The mechanotransduction machinery at work at adherens junctions

Integrative Biology (United Kingdom)

Volumn 7, Issue 10, 2015, Pages 1109-1119

  Ladoux, B ^a,b   Nelson, W J ^c   Yan, J ^b,d   Mege R M ^a  

^a INSTITUT JACQUES MONOD   (France)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c STANFORD UNIVERSITY   (United States)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ALPHA CATENIN; BETA CATENIN; CADHERIN; CATENIN; CYTOPLASM PROTEIN; UVOMORULIN; VINCULIN; ACTIN;

CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL JUNCTION; CELL MIGRATION; CELL MOTION; CELL SHAPE; CELL SURVIVAL; CONFORMATIONAL TRANSITION; EXTRACELLULAR MATRIX; MECHANICAL STRESS; MECHANOTRANSDUCTION; MICROENVIRONMENT; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; ADHERENS JUNCTION; ANIMAL; BIOLOGICAL MODEL; BIOMECHANICS; CHEMISTRY; HUMAN; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN UNFOLDING; TUMOR MICROENVIRONMENT;

ACTINS; ADHERENS JUNCTIONS; ANIMALS; BIOMECHANICAL PHENOMENA; CADHERINS; CATENINS; CELL ADHESION; CELLULAR MICROENVIRONMENT; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; PROTEIN UNFOLDING;

EID: 84943385272     PISSN: 17579694     EISSN: 17579708     Source Type: Journal    
DOI: 10.1039/c5ib00070j     Document Type: Review

References (109)

1. D. W. Thompson, On growth and form, Cambridge University Press, Cambridge, UK, 1917
2. C. Guillot T. Lecuit Mechanics of epithelial tissue homeostasis and morphogenesis Science 2013 340 1185 1189
3. M. Cetera G. R. Ramirez-San Juan P. W. Oakes L. Lewellyn M. J. Fairchild G. Tanentzapf M. L. Gardel S. Horne-Badovinac Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation Nat. Commun. 2014 5 5511
4. J. L. Maitre H. Berthoumieux S. F. Krens G. Salbreux F. Julicher E. Paluch C. P. Heisenberg Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells Science 2012 338 253 256
5. C. P. Heisenberg Y. Bellaiche Forces in tissue morphogenesis and patterning Cell 2013 153 948 962
6. E. Anon X. Serra-Picamal P. Hersen N. C. Gauthier M. P. Sheetz X. Trepat B. Ladoux Cell crawling mediates collective cell migration to close undamaged epithelial gaps Proc. Natl. Acad. Sci. U. S. A. 2012 109 10891 10896
7. S. R. K. Vedula H. Hirata M. H. Nai A. Brugues Y. Toyama X. Trepat C. T. Lim B. Ladoux Epithelial bridges maintain tissue integrity during collective cell migration Nat. Mater. 2014 13 87 96
8. J. K. Mouw Y. Yui L. Damiano R. O. Bainer J. N. Lakins I. Acerbi G. Ou A. C. Wijekoon K. R. Levental P. M. Gilbert et al. Tissue mechanics modulate microRNA-dependent PTEN expression to regulate malignant progression Nat. Med. 2014 20 360 367
9. H. Yu J. K. Mouw V. M. Weaver Forcing form and function: biomechanical regulation of tumor evolution Trends Cell Biol. 2011 21 47 56
10. M. Takeichi Dynamic contacts: rearranging adherens junctions to drive epithelial remodelling Nat. Rev. Mol. Cell Biol. 2014 15 397 410
11. T. J. Harris U. Tepass Adherens junctions: from molecules to morphogenesis Nat. Rev. Mol. Cell Biol. 2010 11 502 514
12. D. J. Montell Morphogenetic cell movements: diversity from modular mechanical properties Science 2008 322 1502 1505
13. B. Ladoux A. Nicolas Physically based principles of cell adhesion mechanosensitivity in tissues Rep. Prog. Phys. 2012 75 116601
