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Cadherin mechanotransduction in tissue remodeling

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Abstract

Mechanical forces are increasingly recognized as central factors in the regulation of tissue morphogenesis and homeostasis. Central to the transduction of mechanical information into biochemical signaling is the contractile actomyosin cytoskeleton. Fluctuations in actomyosin contraction are sensed by tension sensitive systems at the interface between actomyosin and cell adhesion complexes. We review the current knowledge about the mechanical coupling of cell–cell junctions to the cytoskeleton and highlight the central role of α-catenin in this linkage. We assemble current knowledge about α-catenin’s regulation by tension and about its interactions with a diversity of proteins. We present a model in which α-catenin is a force-regulated platform for a machinery of proteins that orchestrates local cortical remodeling in response to force. Finally, we highlight recently described fundamental processes in tissue morphogenesis and argue where and how this α-catenin-dependent cadherin mechanotransduction may be involved.

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Abbreviations

ΔVBS:

Delta vinculin binding site

AJ:

Adherens junction

ARP2/3:

Actin-regulated protein

CAM:

Cell adhesion molecule

Dsc:

Desmocollin

Dsg:

Desmoglein

EC:

Extracellular cadherin

ECM:

Extracellular matrix

EMT:

Epithelial to mesenchymal transition

EPLIN:

Epithelial protein lost in neoplasia

F-actin:

Filamentous actin

FAJ:

Focal adherens junction

FAK:

Focal adhesion kinase

FH:

Formin homology

HGF:

Hepatocyte growth factor

JAM:

Junctional adhesion molecule

LAJ:

Linear adherens junction

MTC:

Magnetic twisting cytometry

N-WASP:

Wiscott–Aldrich syndrome protein

TJ:

Tight junction

VASP:

Vasodilator-stimulated protein

YAP:

Yes-associated protein

ZA:

Zonula adherens

ZAJ:

Zonula adherens junction

ZO:

Zonula occludens

References

  1. Farquhar MG, Palade GE (1963) Junctional complexes in various epithelia. J Cell Biol 17:375–412

    Article  CAS  PubMed  Google Scholar 

  2. Volk T, Geiger B (1984) A 135-kd membrane protein of intercellular adherens junctions. EMBO J 3(10):2249–2260

    CAS  PubMed  Google Scholar 

  3. Takeichi M (1977) Functional correlation between cell adhesive properties and some cell surface proteins. J Cell Biol 75(2 Pt 1):464–474

    Article  CAS  PubMed  Google Scholar 

  4. Yoshida-Noro C, Suzuki N, Takeichi M (1984) Molecular nature of the calcium-dependent cell–cell adhesion system in mouse teratocarcinoma and embryonic cells studied with a monoclonal antibody. Dev Biol 101(1):19–27

    Article  CAS  PubMed  Google Scholar 

  5. Peyrieras N et al (1983) Uvomorulin: a nonintegral membrane protein of early mouse embryo. Proc Natl Acad Sci USA 80(20):6274–6277

    Article  CAS  PubMed  Google Scholar 

  6. Mege RM et al (1988) Construction of epithelioid sheets by transfection of mouse sarcoma cells with cDNAs for chicken cell adhesion molecules. Proc Natl Acad Sci USA 85(19):7274–7278

    Article  CAS  PubMed  Google Scholar 

  7. Hulpiau P, van Roy F (2009) Molecular evolution of the cadherin superfamily. Int J Biochem Cell Biol 41(2):349–369

    Article  CAS  PubMed  Google Scholar 

  8. Ozawa M, Baribault H, Kemler R (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8(6):1711–1717

    CAS  PubMed  Google Scholar 

  9. Davis MA, Ireton RC, Reynolds AB (2003) A core function for p120-catenin in cadherin turnover. J Cell Biol 163(3):525–534

