholar
  24. Ciatto C, Bahna F, Zampieri N, VanSteenhouse HC, Katsamba PS, Ahlsen G, Harrison OJ, Brasch J, Jin X, Posy S, Vendome J, Ranscht B, Jessell TM, Honig B, Shapiro L (2010) T-cadherin structures reveal a novel adhesive binding mechanism. Nat Struct Mol Biol 17(3):339–347PubMedPubMedCentralCrossRefGoogle Scholar
  25. Classen AK, Anderson KI, Marois E, Eaton S (2005) Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9(6):805–817PubMedCrossRefGoogle Scholar
  26. Clevers H, Nusse R (2012) Wnt/beta-catenin signaling and disease. Cell 149(6):1192–1205PubMedCrossRefGoogle Scholar
  27. Cooke JE, Moens CB (2002) Boundary formation in the hindbrain: Eph only it were simple. Trends Neurosci 25(5):260–267PubMedCrossRefGoogle Scholar
  28. Costantini F, Kopan R (2010) Patterning a complex organ: branching morphogenesis and nephron segmentation in kidney development. Dev Cell 18(5):698–712PubMedPubMedCentralCrossRefGoogle Scholar
  29. Cunningham KE, Turner JR (2012) Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann N Y Acad Sci 1258:34–42PubMedPubMedCentralCrossRefGoogle Scholar
  30. Curto M, Cole BK, Lallemand D, Liu CH, McClatchey AI (2007) Contact-dependent inhibition of EGFR signaling by Nf2/Merlin. J Cell Biol 177(5):893–903PubMedPubMedCentralCrossRefGoogle Scholar
  31. D’Souza-Schorey C (2005) Disassembling adherens junctions: breaking up is hard to do. Trends Cell Biol 15(1):19–26PubMedCrossRefGoogle Scholar
  32. Daugherty RL, Gottard CJ (2007) Phospho-regulation of Beta-catenin adhesion and signaling functions. Physiology (Bethesda) 22:303–309CrossRefGoogle Scholar
  33. Davies JA (1996) Mesenchyme to epithelium transition during development of the mammalian kidney tubule. Acta Anat 156(3):187–201PubMedCrossRefGoogle Scholar
  34. Davis MA, Ireton RC, Reynolds AB (2003) A core function for p120-catenin in cadherin turnover. J Cell Biol 163(3):525–534PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dejana E, Vestweber D (2013) The role of VE-cadherin in vascular morphogenesis and permeability control. Prog Mol Biol Transl Sci 116:119–144PubMedCrossRefGoogle Scholar
  36. Dejana E, Orsenigo F, Lampugnani MG (2008) The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 121(Pt 13):2115–2122PubMedCrossRefGoogle Scholar
  37. Dejana E, Tournier-Lasserve E, Weinstein BM (2009) The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell 16(2):209–221PubMedCrossRefGoogle Scholar
  38. Dor Y, Djonov V, Keshet E (2003) Making vascular networks in the adult: branching morphogenesis without a roadmap. Trends Cell Biol 13(3):131–136PubMedCrossRefGoogle Scholar
  39. Fagotto F, Gumbiner BM (1994) Beta-catenin localization during Xenopus embryogenesis: accumulation at tissue and somite boundaries. Development 120(12):3667–3679PubMedGoogle Scholar
  40. Fagotto F, Gumbiner BM (1996) Cell contact-dependent signaling. Dev Biol 180(2):445–454PubMedCrossRefGoogle Scholar
  41. Fagotto F, Funayama N, Gluck U, Gumbiner BM (1996) Binding to cadherins antagonizes the signaling activity of beta-catenin during axis formation in Xenopus. J Cell Biol 132(6):1105–1114PubMedCrossRefGoogle Scholar
  42. Fan R, Kim NG, Gumbiner BM (2013) Regulation of Hippo pathway by mitogenic growth factors via phosphoinositide 3-kinase and phosphoinositide-dependent kinase-1. Proc Natl Acad Sci U S A 110(7):2569–2574PubMedPubMedCentralCrossRefGoogle Scholar
  43. Fannon AM, Sherman DL, Ilyina-Gragerova G, Brophy PJ, Friedrich VL Jr, Colman DR (1995) Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions. J Cell Biol 129(1):189–202PubMedCrossRefGoogle Scholar
  44. Fleming TP, Johnson MH (1988) From egg to epithelium. Ann Rev Cell Biol 4:459–485PubMedCrossRefGoogle Scholar