14. D. Mitrossilis J. Fouchard D. Pereira F. Postic A. Richert M. Saint-Jean A. Asnacios Real-time single-cell response to stiffness Proc. Natl. Acad. Sci. U. S. A. 2010 107 16518 16523
15. A. Munjal T. Lecuit Actomyosin networks and tissue morphogenesis Development 2014 141 1789 1793
16. D. Mitrossilis J. Fouchard A. Guiroy N. Desprat N. Rodriguez B. Fabry A. Asnacios Single-cell response to stiffness exhibits muscle-like behavior Proc. Natl. Acad. Sci. U. S. A. 2009 106 18243 18248
17. Y. Mao B. Baum Tug of war-The influence of opposing physical forces on epithelial cell morphology Dev. Biol. 2015 401 92 102
18. S. Ishihara K. Sugimura S. J. Cox I. Bonnet Y. Bellaiche F. Graner Comparative study of non-invasive force and stress inference methods in tissue Eur. Phys. J. E: Soft Matter Biol. Phys. 2013 36 9859
19. V. Vogel M. Sheetz Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 2006 7 265 275
20. A. Bershadsky M. Kozlov B. Geiger Adhesion-mediated mechanosensitivity: a time to experiment, and a time to theorize Curr. Opin. Cell Biol. 2006 18 472 481
21. D. E. Leckband J. de Rooij Cadherin adhesion and mechanotransduction Annu. Rev. Cell Dev. Biol. 2014 30 291 315
22. A. Ganz M. Lambert A. Saez P. Silberzan A. Buguin R. M. Mege B. Ladoux Traction forces exerted through N-cadherin contacts Biol. Cell. 2006 98 721 730
23. B. Ladoux E. Anon M. Lambert A. Rabodzey P. Hersen A. Buguin P. Silberzan R. M. Mege Strength dependence of cadherin-mediated adhesions Biophys. J. 2010 98 534 542
24. P. Hulpiau I. S. Gul F. van Roy New insights into the evolution of metazoan cadherins and catenins Prog. Mol. Biol. Transl. Sci. 2013 116 71 94
25. P. W. Miller D. N. Clarke W. I. Weis C. J. Lowe W. J. Nelson The evolutionary origin of epithelial cell-cell adhesion mechanisms Curr. Top. Membr. 2013 72 267 311
26. H. V. Wilson On some phenomena of coalescence and regeneration in sponges J. Exp. Zool. 1907 5 245 258
27. M. S. Steinberg Adhesion in development: an historical overview Dev. Biol. 1996 180 377 388
28. G. M. Edelman Cell adhesion molecules in the regulation of animal form and tissue pattern Annu. Rev. Cell Biol. 1986 2 81 116
29. A. J. Engler S. Sen H. L. Sweeney D. E. Discher Matrix elasticity directs stem cell lineage specification Cell 2006 126 677 689
30. B. Geiger J. P. Spatz A. D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 2009 10 21 33
31. B. Geiger A. Bershadsky R. Pankov K. M. Yamada Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk Nat. Rev. Mol. Cell Biol. 2001 2 793 805
32. T. Iskratsch H. Wolfenson M. P. Sheetz Appreciating force and shape-the rise of mechanotransduction in cell biology Nat. Rev. Mol. Cell Biol. 2014 15 825 833
33. U. S. Schwarz S. A. Safran Physics of adherent cells Rev. Mod. Phys. 2013 85 1327 1372
34. N. Q. Balaban U. S. Schwarz D. Riveline P. Goichberg G. Tzur I. Sabanay D. Mahalu S. Safran A. Bershadsky L. Addadi et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates Nat. Cell Biol. 2001 3 466 472
35. J. Stricker Y. Aratyn-Schaus P. W. Oakes M. L. Gardel Spatiotemporal constraints on the force-dependent growth of focal adhesions Biophys. J. 2011 100 2883 2893