    Article  CAS  PubMed  Google Scholar 

  10. Hinck L et al (1994) Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly. J Cell Biol 125(6):1327–1340

    Article  CAS  PubMed  Google Scholar 

  11. Takahashi K et al (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):539–549

    Article  CAS  PubMed  Google Scholar 

  12. Stevenson BR et al (1986) 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(3):755–766

    Article  CAS  PubMed  Google Scholar 

  13. Gumbiner B, Lowenkopf T, Apatira D (1991) Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc Natl Acad Sci USA 88(8):3460–3464

    Article  CAS  PubMed  Google Scholar 

  14. Haskins J et al (1998) 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(1):199–208

    Article  CAS  PubMed  Google Scholar 

  15. Furuse M et al (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123(6 Pt 2):1777–1788

    Article  CAS  PubMed  Google Scholar 

  16. Saitou M et al (1998) Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions. J Cell Biol 141(2):397–408

    Article  CAS  PubMed  Google Scholar 

  17. Furuse M et al (1998) Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141(7):1539–1550

    Article  CAS  PubMed  Google Scholar 

  18. Franke WW et al (1981) Antibodies to high molecular weight polypeptides of desmosomes: specific localization of a class of junctional proteins in cells and tissue. Differentiation 20(3):217–241

    Article  CAS  PubMed  Google Scholar 

  19. Franke WW et al (1983) Significance of two desmosome plaque-associated polypeptides of molecular weights 75 000 and 83 000. EMBO J 2(12):2211–2215

    CAS  PubMed  Google Scholar 

  20. Koch PJ et al (1990) Identification of desmoglein, a constitutive desmosomal glycoprotein, as a member of the cadherin family of cell adhesion molecules. Eur J Cell Biol 53(1):1–12

    CAS  PubMed  Google Scholar 

  21. Koch PJ et al (1991) Amino acid sequence of bovine muzzle epithelial desmocollin derived from cloned cDNA: a novel subtype of desmosomal cadherins. Differentiation 47(1):29–36

    Article  CAS  PubMed  Google Scholar 

  22. Niessen CM (2007) Tight junctions/adherens junctions: basic structure and function. J Invest Dermatol 127(11):2525–2532

    Article  CAS  PubMed  Google Scholar 

  23. Watabe-Uchida M et al (1998) alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells. J Cell Biol 142(3):847–857

    Article  CAS  PubMed  Google Scholar 

  24. Kametani Y, Takeichi M (2007) Basal-to-apical cadherin flow at cell junctions. Nat Cell Biol 9(1):92–98

    Article  CAS  PubMed  Google Scholar 

  25. Yonemura S et al (1995) Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. J Cell Sci 108(Pt 1):127–142

    CAS  PubMed  Google Scholar 

  26. Sakisaka T et al (2007) The roles of nectins in cell adhesions: cooperation with other cell adhesion molecules and growth factor receptors. Curr Opin Cell Biol 19(5):593–602

    Article  CAS  PubMed  Google Scholar 

  27. Adams CL, Nelson WJ (1998) Cytomechanics of cadherin-mediated cell–cell adhesion. Curr Opin Cell Biol 10(5):572–577

    Article  CAS  PubMed  Google Scholar 

  28. Vasioukhin V et al (2000) Directed actin polymerization is the driving force for epithelial cell–cell adhesion. Cell 100(2):209–219

    Article  CAS  PubMed  Google Scholar 

  29. Ayollo DV et al (2009) Rearrangements of the actin cytoskeleton and E-cadherin-based adherens junctions caused by neoplasic transformation change cell–cell interactions. PLoS One 4(11):e8027

    Article  PubMed  CAS  Google Scholar 

  30. de Rooij J et al (2005) Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J Cell Biol 171(1):153–164

    Article  PubMed  CAS  Google Scholar 

  31. Loerke D et al (2012) Quantitative imaging of epithelial cell scattering identifies specific inhibitors of cell motility and cell–cell dissociation. Sci Signal 5(231):rs5

    Article  PubMed  CAS  Google Scholar 

  32. Taguchi K, Ishiuchi T, Takeichi M (2011) Mechanosensitive EPLIN-dependent remodeling of adherens junctions regulates epithelial reshaping. J Cell Biol 194(4):643–656

