Cell adhesion strength from cortical tension - An integration of concepts

Journal of Cell Science

Volumn 128, Issue 20, 2015, Pages 3687-3693

  Winklbauer, Rudolf ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adhesion strength; Cell adhesion; Cortical tension; Tissue surface tension

Indexed keywords

CELL ADHESION MOLECULE;

ADHERENT CELL; ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL CONTACT; CELL ENERGY; CELL INTERACTION; CELL MOTION; CYTOKINESIS; CYTOSKELETON; HUMAN; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; SURFACE TENSION; TENSION; ANIMAL; CHEMISTRY; METABOLISM;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; HUMANS; SURFACE TENSION;

EID: 84946038955     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.174623     Document Type: Article

References (63)

1. Al-Amoudi, A., Díez, D. C., Betts, M. J. and Frangakis, A. S. (2007). The molecular architecture of cadherins in native epidermal desmosomes. Nature 450, 832-837.
2. Amack, J. D. and Manning, L. M. (2012). Knowing the boundaries: extending the differential adhesion hypothesis in embryonic cell sorting. Science 338, 212-215.
3. Bajpai, S., Correia, J., Feng, Y., Figueiredo, J., Sun, S. X., Longmore, G. D., Suriano, G. and Wirtz, D. (2008). a-catenin mediates initial E-cadherindependent cell-cell recognition and subsequent bond strengthening. Proc. Natl. Acad. Sci. USA 105, 18331-18336.
4. Bell, G. I. (1978). Models for the specific adhesion of cells to cells. Science 200, 618-627.
5. Bergert, M., Chandradoss, S. D., Desai, R. A. and Paluch, E. (2012). Cell mechanics control rapid transitions between blebs and lamellipodia during migration. Proc. Natl. Acad. Sci. USA 109, 14434-14439.
6. Brodland, W. G. and Chen, H. H. (2000). The mechanics of cell sorting and envelopment. J. Biomech. 33, 845-851.
7. Bucior, I. and Burger, M. M. (2004). Carbohydrate-carbohydrate interactions in cell recognition. Curr. Opin. Struct. Biol. 14, 631-637.
8. Cavey, M., Rauzi, M., Lenne, P.-F. and Lecuit, T. (2008). A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 453, 751-756.
9. Chaigne, A., Campillo, C., Gov, N. S., Voituriez, R., Azoury, J., Umaña-Diaz, C., Almonacid, M., Queguiner, I., Nassoy, P., Sykes, C. et al. (2013). A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat. Cell Biol. 15, 958-966.
10. Chu, Y.-S., Thomas, W. A., Eder, O., Pincet, F., Perez, E., Thiery, J. P. and Dufour, S. (2004). Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J. Cell Biol. 167, 1183-1194.
11. Clark, A. G., Wartlick, O., Salbreux, G. and Paluch, E. K. (2014). Stresses at the cell surface during animal cell morphogenesis. Curr. Biol. 24, R484-R494.
12. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
13. David, R., Ninomiya, H., Winklbauer, R. and Neumann, A. W. (2009). Tissue surface tension measurement by rigorous axisymmetric drop shape analysis. Colloids Surf. B Biointerfaces 72, 236-240.
14. David, R., Luu, O., Damm, E. W., Wen, J. W. H., Nagel, M. and Winklbauer, R. (2014). Tissue cohesion and the mechanics of cell rearrangement. Development 141, 3672-3682.
15. Davis, G. S., Phillips, H. M. and Steinberg, M. S. (1997). Germ-layer surface tensions and "tissue affinities" in Rana pipiens gastrulae: quantitative measurements. Dev. Biol. 192, 630-644.
16. Décavé, E., Garrivier, D., Bréchet, Y., Bruckert, F. and Fourcade, B. (2002). Peeling process in living cell movement under shear flow. Phys. Rev. Lett. 89, 108101.
17. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). Alphacatenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123, 903-915.
18. Eghiaian, F., Rigato, A. and Scheuring, S. (2015). Structural, mechanical, and dynamical variability of the actin cortex in living cells. Biophys. J. 108, 1330-1340.
19. Evans, E. and Yeung, A. (1989). Apparent viscosity and cortical tension of blood granulocytes determined by micropipet aspiration. Biophys. J. 56, 151-160.
20. Fagotto, F. (2014). The cellular basis of tissue separation. Development 141, 3303-3318.
21. Forgacs, G., Foty, R. A., Shafrir, Y. and Steinberg, M. S. (1998). Viscoelastic properties of living embryonic tissues: a quantitative study. Biophys. J. 74, 2227-2234.
22. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
23. Foty, R. A., Pfleger, C. M., Forgacs, G. and Steinberg, M. S. (1996). Surface tensions of embryonic tissues predict their mutual envelopment behavior. Development 122, 1611-1620.