36. S. V. Plotnikov A. M. Pasapera B. Sabass C. M. Waterman Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration Cell 2012 151 1513 1527
37. W. W. Franke Discovering the molecular components of intercellular junctions-a historical view Cold Spring Harbor Perspect. Biol. 2009 1 a003061
38. O. Nekrasova K. J. Green Desmosome assembly and dynamics Trends Cell Biol. 2013 23 537 546
39. R. M. Mege J. Gavard M. Lambert Regulation of cell-cell junctions by the cytoskeleton Curr. Opin. Cell Biol. 2006 18 541 548
40. U. Tepass G. Tanentzapf R. Ward R. Fehon Epithelial cell polarity and cell junctions in Drosophila Annu. Rev. Genet. 2001 35 747 784
41. A. Kobielak E. Fuchs Alpha-catenin: at the junction of intercellular adhesion and actin dynamics Nat. Rev. Mol. Cell Biol. 2004 5 614 625
42. S. Huveneers J. de Rooij Mechanosensitive systems at the cadherin-F-actin interface J. Cell Sci. 2013 126 403 413
43. C. L. Adams Y. T. Chen S. J. Smith W. J. Nelson Mechanisms of epithelial cell-cell adhesion and cell compaction revealed by high-resolution tracking of E-cadherin-green fluorescent protein J. Cell Biol. 1998 142 1105 1119
44. Y. Wu P. Kanchanawong R. Zaidel-Bar Actin-delimited adhesion-independent clustering of e-cadherin forms the nanoscale building blocks of adherens junctions Dev. Cell 2015 32 139 154
45. J. Gavard M. Lambert I. Grosheva V. Marthiens T. Irinopoulou J. F. Riou A. Bershadsky R. M. Mege Lamellipodium extension and cadherin adhesion: two cell responses to cadherin activation relying on distinct signalling pathways J. Cell Sci. 2004 117 257 270
46. Q. le Duc Q. Shi I. Blonk A. Sonnenberg N. Wang D. Leckband J. de Rooij Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner J. Cell Biol. 2010 189 1107 1115
47. V. Vasioukhin C. Bauer M. Yin E. Fuchs Directed actin polymerization is the driving force for epithelial cell-cell adhesion Cell 2000 100 209 219
48. J. Kartenbeck W. W. Franke J. G. Moser U. Stoffels Specific attachment of desmin filaments to desmosomal plaques in cardiac myocytes EMBO J. 1983 2 735 742
49. C. Luccardini L. Hennekinne L. Viou M. Yanagida F. Murakami N. Kessaris X. Ma R. S. Adelstein R. M. Mege C. Metin N-cadherin sustains motility and polarity of future cortical interneurons during tangential migration J. Neurosci. 2013 33 18149 18160
50. S. J. Franco I. Martinez-Garay C. Gil-Sanz S. R. Harkins-Perry U. Muller Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex Neuron 2011 69 482 497
51. L. Bard C. Boscher M. Lambert R. M. Mege D. Choquet O. Thoumine A molecular clutch between the actin flow and N-cadherin adhesions drives growth cone migration J. Neurosci. 2008 28 5879 5890
52. G. Giannone R. M. Mege O. Thoumine Multi-level molecular clutches in motile cell processes Trends Cell Biol. 2009 19 475 486
53. Y. Wu J. Vendome L. Shapiro A. Ben-Shaul B. Honig Transforming binding affinities from three dimensions to two with application to cadherin clustering Nature 2011 475 510 513
54. O. J. Harrison X. Jin S. Hong F. Bahna G. Ahlsen J. Brasch Y. Wu J. Vendome K. Felsovalyi C. M. Hampton et al. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins Structure 2011 19 244 256
55. M. Lambert D. Choquet R. M. Mege Dynamics of ligand-induced, Rac1-dependent anchoring of cadherins to the actin cytoskeleton J. Cell Biol. 2002 157 469 479