    Article  PubMed  CAS  Google Scholar 

  33. Huveneers S et al (2012) Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J Cell Biol 196(5):641–652

    Article  CAS  PubMed  Google Scholar 

  34. Millan J et al (2010) Adherens junctions connect stress fibres between adjacent endothelial cells. BMC Biol 8:11

    Article  PubMed  CAS  Google Scholar 

  35. Shewan AM et al (2005) Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell–cell contacts. Mol Biol Cell 16(10):4531–4542

    Article  CAS  PubMed  Google Scholar 

  36. Miyake Y et al (2006) Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp Cell Res 312(9):1637–1650

    Article  CAS  PubMed  Google Scholar 

  37. 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 USA 105(1):13–19

    Article  CAS  PubMed  Google Scholar 

  38. Ratheesh A et al (2012) Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat Cell Biol 14(8):818–828

    Article  CAS  PubMed  Google Scholar 

  39. Drees F et al (2005) Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123(5):903–915

    Article  CAS  PubMed  Google Scholar 

  40. Yamada S et al (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123(5):889–901

    Article  CAS  PubMed  Google Scholar 

  41. Ogita H et al (2010) Cell adhesion molecules nectins and associating proteins: implications for physiology and pathology. Proc Jpn Acad B 86(6):621–629

    Article  CAS  PubMed  Google Scholar 

  42. Takai Y et al (2008) The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu Rev Cell Dev Biol 24:309–342

    Article  CAS  PubMed  Google Scholar 

  43. Noren NK et al (2001) Cadherin engagement regulates Rho family GTPases. J Biol Chem 276(36):33305–33308

    Article  CAS  PubMed  Google Scholar 

  44. Sakurai A et al (2006) MAGI-1 is required for Rap1 activation upon cell–cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol Biol Cell 17(2):966–976

    Article  CAS  PubMed  Google Scholar 

  45. McLachlan RW et al (2007) E-cadherin adhesion activates c-Src signaling at cell–cell contacts. Mol Biol Cell 18(8):3214–3223

    Article  CAS  PubMed  Google Scholar 

  46. Kovacs EM et al (2002) Cadherin-directed actin assembly: e-cadherin physically associates with the Arp2/3 complex to direct actin assembly in nascent adhesive contacts. Curr Biol 12(5):379–382

    Article  CAS  PubMed  Google Scholar 

  47. Helwani FM et al (2004) Cortactin is necessary for E-cadherin-mediated contact formation and actin reorganization. J Cell Biol 164(6):899–910

    Article  CAS  PubMed  Google Scholar 

  48. Kovacs EM et al (2011) N-WASP regulates the epithelial junctional actin cytoskeleton through a non-canonical post-nucleation pathway. Nat Cell Biol 13(8):934–943

    Article  CAS  PubMed  Google Scholar 

  49. Kobielak A, Pasolli HA, Fuchs E (2004) Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 6(1):21–30

    Article  CAS  PubMed  Google Scholar 

  50. Smutny M et al (2010) Myosin II isoforms identify distinct functional modules that support integrity of the epithelial zonula adherens. Nat Cell Biol 12(7):696–702

    Article  CAS  PubMed  Google Scholar 

  51. Ratheesh A, Yap AS (2012) A bigger picture: classical cadherins and the dynamic actin cytoskeleton. Nat Rev Mol Cell Biol 13(10):673–679

    Article  CAS  PubMed  Google Scholar 

  52. Brieher WM, Yap AS (2013) Cadherin junctions and their cytoskeleton(s). Curr Opin Cell Biol 25(1):39–46

    Google Scholar 

  53. Georgiou M et al (2008) Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18(21):1631–1638

    Article  CAS  PubMed  Google Scholar 

  54. Angres B, Barth A, Nelson WJ (1996) Mechanism for transition from initial to stable cell–cell adhesion: kinetic analysis of E-cadherin-mediated adhesion using a quantitative adhesion assay. J Cell Biol 134(2):549–557