  45. Franke JD, Montague RA, Kiehart DP (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15(24):2208–2221PubMedCrossRefGoogle Scholar
  46. Frenzel EM, Johnson RG (1996) Gap junction formation between cultured embryonic lens cells is inhibited by antibody to N-cadherin. Dev Biol 179(1):1–16PubMedCrossRefGoogle Scholar
  47. Gavard J, Gutkind JS (2006) VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8(11):1223–1234PubMedCrossRefGoogle Scholar
  48. Geisbrecht ER, Montell DJ (2002) Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol 4(8):616–620PubMedGoogle Scholar
  49. Giancotti FG (2003) A structural view of integrin activation and signaling. Dev Cell 4(2):149–151PubMedCrossRefGoogle Scholar
  50. Gottardi CJ, Gumbiner BM (2004) Distinct molecular forms of beta-catenin are targeted to adhesive or transcriptional complexes. J Cell Biol 167(2):339–349PubMedPubMedCentralCrossRefGoogle Scholar
  51. Gottardi CJ, Wong E, Gumbiner BM (2001) E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol 153(5):1049–1060PubMedPubMedCentralCrossRefGoogle Scholar
  52. Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, Taite H, Scoular R, Miller A, Reeve AE (1998) E-cadherin germline mutations in familial gastric cancer. Nature 392(6674):402–405PubMedCrossRefGoogle Scholar
  53. Gumbiner BM (2005) Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6(8):622–634PubMedCrossRefGoogle Scholar
  54. Gumbiner BM, Kim NG (2014) The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 127(Pt 4):709–717PubMedPubMedCentralCrossRefGoogle Scholar
  55. Haas AR, Tuan RS (1999) Chondrogenic differentiation of murine C3H10T1/2 multipotential mesenchymal cells: II. Stimulation by bone morphogenetic protein-2 requires modulation of N-cadherin expression and function. Differentiation 64(2):77–89PubMedCrossRefGoogle Scholar
  56. Hardin J, Lynch A, Loveless T, Pettitt J (2013) Cadherins and their partners in the nematode worm Caenorhabditis elegans. Prog Mol Biol Transl Sci 116:239–262PubMedCrossRefGoogle Scholar
  57. Harrison OJ, Bahna F, Katsamba PS, Jin X, Brasch J, Vendome J, Ahlsen G, Carroll KJ, Price SR, Honig B, Shapiro L (2010) Two-step adhesive binding by classical cadherins. Nat Struct Mol Biol 17(3):348–357PubMedPubMedCentralCrossRefGoogle Scholar
  58. Hazan RB, Qiao R, Keren R, Badano I, Suyama K (2004) Cadherin switch in tumor progression. Ann N Y Acad Sci 1014:155–163PubMedCrossRefGoogle Scholar
  59. Heasman J, Crawford A, Goldstone K, Garner-Hamrick P, Gumbiner B, McCrea P, Kintner C, Noro CY, Wylie C (1994) Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 79(5):791–803PubMedCrossRefGoogle Scholar
  60. Hewat EA, Durmort C, Jacquamet L, Concord E, Gulino-Debrac D (2007) Architecture of the VE-cadherin hexamer. J Mol Biol 365(3):744–751PubMedCrossRefGoogle Scholar
  61. Hirate Y, Hirahara S, Inoue K, Suzuki A, Alarcon VB, Akimoto K, Hirai T, Hara T, Adachi M, Chida K, Ohno S, Marikawa Y, Nakao K, Shimono A, Sasaki H (2013) Polarity-dependent distribution of angiomotin localizes hippo signaling in preimplantation embryos. Curr Biol 23(13):1181–1194PubMedPubMedCentralCrossRefGoogle Scholar
  62. Holgate ST (2010) Has the time come to rethink the pathogenesis of asthma? Curr Opin Allergy Clin Immunol 10(1):48–53PubMedCrossRefGoogle Scholar
  63. Hulpiau P, van Roy F (2009) Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41(2):349–369PubMedCrossRefGoogle Scholar
  64. Huveneers S, Oldenburg J, Spanjaard E, van der Krogt G, Grigoriev I, Akhmanova A, Rehmann H, de Rooij J (2012) Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 196(5):641–652PubMedPubMedCentralCrossRefGoogle Scholar