56. M. Peifer A. S. Yap Traffic control: p120-catenin acts as a gatekeeper to control the fate of classical cadherins in mammalian cells J. Cell Biol. 2003 163 437 440
57. A. Nagafuchi M. Takeichi Cell binding function of E-cadherin is regulated by the cytoplasmic domain EMBO J. 1988 7 3679 3684
58. H. Aberle S. Butz J. Stappert H. Weissig R. Kemler H. Hoschuetzky Assembly of the cadherin-catenin complex in vitro with recombinant proteins J. Cell Sci. 1994 107 3655 3663
59. S. Yamada S. Pokutta F. Drees W. I. Weis W. J. Nelson Deconstructing the cadherin-catenin-actin complex Cell 2005 123 889 901
60. M. Yao W. Qiu R. Liu A. K. Efremov P. Cong R. Seddiki M. Payre C. T. Lim B. Ladoux R. M. Mege et al. Force-dependent conformational switch of alpha-catenin controls vinculin binding Nat. Commun. 2014 5 4525
61. C. D. Buckley J. Tan K. L. Anderson D. Hanein N. Volkmann W. I. Weis W. J. Nelson A. R. Dunn Cell adhesion. The minimal cadherin-catenin complex binds to actin filaments under force Science 2014 346 1254211
62. A. K. Barry H. Tabdili I. Muhamed J. Wu N. Shashikanth G. A. Gomez A. S. Yap C. J. Gottardi J. de Rooij N. Wang et al. alpha-catenin cytomechanics-role in cadherin-dependent adhesion and mechanotransduction J. Cell Sci. 2014 127 1779 1791
63. V. Maruthamuthu M. L. Gardel Protrusive activity guides changes in cell-cell tension during epithelial cell scattering Biophys. J. 2014 107 555 563
64. H. Tabdili M. Langer Q. Shi Y. C. Poh N. Wang D. Leckband Cadherin-dependent mechanotransduction depends on ligand identity but not affinity J. Cell Sci. 2012 125 4362 4371
65. N. Borghi M. Sorokina O. G. Shcherbakova W. I. Weis B. L. Pruitt W. J. Nelson A. R. Dunn E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch Proc. Natl. Acad. Sci. U. S. A. 2012 109 12568 12573
66. D. E. Conway M. T. Breckenridge E. Hinde E. Gratton C. S. Chen M. A. Schwartz Fluid shear stress on endothelial cells modulates mechanical tension across VE-cadherin and PECAM-1 Curr. Biol. 2013 23 1024 1030
67. D. Cai S. C. Chen M. Prasad L. He X. Wang V. Choesmel-Cadamuro J. K. Sawyer G. Danuser D. J. Montell Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration Cell 2014 157 1146 1159
68. L. Trichet J. Le Digabel R. J. Hawkins S. R. Vedula M. Gupta C. Ribrault P. Hersen R. Voituriez B. Ladoux Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness Proc. Natl. Acad. Sci. U. S. A. 2012 109 6933 6938
69. Cas Cell 2006 127 1015 1026
70. A. del Rio R. Perez-Jimenez R. Liu P. Roca-Cusachs J. M. Fernandez M. P. Sheetz Stretching single talin rod molecules activates vinculin binding Science 2009 323 638 641
71. M. Yao B. T. Goult H. Chen P. Cong M. P. Sheetz J. Yan Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation Sci. Rep. 2014 4 4610
72. B. L. Pruitt A. R. Dunn W. I. Weis W. J. Nelson Mechano-transduction: from molecules to tissues PLoS Biol. 2014 12 e1001996
73. P. Kanchanawong G. Shtengel A. M. Pasapera E. B. Ramko M. W. Davidson H. F. Hess C. M. Waterman Nanoscale architecture of integrin-based cell adhesions Nature 2010 468 580 584
74. S. Yonemura Y. Wada T. Watanabe A. Nagafuchi M. Shibata alpha-Catenin as a tension transducer that induces adherens junction development Nat. Cell Biol. 2010 12 533 542