    Article  CAS  PubMed  Google Scholar 

  55. Lambert M et al (2007) Nucleation and growth of cadherin adhesions. Exp Cell Res 313(19):4025–4040

    Article  CAS  PubMed  Google Scholar 

  56. Krendel M et al (1999) Myosin-dependent contractile activity of the actin cytoskeleton modulates the spatial organization of cell–cell contacts in cultured epitheliocytes. Proc Natl Acad Sci USA 96(17):9666–9670

    Article  CAS  PubMed  Google Scholar 

  57. Gloushankova NA et al (1998) Dynamics of contacts between lamellae of fibroblasts: essential role of the actin cytoskeleton. Proc Natl Acad Sci USA 95(8):4362–4367

    Article  CAS  PubMed  Google Scholar 

  58. Twiss F et al (2012) Vinculin-dependent Cadherin mechanosensing regulates efficient epithelial barrier formation. Biol Open 1(11):1128–1140

    Article  CAS  PubMed  Google Scholar 

  59. le Duc Q et al (2010) Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 189(7):1107–1115

    Article  PubMed  Google Scholar 

  60. Pokutta S et al (2002) Biochemical and structural definition of the l-afadin- and actin-binding sites of alpha-catenin. J Biol Chem 277(21):18868–18874

    Article  CAS  PubMed  Google Scholar 

  61. Tachibana K et al (2000) Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J Cell Biol 150(5):1161–1176

    Article  CAS  PubMed  Google Scholar 

  62. Yamamoto T et al (1997) The Ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol 139(3):785–795

    Article  CAS  PubMed  Google Scholar 

  63. Ooshio T et al (2010) Involvement of the interaction of afadin with ZO-1 in the formation of tight junctions in Madin-Darby canine kidney cells. J Biol Chem 285(7):5003–5012

    Article  CAS  PubMed  Google Scholar 

  64. Imamura Y et al (1999) Functional domains of alpha-catenin required for the strong state of cadherin-based cell adhesion. J Cell Biol 144(6):1311–1322

    Article  CAS  PubMed  Google Scholar 

  65. Rajasekaran AK et al (1996) Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J Cell Biol 132(3):451–463

    Article  CAS  PubMed  Google Scholar 

  66. Mandai K et al (1997) Afadin: a novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J Cell Biol 139(2):517–528

    Article  CAS  PubMed  Google Scholar 

  67. Gumbiner B, Stevenson B, Grimaldi A (1988) The role of the cell adhesion molecule uvomorulin in the formation and maintenance of the epithelial junctional complex. J Cell Biol 107(4):1575–1587

    Article  CAS  PubMed  Google Scholar 

  68. Ikeda W et al (1999) Afadin: a key molecule essential for structural organization of cell–cell junctions of polarized epithelia during embryogenesis. J Cell Biol 146(5):1117–1132

    Article  CAS  PubMed  Google Scholar 

  69. Sawyer JK et al (2011) A contractile actomyosin network linked to adherens junctions by Canoe/afadin helps drive convergent extension. Mol Biol Cell 22(14):2491–2508

    Article  CAS  PubMed  Google Scholar 

  70. Sawyer JK et al (2009) The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction. J Cell Biol 186(1):57–73

    Article  CAS  PubMed  Google Scholar 

  71. Yonemura S et al (2010) alpha-Catenin as a tension transducer that induces adherens junction development. Nat Cell Biol 12(6):533–542

    Article  CAS  PubMed  Google Scholar 

  72. Kwiatkowski AV et al (2010) In vitro and in vivo reconstitution of the cadherin-catenin-actin complex from Caenorhabditis elegans. Proc Natl Acad Sci USA 107(33):14591–14596

    Article  CAS  PubMed  Google Scholar 

  73. Rangarajan ES, Izard T (2012) The cytoskeletal protein alpha-catenin unfurls upon binding to vinculin. J Biol Chem 287(22):18492–18499

    Article  CAS  PubMed  Google Scholar 

  74. Choi HJ et al (2012) alphaE-catenin is an autoinhibited molecule that coactivates vinculin. Proc Natl Acad Sci USA 109(22):8576–8581