  65. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687PubMedCrossRefGoogle Scholar
  66. Hynes RO (2003) Structural biology. Changing Partners Sci 300(5620):755–756Google Scholar
  67. Ichii T, Takeichi M (2007) p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells 12(7):827–839PubMedCrossRefGoogle Scholar
  68. Ishiyama N, Lee SH, Liu S, Li GY, Smith MJ, Reichardt LF, Ikura M (2010) Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell-cell adhesion. Cell 141(1):117–128PubMedCrossRefGoogle Scholar
  69. Ivanov AI, Nusrat A, Parkos CA (2004) The epithelium in inflammatory bowel disease: potential role of endocytosis of junctional proteins in barrier disruption. Novartis Found Symp 263:115–124; discussion 124–32, 211–8PubMedCrossRefGoogle Scholar
  70. Ivanov AI, Bachar M, Babbin BA, Adelstein RS, Nusrat A, Parkos CA (2007) A unique role for nonmuscle myosin heavy chain IIA in regulation of epithelial apical junctions. PLoS One 2(7):e658PubMedPubMedCentralCrossRefGoogle Scholar
  71. Ivanov AI, Parkos CA, Nusrat A (2010) Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol 177(2):512–524PubMedPubMedCentralCrossRefGoogle Scholar
  72. Jin X, Walker MA, Felsovalyi K, Vendome J, Bahna F, Mannepalli S, Cosmanescu F, Ahlsen G, Honig B, Shapiro L (2012) Crystal structures of Drosophila N-cadherin ectodomain regions reveal a widely used class of Ca(2)+-free interdomain linkers. Proc Natl Acad Sci U S A 109(3):E127–E134PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kane DA, McFarland KN, Warga RM (2005) Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 132(5):1105–1116PubMedCrossRefGoogle Scholar
  74. Katsamba P, Carroll K, Ahlsen G, Bahna F, Vendome J, Posy S, Rajebhosale M, Price S, Jessell TM, Ben-Shaul A, Shapiro L, Honig BH (2009) Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc Natl Acad Sci U S A 106(28):11594–11599PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kaurah P, MacMillan A, Boyd N, Senz J, De Luca A, Chun N, Suriano G, Zaor S, Van Manen L, Gilpin C, Nikkel S, Connolly-Wilson M, Weissman S, Rubinstein WS, Sebold C et al (2007) Founder and recurrent CDH1 mutations in families with hereditary diffuse gastric cancer. JAMA 297(21):2360–2372PubMedCrossRefGoogle Scholar
  76. Kazmierczak P, Sakaguchi H, Tokita J, Wilson-Kubalek EM, Milligan RA, Muller U, Kachar B (2007) Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449(7158):87–91PubMedCrossRefGoogle Scholar
  77. Keller R (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298(5600):1950–1954PubMedCrossRefGoogle Scholar
  78. Keller R (2006) Mechanisms of elongation in embryogenesis. Development 133(12):2291–2302PubMedCrossRefGoogle Scholar
  79. Keller R, Davidson L, Edlund A, Elul T, Ezin M, Shook D, Skoglund P (2000) Mechanisms of convergence and extension by cell intercalation. Philos Trans R Soc Lond Ser B Biol Sci 355(1399):897–922CrossRefGoogle Scholar
  80. Kemp HA, Cooke JE, Moens CB (2009) EphA4 and EfnB2a maintain rhombomere coherence by independently regulating intercalation of progenitor cells in the zebrafish neural keel. Dev Biol 327(2):313–326PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kim JH, Kushiro K, Graham NA, Asthagiri AR (2009) Tunable interplay between epidermal growth factor and cell-cell contact governs the spatial dynamics of epithelial growth. Proc Natl Acad Sci U S A 106(27):11149–11153PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kim NG, Koh E, Chen X, Gumbiner BM (2011) E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci U S A 108(29):11930–11935PubMedPubMedCentralCrossRefGoogle Scholar