75. S. Huveneers J. Oldenburg E. Spanjaard G. van der Krogt I. Grigoriev A. Akhmanova H. Rehmann J. de Rooij Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling J. Cell Biol. 2012 196 641 652
76. W. A. Thomas C. Boscher Y.-S. Chu D. Cuvelier C. Martinez-Rico R. Seddiki J. Heysch B. Ladoux J. P. Thiery R.-M. Mege et al. α-Catenin and vinculin cooperate to promote high E-cadherin-based adhesion strength J. Biol. Chem. 2013 288 4957 4969
77. M. Watabe-Uchida N. Uchida Y. Imamura A. Nagafuchi K. Fujimoto T. Uemura S. Vermeulen F. van Roy E. D. Adamson M. Takeichi alpha-Catenin-vinculin interaction functions to organize the apical junctional complex in epithelial cells J. Cell Biol. 1998 142 847 857
78. X. Peng L. E. Cuff C. D. Lawton K. A. DeMali Vinculin regulates cell-surface E-cadherin expression by binding to beta-catenin J. Cell Sci. 2010 123 567 577
79. H. J. Choi S. Pokutta G. W. Cadwell A. A. Bobkov L. A. Bankston R. C. Liddington W. I. Weis alpha-E-catenin is an autoinhibited molecule that coactivates vinculin Proc. Natl. Acad. Sci. U. S. A. 2012 109 8576 8581
80. N. Ishiyama N. Tanaka K. Abe Y. J. Yang Y. M. Abbas M. Umitsu B. Nagar S. A. Bueler J. L. Rubinstein M. Takeichi et al. An Autoinhibited Structure of α-catenin and Its Implications for Vinculin Recruitment to Adherens Junctions J. Biol. Chem. 2013 288 15913 15925
81. E. S. Rangarajan T. Izard The cytoskeletal protein alpha-catenin unfurls upon binding to vinculin J. Biol. Chem. 2012 287 18492 18499
82. D. M. Cohen H. Chen R. P. Johnson B. Choudhury S. W. Craig Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin J. Biol. Chem. 2005 280 17109 17117
83. P. R. J. Bois B. P. O'Hara D. Nietlispach J. Kirkpatrick T. Izard The vinculin binding sites of talin and alpha-actinin are sufficient to activate vinculin J. Biol. Chem. 2006 281 7228 7236
84. Y. Imamura M. Itoh Y. Maeno S. Tsukita A. Nagafuchi Functional domains of alpha-catenin required for the strong state of cadherin-based cell adhesion J. Cell Biol. 1999 144 1311 1322
85. M. Itoh Involvement of ZO-1 in Cadherin-based Cell Adhesion through Its Direct Binding to alpha Catenin and Actin Filaments J. Cell Biol. 1997 138 181 192
86. S. Pokutta F. Drees Y. Takai W. J. Nelson W. I. Weis Biochemical and structural definition of the l-afadin- and actin-binding sites of alpha-catenin J. Biol. Chem. 2002 277 18868 18874
87. J. E. Nieset A. R. Redfield F. Jin K. A. Knudsen K. R. Johnson M. J. Wheelock Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin J. Cell Sci. 1997 110 Pt 8 1013 1022
88. A. Kobielak H. A. Pasolli E. Fuchs Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables Nat. Cell Biol. 2004 6 21 30
89. K. Abe M. Takeichi EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt Proc. Natl. Acad. Sci. U. S. A. 2008 105 13 19
90. A. Valbuena A. M. Vera J. Oroz M. Menendez M. Carrion-Vazquez Mechanical properties of beta-catenin revealed by single-molecule experiments Biophys. J. 2012 103 1744 1752
91. S. Rakshit Y. Zhang K. Manibog O. Shafraz S. Sivasankar Ideal, catch, and slip bonds in cadherin adhesion Proc. Natl. Acad. Sci. U. S. A. 2012 109 18815 18820
92. T. J. Kim S. Zheng J. Sun I. Muhamed J. Wu L. Lei X. Kong D. E. Leckband Y. Wang Dynamic Visualization of alpha-Catenin Reveals Rapid, Reversible Conformation Switching between Tension States Curr. Biol. 2015 25 218 224