    Article  CAS  PubMed  Google Scholar 

  75. Nieset JE et al (1997) Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin. J Cell Sci 110(Pt 8):1013–1022

    CAS  PubMed  Google Scholar 

  76. Huttelmaier S et al (1997) Characterization of two F-actin-binding and oligomerization sites in the cell-contact protein vinculin. Eur J Biochem 247(3):1136–1142

    Article  CAS  PubMed  Google Scholar 

  77. Wen KK, Rubenstein PA, DeMali KA (2009) Vinculin nucleates actin polymerization and modifies actin filament structure. J Biol Chem 284(44):30463–30473

    Article  CAS  PubMed  Google Scholar 

  78. Scott JA et al (2006) Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts. Mol Biol Cell 17(3):1085–1095

    Article  CAS  PubMed  Google Scholar 

  79. DeMali KA, Burridge K (2003) Coupling membrane protrusion and cell adhesion. J Cell Sci 116(Pt 12):2389–2397

    Article  CAS  PubMed  Google Scholar 

  80. Otey CA, Carpen O (2004) Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskelet 58(2):104–111

    Article  CAS  Google Scholar 

  81. Nola S et al (2011) Ajuba is required for Rac activation and maintenance of E-cadherin adhesion. J Cell Biol 195(5):855–871

    Article  CAS  PubMed  Google Scholar 

  82. Dobrosotskaya IY, James GL (2000) MAGI-1 interacts with beta-catenin and is associated with cell–cell adhesion structures. Biochem Biophys Res Commun 270(3):903–909

    Article  CAS  PubMed  Google Scholar 

  83. Cavey M et al (2008) A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453(7196):751–756

    Article  CAS  PubMed  Google Scholar 

  84. Farhadifar R et al (2007) The influence of cell mechanics, cell–cell interactions, and proliferation on epithelial packing. Curr Biol 17(24):2095–2104

    Article  CAS  PubMed  Google Scholar 

  85. Sumida GM et al (2011) Myosin II activity dependent and independent vinculin recruitment to the sites of E-cadherin-mediated cell–cell adhesion. BMC Cell Biol 12:48

    Article  CAS  PubMed  Google Scholar 

  86. Grashoff C et al (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466(7303):263–266

    Article  CAS  PubMed  Google Scholar 

  87. Borghi N et al (2012) E-cadherin is under constitutive actomyosin-generated tension that is increased at cell–cell contacts upon externally applied stretch. Proc Natl Acad Sci USA 109(31):12568–12573

    Article  CAS  PubMed  Google Scholar 

  88. Weber GF, Bjerke MA, DeSimone DW (2011) Integrins and cadherins join forces to form adhesive networks. J Cell Sci 124(Pt 8):1183–1193

    Article  CAS  PubMed  Google Scholar 

  89. Behrndt M et al (2012) Forces driving epithelial spreading in zebrafish gastrulation. Science 338(6104):257–260

    Article  CAS  PubMed  Google Scholar 

  90. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10(7):445–457

    Article  CAS  PubMed  Google Scholar 

  91. Ng MR et al (2012) Substrate stiffness regulates cadherin-dependent collective migration through myosin-II contractility. J Cell Biol 199(3):545–563