  83. Lampugnani MG, Zanetti A, Breviario F, Balconi G, Orsenigo F, Corada M, Spagnuolo R, Betson M, Braga V, Dejana E (2002) VE-cadherin regulates endothelial actin activating Rac and increasing membrane association of Tiam. Mol Biol Cell 13(4):1175–1189PubMedPubMedCentralCrossRefGoogle Scholar
  84. Levayer R, Pelissier-Monier A, Lecuit T (2011) Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat Cell Biol 13(5):529–540PubMedCrossRefGoogle Scholar
  85. Li J, Radice GL (2010) A new perspective on intercalated disc organization: implications for heart disease. Dermatol Res Pract 2010:207835PubMedPubMedCentralGoogle Scholar
  86. Lilien J, Balsamo J (2005) The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin. Curr Opin Cell Biol 17(5):459–465PubMedCrossRefGoogle Scholar
  87. Lu Z, Ghosh S, Wang Z, Hunter T (2003) Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion. Cancer Cell 4(6):499–515PubMedCrossRefGoogle Scholar
  88. Maddugoda MP, Crampton MS, Shewan AM, Yap AS (2007) Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell cell contacts in mammalian epithelial cells. J Cell Biol 178(3):529–540PubMedPubMedCentralCrossRefGoogle Scholar
  89. Maher MT, Flozak AS, Stocker AM, Chenn A, Gottardi CJ (2009) Activity of the beta-catenin phosphodestruction complex at cell-cell contacts is enhanced by cadherin-based adhesion. J Cell Biol 186(2):219–228PubMedPubMedCentralCrossRefGoogle Scholar
  90. Maitre JL, Heisenberg CP (2013) Three functions of cadherins in cell adhesion. Curr Biol 23(14):R626–R633PubMedPubMedCentralCrossRefGoogle Scholar
  91. Maitre JL, Berthoumieux H, Krens SF, Salbreux G, Julicher F, Paluch E, Heisenberg CP (2012) Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338(6104):253–256PubMedCrossRefGoogle Scholar
  92. McClatchey AI, Yap AS (2012) Contact inhibition (of proliferation) redux. Curr Opin Cell Biol 24(5):685–694PubMedCrossRefGoogle Scholar
  93. McCrea PD, Turck CW, Gumbiner B (1991) A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin. Science 254(5036):1359–1361PubMedCrossRefGoogle Scholar
  94. McCrea PD, Maher MT, Gottardi CJ (2015) Nuclear signaling from cadherin adhesion complexes. Curr Top Dev Biol 112:129–196PubMedPubMedCentralCrossRefGoogle Scholar
  95. McLachlan RW, Yap AS (2007) Not so simple: the complexity of phosphotyrosine signaling at cadherin adhesive contacts. J Mol Med 85(6):545–554PubMedCrossRefGoogle Scholar
  96. Meng W, Mushika Y, Ichii T, Takeichi M (2008) Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135(5):948–959PubMedCrossRefGoogle Scholar
  97. Nelson WJ, Nusse R (2004) Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303(5663):1483–1487PubMedPubMedCentralCrossRefGoogle Scholar
  98. Niessen CM, Gumbiner BM (2002) Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J Cell Biol 156(2):389–399PubMedPubMedCentralCrossRefGoogle Scholar
  99. Nishimura T, Takeichi M (2009) Remodeling of the adherens junctions during morphogenesis. Curr Top Dev Biol 89:33–54PubMedCrossRefGoogle Scholar
  100. Nose A, Nagafuchi A, Takeichi M (1988) Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993–1001PubMedCrossRefGoogle Scholar
  101. Nottebaum AF, Cagna G, Winderlich M, Gamp AC, Linnepe R, Polaschegg C, Filippova K, Lyck R, Engelhardt B, Kamenyeva O, Bixel MG, Butz S, Vestweber D (2008) VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J Exp Med 205(12):2929–2945PubMedPubMedCentralCrossRefGoogle Scholar
  102. Nusrat A, Parkos CA, Liang TW, Carnes DK, Madara JL (1997) Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology 113(5):1489–1500PubMedCrossRefGoogle Scholar
  103. Oda H, Takeichi M (2011) Evolution: structural and functional diversity of cadherin at the adherens junction. J Cell Biol 193(7):1137–1146PubMedPubMedCentralCrossRefGoogle Scholar