93. K. Chinthalapudi E. S. Rangarajan D. N. Patil E. M. George D. T. Brown T. Izard Lipid binding promotes oligomerization and focal adhesion activity of vinculin J. Cell Biol. 2014 207 643 656
94. J. M. Leerberg G. A. Gomez S. Verma E. J. Moussa S. K. Wu R. Priya B. D. Hoffman C. Grashoff M. A. Schwartz A. S. Yap Tension-sensitive actin assembly supports contractility at the epithelial zonula adherens Curr. Biol. 2014 24 1689 1699
95. M. Rauzi P. F. Lenne T. Lecuit Planar polarized actomyosin contractile flows control epithelial junction remodelling Nature 2010 468 1110 1114
96. M. Cavey M. Rauzi P. F. Lenne T. Lecuit A two-tiered mechanism for stabilization and immobilization of E-cadherin Nature 2008 453 751 756
97. K. Bambardekar R. Clement O. Blanc C. Chardes P. F. Lenne Direct laser manipulation reveals the mechanics of cell contacts in vivo Proc. Natl. Acad. Sci. U. S. A. 2015 112 1416 1421
98. Z. Liu J. L. Tan D. M. Cohen M. T. Yang N. J. Sniadecki S. A. Ruiz C. M. Nelson C. S. Chen Mechanical tugging force regulates the size of cell-cell junctions Proc. Natl. Acad. Sci. U. S. A. 2010 107 9944 9949
99. Q. Tseng E. Duchemin-Pelletier A. Deshiere M. Balland H. Guillou O. Filhol M. Thery Spatial organization of the extracellular matrix regulates cell-cell junction positioning Proc. Natl. Acad. Sci. U. S. A. 2012 109 1506 1511
100. V. Maruthamuthu B. Sabass U. S. Schwarz M. L. Gardel Cell-ECM traction force modulates endogenous tension at cell-cell contacts Proc. Natl. Acad. Sci. U. S. A. 2011 108 4708 4713
101. M. R. Ng A. Besser J. S. Brugge G. Danuser Mapping the dynamics of force transduction at cell-cell junctions of epithelial clusters eLife 2014 3 e03282
102. Y. S. Chu W. A. Thomas O. Eder F. Pincet E. Perez J. P. Thiery S. Dufour Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42 J. Cell Biol. 2004 167 1183 1194
103. D. T. Tambe C. C. Hardin T. E. Angelini K. Rajendran C. Y. Park X. Serra-Picamal E. H. Zhou M. H. Zaman J. P. Butler D. A. Weitz et al. Collective cell guidance by cooperative intercellular forces Nat. Mater. 2011 10 469 475
104. A. Saez E. Anon M. Ghibaudo O. du Roure J. M. Di Meglio P. Hersen P. Silberzan A. Buguin B. Ladoux Traction forces exerted by epithelial cell sheets J. Phys.: Condens. Matter 2010 22 194119
105. K. Doxzen S. R. Vedula M. C. Leong H. Hirata N. S. Gov A. J. Kabla B. Ladoux C. T. Lim Guidance of collective cell migration by substrate geometry Integr. Biol. 2013 5 1026 1035
106. S. R. K. Vedula G. Peyret I. Cheddadi T. Chen A. Brugues H. Hirata H. Lopez-Menendez Y. Toyama L. Neves de Almeida X. Trepat et al. Mechanics of epithelial closure over non-adherent environments Nat. Commun. 2015 6 6111
107. B. A. Truong Quang M. Mani O. Markova T. Lecuit P. F. Lenne Principles of E-cadherin supramolecular organization in vivo Curr. Biol. 2013 23 2197 2207
108. N. S. Gov Traction forces during collective cell motion HFSP J. 2009 3 223 227
109. S. F. Bensamoun L. Robert G. E. Leclerc L. Debernard F. Charleux Stiffness imaging of the kidney and adjacent abdominal tissues measured simultaneously using magnetic resonance elastography Clin. Imaging 2011 35 284 287