    Article  CAS  PubMed  Google Scholar 

  92. Desai RA et al (2009) Cell polarity triggered by cell–cell adhesion via E-cadherin. J Cell Sci 122(Pt 7):905–911

    Article  CAS  PubMed  Google Scholar 

  93. Krens SF, Heisenberg CP (2011) Cell sorting in development. Curr Top Dev Biol 95:189–213

    Article  PubMed  Google Scholar 

  94. Krieg M et al (2008) Tensile forces govern germ-layer organization in zebrafish. Nat Cell Biol 10(4):429–436

    Article  CAS  PubMed  Google Scholar 

  95. Maitre JL et al (2012) Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338(6104):253–256

    Article  CAS  PubMed  Google Scholar 

  96. Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457(7228):495–499

    Article  CAS  PubMed  Google Scholar 

  97. Martin AC et al (2010) Integration of contractile forces during tissue invagination. J Cell Biol 188(5):735–749

    Article  CAS  PubMed  Google Scholar 

  98. Rauzi M, Lenne PF, Lecuit T (2010) Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468(7327):1110–1114

    Article  CAS  PubMed  Google Scholar 

  99. Solon J et al (2009) Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137(7):1331–1342

    Article  PubMed  Google Scholar 

  100. He L et al (2010) Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat Cell Biol 12(12):1133–1142

    Article  CAS  PubMed  Google Scholar 

  101. Moore KA et al (2005) Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232(2):268–281

    Article  CAS  PubMed  Google Scholar 

  102. Paszek MJ et al (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241–254

    Article  CAS  PubMed  Google Scholar 

  103. Alcaraz J et al (2008) Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J 27(21):2829–2838

    Article  CAS  PubMed  Google Scholar 

  104. Santos OF, Nigam SK (1993) HGF-induced tubulogenesis and branching of epithelial cells is modulated by extracellular matrix and TGF-beta. Dev Biol 160(2):293–302

    Article  CAS  PubMed  Google Scholar 

  105. Pozzi A, Zent R (2011) Extracellular matrix receptors in branched organs. Curr Opin Cell Biol 23(5):547–553

    Article  CAS  PubMed  Google Scholar 

  106. Zebda N, Dubrovskyi O, Birukov KG (2012) Focal adhesion kinase regulation of mechanotransduction and its impact on endothelial cell functions. Microvasc Res 83(1):71–81

    Article  CAS  PubMed  Google Scholar 

  107. Daley WP, Kohn JM, Larsen M (2011) A focal adhesion protein-based mechanochemical checkpoint regulates cleft progression during branching morphogenesis. Dev Dyn 240(9):2069–2083

    Article  CAS  PubMed  Google Scholar 

  108. van Miltenburg MH et al (2009) Complete focal adhesion kinase deficiency in the mammary gland causes ductal dilation and aberrant branching morphogenesis through defects in Rho kinase-dependent cell contractility. FASEB J 23(10):3482–3493

    Article  PubMed  CAS  Google Scholar 

  109. Zhang YW, Vande Woude GF (2003) HGF/SF-met signaling in the control of branching morphogenesis and invasion. J Cell Biochem 88(2):408–417

    Article  CAS  PubMed  Google Scholar 

  110. Provenzano PP, Keely PJ (2011) Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J Cell Sci 124(Pt 8):1195–1205

    Article  CAS  PubMed  Google Scholar 

  111. Engler AJ et al (2006) Matrix elasticity directs stem cell lineage specification. Cell 126(4):677–689

    Article  CAS  PubMed  Google Scholar 

  112. Dupont S et al (2011) Role of YAP/TAZ in mechanotransduction. Nature 474(7350):179–183

    Article  CAS  PubMed  Google Scholar 

  113. Cordenonsi M et al (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147(4):759–772

    Article  CAS  PubMed  Google Scholar 

  114. Kim NG et al (2011) E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci USA 108(29):11930–11935

    Article  CAS  PubMed  Google Scholar 

  115. Silvis MR et al (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):ra33

    Article  PubMed  CAS  Google Scholar 

  116. Schlegelmilch K et al (2011) Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 144(5):782–795

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Johan de Rooij and Floor Twiss were supported by a grant from the Netherlands Scientific Organization (NWO-VIDI).

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  1. Hubrecht Institute for Developmental Biology and Stem Cell Research and University Medical Centre Utrecht, Uppsalalaan 8, 3884 CT, Utrecht, The Netherlands

    Floor Twiss & Johan de Rooij

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Correspondence to Johan de Rooij.

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Twiss, F., de Rooij, J. Cadherin mechanotransduction in tissue remodeling. Cell. Mol. Life Sci. 70, 4101–4116 (2013). https://doi.org/10.1007/s00018-013-1329-x

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