  104. Oda H, Tsukita S, Takeichi M (1998) Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation. Dev Biol 203(2):435–450PubMedCrossRefGoogle Scholar
  105. Ogata S, Morokuma J, Hayata T, Kolle G, Niehrs C, Ueno N, Cho KW (2007) TGF-beta signaling-mediated morphogenesis: modulation of cell adhesion via cadherin endocytosis. Genes Dev 21(14):1817–1831PubMedPubMedCentralCrossRefGoogle Scholar
  106. Park KS, Gumbiner BM (2010) Cadherin 6B induces BMP signaling and de-epithelialization during the epithelial mesenchymal transition of the neural crest. Development 137(16):2691–2701PubMedPubMedCentralCrossRefGoogle Scholar
  107. Parkos CA (1997) Molecular events in neutrophil transepithelial migration. BioEssays 19(10):865–873Google Scholar
  108. Patel SD, Ciatto C, Chen CP, Bahna F, Rajebhosale M, Arkus N, Schieren I, Jessell TM, Honig B, Price SR, Shapiro L (2006) Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124(6):1255–1268PubMedCrossRefGoogle Scholar
  109. Peglion F, Llense F, Etienne-Manneville S (2014) Adherens junction treadmilling during collective migration. Nat Cell Biol 16(7):639–651PubMedCrossRefGoogle Scholar
  110. Peifer M, McCrea PD, Green KJ, Wieschaus E, Gumbiner BM (1992) The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J Cell Biol 118(3):681–691PubMedCrossRefGoogle Scholar
  111. Perrais M, Chen X, Perez-Moreno M, Gumbiner BM (2007) E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell 18(6):2013–2025PubMedPubMedCentralCrossRefGoogle Scholar
  112. Petrova YI, Spano MM, Gumbiner BM (2012) Conformational epitopes at cadherin calcium-binding sites and p120-catenin phosphorylation regulate cell adhesion. Mol Biol Cell 23(11):2092–2108PubMedPubMedCentralCrossRefGoogle Scholar
  113. Pettitt J, Cox EA, Broadbent ID, Flett A, Hardin J (2003) The Caenorhabditis elegans p120 catenin homologue, JAC-1, modulates cadherin-catenin function during epidermal morphogenesis. J Cell Biol 162(1):15–22PubMedPubMedCentralCrossRefGoogle Scholar
  114. Pharoah PD, Guilford P, Caldas C (2001) Incidence of gastric cancer and breast cancer in CDH1 (E-cadherin) mutation carriers from hereditary diffuse gastric cancer families. Gastroenterology 121(6):1348–1353PubMedCrossRefGoogle Scholar
  115. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M (2003) p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha-catenin Interaction. Mol Cell Biol 23(7):2287–2297PubMedPubMedCentralCrossRefGoogle Scholar
  116. Prowse DM, Cadwallader GP, Pitts JD (1997) E-cadherin expression can alter the specificity of gap junction formation. Cell Biol Int 21(12):833–843PubMedCrossRefGoogle Scholar
  117. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR (2004) E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J 23(8):1739–1748PubMedPubMedCentralCrossRefGoogle Scholar
  118. Radice GL (2013) N-cadherin-mediated adhesion and signaling from development to disease: lessons from mice. Prog Mol Biol Transl Sci 116:263–289PubMedCrossRefGoogle Scholar
  119. Ratheesh A, Gomez GA, Priya R, Verma S, Kovacs EM, Jiang K, Brown NH, Akhmanova A, Stehbens SJ, Yap AS (2012) Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 14(8):818–828PubMedPubMedCentralCrossRefGoogle Scholar
  120. Reddy BV, Irvine KD (2013) Regulation of Hippo signaling by EGFR-MAPK signaling through Ajuba family proteins. Dev Cell 24(5):459–471PubMedPubMedCentralCrossRefGoogle Scholar
  121. Reynolds AB (2007) p120-catenin: past and present. Biochim Biophys Acta 1773(1):2–7PubMedPubMedCentralCrossRefGoogle Scholar
  122. Reynolds AB, Daniel J, McCrea PD, Wheelock MJ, Wu J, Zhang Z (1994) Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol Cell Biol 14(12):8333–8342PubMedPubMedCentralCrossRefGoogle Scholar
  123. Rodriguez I, Basler K (1997) Control of compartmental affinity boundaries by hedgehog. Nature 389(6651):614–618PubMedCrossRefGoogle Scholar
  124. Roura S, Miravet S, Piedra J, Garcia A (1999) de Herreros, and M. Dunach. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J Biol Chem 274(51):36734–36740PubMedCrossRefGoogle Scholar
  125. Rudini N, Felici A, Giampietro C, Lampugnani M, Corada M, Swirsding K, Garre M, Liebner S, Letarte M, ten Dijke P, Dejana E (2008) VE-cadherin is a critical endothelial regulator of TGF-beta signalling. EMBO J 27(7):993–1004PubMedPubMedCentralCrossRefGoogle Scholar
  126. Samarin SN, Ivanov AI, Flatau G, Parkos CA, Nusrat A (2007) Rho/Rho-associated kinase-II signaling mediates disassembly of epithelial apical junctions. Mol Biol Cell 18(9):3429–3439PubMedPubMedCentralCrossRefGoogle Scholar
  127. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, Camargo FD (2011) Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144(5):782–795PubMedPubMedCentralCrossRefGoogle Scholar
  128. Schroeder MC, Halder G (2012) Regulation of the Hippo pathway by cell architecture and mechanical signals. Semin Cell Dev Biol 23(7):803–811PubMedCrossRefGoogle Scholar
  129. Shahbazi MN, Megias D, Epifano C, Akhmanova A, Gundersen GG, Fuchs E, Perez-Moreno M (2013) CLASP2 interacts with p120-catenin and governs microtubule dynamics at adherens junctions. J Cell Biol 203(6):1043–1061PubMedPubMedCentralCrossRefGoogle Scholar
  130. Shamir ER, Pappalardo E, Jorgens DM, Coutinho K, Tsai WT, Aziz K, Auer M, Tran PT, Bader JS, Ewald AJ (2014) Twist1-induced dissemination preserves epithelial identity and requires E-cadherin. J Cell Biol 204(5):839–856PubMedPubMedCentralCrossRefGoogle Scholar
  131. Shen L, Weber CR, Raleigh DR, Yu D, Turner JR (2011) Tight junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 73:283–309PubMedPubMedCentralCrossRefGoogle Scholar
  132. Shore EM, Nelson WJ (1991) Biosynthesis of the cell adhesion molecule uvomorulin (E-cadherin) in Madin-Darby canine kidney epithelial cells. J Biol Chem 266(29):19672–19680PubMedGoogle Scholar
  133. Silvis MR, Kreger BT, Lien WH, Klezovitch O, Rudakova GM, Camargo FD, Lantz DM, Seykora JT, Vasioukhin V (2011) alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 4(174):ra33PubMedPubMedCentralCrossRefGoogle Scholar
  134. Simcha I, Kirkpatrick C, Sadot E, Shtutman M, Polevoy G, Geiger B, Peifer M, Ben-Ze’ev A (2001) Cadherin sequences that inhibit beta-catenin signaling: a study in yeast and mammalian cells. Mol Biol Cell 12(4):1177–1188PubMedPubMedCentralCrossRefGoogle Scholar
  135. Simoes Sde M, Mainieri A, Zallen JA (2014) Rho GTPase and Shroom direct planar polarized actomyosin contractility during convergent extension. J Cell Biol 204(4):575–589PubMedCrossRefGoogle Scholar
  136. Smith AL, Dohn MR, Brown MV, Reynolds AB (2012) Association of Rho-associated protein kinase 1 with E-cadherin complexes is mediated by p120-catenin. Mol Biol Cell 23(1):99–110PubMedPubMedCentralCrossRefGoogle Scholar
  137. Steinberg MS (2007) Differential adhesion in morphogenesis: a modern view. Curr Opin Genet Dev 17(4):281–286PubMedCrossRefGoogle Scholar
  138. Steinberg MS, Takeichi M (1994) Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc Natl Acad Sci U S A 91(1):206–209PubMedPubMedCentralCrossRefGoogle Scholar
  139. Straub BK, Rickelt S, Zimbelmann R, Grund C, Kuhn C, Iken M, Ott M, Schirmacher P, Franke WW (2011) E-N-cadherin heterodimers define novel adherens junctions connecting endoderm-derived cells. J Cell Biol 195(5):873–887PubMedPubMedCentralCrossRefGoogle Scholar
  140. Suyama K, Shapiro I, Guttman M, Hazan RB (2002) A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2(4):301–314PubMedCrossRefGoogle Scholar
  141. Takahashi K, Nakanishi H, Miyahara M, Mandai K, Satoh K, Satoh A, Nishioka H, Aoki J, Nomoto A, Mizoguchi A, Takai Y (1999) 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(3):539–549PubMedPubMedCentralCrossRefGoogle Scholar
  142. Takai Y, Miyoshi J, Ikeda W, Ogita H (2008) Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol 9(8):603–615PubMedCrossRefGoogle Scholar
  143. Takeda H, Nagafuchi A, Yonemura S, Tsukita S, Behrens J, Birchmeier W (1995) V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J Cell Biol 131(6 Pt 2):1839–1847PubMedCrossRefGoogle Scholar
  144. Takeichi M (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251(5000):1451–1455PubMedCrossRefGoogle Scholar
  145. Takeichi M, Abe K (2005) Synaptic contact dynamics controlled by cadherin and catenins. Trends Cell Biol 15(4):216–221PubMedCrossRefGoogle Scholar
  146. Tamada M, Farrell DL, Zallen JA (2012) Abl regulates planar polarized junctional dynamics through beta-catenin tyrosine phosphorylation. Dev Cell 22(2):309–319PubMedPubMedCentralCrossRefGoogle Scholar
  147. Theveneau E, Mayor R (2012) Cadherins in collective cell migration of mesenchymal cells. Curr Opin Cell Biol 24(5):677–684PubMedCrossRefGoogle Scholar
  148. Theveneau E, Marchant L, Kuriyama S, Gull M, Moepps B, Parsons M, Mayor R (2010) Collective chemotaxis requires contact-dependent cell polarity. Dev Cell 19(1):39–53PubMedPubMedCentralCrossRefGoogle Scholar
  149. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139(5):871–890PubMedCrossRefGoogle Scholar
  150. Townes PL, Holtfreter J (1955) Directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool 128:53–120CrossRefGoogle Scholar
  151. Tsukita S, Furuse M (2002) Claudin-based barrier in simple and stratified cellular sheets. Curr Opin Cell Biol 14(5):531–536PubMedCrossRefGoogle Scholar
  152. Tumaneng K, Russell RC, Guan KL (2012) Organ size control by Hippo and TOR pathways. Curr Biol 22(9):R368–R379PubMedPubMedCentralCrossRefGoogle Scholar
  153. Van Itallie CM, Anderson JM (2013) Claudin interactions in and out of the tight junction. Tissue Barriers 1(3):e25247PubMedPubMedCentralCrossRefGoogle Scholar
  154. van Roy F, Berx G (2008) The cell-cell adhesion molecule E-cadherin. Cell Mol Life Sci 65(23):3756–3788PubMedCrossRefGoogle Scholar
  155. Vestweber D, Gossler A, Boller K, Kemler R (1987) Expression and distribution of cell adhesion molecule uvomorulin in mouse preimplantation embryos. Dev Biol 124:451–456PubMedCrossRefGoogle Scholar
  156. Vestweber D, Broermann A, Schulte D (2010) Control of endothelial barrier function by regulating vascular endothelial-cadherin. Curr Opin Hematol 17(3):230–236PubMedCrossRefGoogle Scholar
  157. Volk T, Cohen O, Geiger B (1987) Formation of heterotypic adherens-type junctions between L-CAM-containing liver cells and A-CAM-containing lens cells. Cell 50(6):987–994PubMedCrossRefGoogle Scholar
  158. Webb DJ, Parsons JT, Horwitz AF (2002) Adhesion assembly, disassembly and turnover in migrating cells -- over and over and over again. Nat Cell Biol 4(4):E97–E100PubMedCrossRefGoogle Scholar
  159. Weber GF, Bjerke MA, DeSimone DW (2012) A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 22(1):104–115PubMedPubMedCentralCrossRefGoogle Scholar
  160. Wegener KL, Partridge AW, Han J, Pickford AR, Liddington RC, Ginsberg MH, Campbell ID (2007) Structural basis of integrin activation by talin. Cell 128(1):171–182PubMedCrossRefGoogle Scholar
  161. Wheelock MJ, Johnson KR (2003) Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15(5):509–514PubMedCrossRefGoogle Scholar
  162. Wheelock MJ, Shintani Y, Maeda M, Fukumoto Y, Johnson KR (2008) Cadherin switching. J Cell Sci 121(Pt 6):727–735PubMedCrossRefGoogle Scholar
  163. Williams EJ, Williams G, Howell FV, Skaper SD, Walsh FS, Doherty P (2001) Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. J Biol Chem 276(47):43879–43886PubMedCrossRefGoogle Scholar
  164. Winkel GK, Ferguson JE, Takeichi M, Nuccitelli R (1990) Activation of protein kinase C triggers premature compaction in the four-cell stage mouse embryo. Dev Biol 138(1):1–15PubMedCrossRefGoogle Scholar
  165. Wirtz-Peitz F, Zallen JA (2009) Junctional trafficking and epithelial morphogenesis. Curr Opin Genet Dev 19(4):350–356PubMedPubMedCentralCrossRefGoogle Scholar
  166. Wizenmann A, Lumsden A (1997) Segregation of rhombomeres by differential chemoaffinity. Mol Cell Neurosci 9(5–6):448–459PubMedCrossRefGoogle Scholar
  167. Wong LE, Reynolds AB, Dissanayaka NT, Minden A (2010) p120-catenin is a binding partner and substrate for Group B Pak kinases. J Cell Biochem 110(5):1244–1254PubMedCrossRefGoogle Scholar
  168. Wood W, Jacinto A, Grose R, Woolner S, Gale J, Wilson C, Martin P (2002) Wound healing recapitulates morphogenesis in Drosophila embryos. Nat Cell Biol 4(11):907–912PubMedCrossRefGoogle Scholar
  169. Wu Y, Jin X, Harrison O, Shapiro L, Honig BH, Ben-Shaul A (2010) Cooperativity between trans and cis interactions in cadherin-mediated junction formation. Proc Natl Acad Sci U S A 107(41):17592–17597PubMedPubMedCentralCrossRefGoogle Scholar
  170. Wu Y, Kanchanawong P, Zaidel-Bar R (2015) Actin-delimited adhesion-independent clustering of E-cadherin forms the nanoscale building blocks of adherens junctions. Dev Cell 32(2):139–154PubMedCrossRefGoogle Scholar
  171. Xiao K, Garner J, Buckley KM, Vincent PA, Chiasson CM, Dejana E, Faundez V, Kowalczyk AP (2005) p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol Biol Cell 16(11):5141–5151PubMedPubMedCentralCrossRefGoogle Scholar
  172. Yang J, Weinberg RA (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14(6):818–829PubMedCrossRefGoogle Scholar
  173. Yang CC, Graves HK, Moya IM, Tao C, Hamaratoglu F, Gladden AB, Halder G (2015) Differential regulation of the Hippo pathway by adherens junctions and apical-basal cell polarity modules. Proc Natl Acad Sci U S A 112(6):1785–1790PubMedPubMedCentralCrossRefGoogle Scholar
  174. Yap AS, Brieher WM, Gumbiner BM (1997) Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol 13:119–146PubMedCrossRefGoogle Scholar
  175. Yonemura S, Wada Y, Watanabe T, Nagafuchi A, Shibata M (2010) alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12(6):533–542PubMedCrossRefGoogle Scholar
  176. Yu FX, Zhao B, Panupinthu N, Jewell JL, Lian I, Wang LH, Zhao J, Yuan H, Tumaneng K, Li H, Fu XD, Mills GB, Guan KL (2012) Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150(4):780–791PubMedPubMedCentralCrossRefGoogle Scholar
  177. Zhong Y, Brieher WM, Gumbiner BM (1999) Analysis of C-cadherin regulation during tissue morphogenesis with an activating antibody. J Cell Biol 144(2):351–359PubMedPubMedCentralCrossRefGoogle Scholar
  178. Zipursky SL, Sanes JR (2010) Chemoaffinity revisited: dscams, protocadherins, and neural circuit assembly. Cell 143(3):343–353PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  1. 1.Center for Developmental Biology and Regenerative MedicineSeattle Children’s Research InstituteSeattleUSA
  2. 2.Department of PediatricsUniversity of Washington School of MedicineSeattleUSA

Personalised recommendations