24. Fukui, Y. (1993). Toward a new concept of cell motility: cytoskeletal dynamics in amoeboid movement and cell division. Int. Rev. Cytol. 144, 85-127.
25. Garcia-Manyes, S., Bucior, I., Ros, R., Anselmetti, D., Sanz, F., Burger, M. M. and Fernandez-Busquets, X. (2006). Proteoglycan mechanics studied by single-molecule force spectroscopy of allotypic cell adhesion glycans. J. Biol. Chem. 281, 5992-5999.
26. Gonzalez-Rodriguez, D., Bonnemay, L., Elgeti, J., Dufour, S., Cuvelier, D. and Brochard-Wyart, F. (2013). Detachment and fracture of cellular aggregates. Soft Matter 9, 2282-2290.
27. Graner, F. (1993). Can surface adhesion drive cell-rearrangement? Part I: Biological cell-sorting. J. Theor. Biol. 164, 445-476.
28. Griffin, M. A., Engler, A. J., Barber, T. A., Healy, K. E., Sweeney, H. L. and Discher, D. E. (2004). Patterning, prestress, and peeling dynamics of myocytes. Biophys. J. 86, 1209-1222.
29. Harris, A. K. (1976). Is cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J. Theor. Biol. 61, 267-285.
30. Hegedüs, B., Marga, F., Jakab, K., Sharpe-Timms, K. L. and Forgacs, G. (2006). The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors. Biophys. J. 91, 2708-2716.
31. Hidalgo-Carcedo, C., Hooper, S., Chaudhry, S. I., Williamson, P., Harrington, K., Leitinger, B. and Sahai, E. (2011). Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 13, 49-58.
32. Hosu, B. G., Sun, M., Marga, F., Grandbois, M. and Forgacs, G. (2007). Eukaryotic membrane tethers revisited using magnetic tweezers. Phys. Biol. 4, 67-78.
33. Kashef, J. and Franz, C. M. (2015). Quantitative methods for analyzing cell-cell adhesion in development. Dev. Biol. 401, 165-174.
34. Krieg, M., Arboleda-Estudillo, Y., Puech, P.-H., Käfer, J., Graner, F., Müller, D. J. and Heisenberg, C.-P. (2008). Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10, 429-436.
35. Lam, J., Herant, M., Dembo, M. and Heinrich, V. (2009). Baseline mechanical characterization of J774 macrophages. Biophys. J. 96, 248-254.
36. Leckband, D. and Prakasam, A. (2006). Mechanism and dynamics of cadherin adhesion. Annu. Rev. Biomed. Eng. 8, 259-287.
37. Lecuit, T. and Lenne, P.-F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644.
38. Lecuit, T. and Yap, A. S. (2015). E-cadherin junctions as active mechanical integrators in tissue dynamics. Nat. Cell Biol. 17, 533-539.
39. Lomakina, E. B., Spillmann, C. M., King, M. R. and Waugh, R. E. (2004). Rheological analysis and measurement of neutrophil indentation. Biophys. J. 87, 4246-4258.
40. Maître, J.-L. and Heisenberg, C.-P. (2013). Three functions of cadherins in cell adhesion. Curr. Biol. 23, R626-R633.
41. Maître, J.-L., Berthoumieux, H., Krens, S. F. G., Salbreux, G., Jülicher, F., Paluch, E. and Heisenberg, C.-P. (2012). Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 338, 253-256.
42. Manning, M. L., Foty, R. A., Steinberg, M. S. and Schoetz, E.-M. (2010). Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl. Acad. Sci. USA 107, 12517-12522.
43. Marmottant, P., Mgharbel, A., Käfer, J., Audren, B., Rieu, J.-P., Vial, J.-C., van der Sanden, B., Maree, A. F.M., Graner, F. and Delanoe-Ayari, H. (2009). The role of fluctuations and stress on the effective viscosity of cell aggregates. Proc. Natl. Acad. Sci. USA 106, 17271-17275.
44. Murai, K. K. and Pasquale, E. B. (2003). 'Eph'ective signaling: forward, reverse and crosstalk. J. Cell Sci. 116, 2823-2832.
45. Nelson, W. J. (2008). Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36, 149-155.
46. Pasternak, C., Spudich, J. A. and Elson, E. L. (1989). Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341, 549-551.
47. Pierres, A., Prakasam, A., Touchard, D., Benoliel, A.-M., Bongrand, P. and Leckband, D. (2007). Dissecting subsecond cadherin bound states reveals an efficient way for cells to achieve ultrafast probing of their environment. FEBS Lett. 581, 1841-1846.
48. Priya, R. and Yap, A. S. (2015). Active tension: the role of cadherin adhesion and signaling in generating junctional contractility. Curr. Top. Dev. Biol. 112, 65-102.
49. Reffay, M., Parrini, M. C., Cochet-Escartin, O., Ladoux, B., Buguin, A., Coscoy, S., Amblard, F., Camonis, J. and Silberzan, P. (2014). Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat. Cell Biol. 16, 217-223.
50. Salbreux, G., Charras, G. and Paluch, E. (2012). Actin cortex mechanics and cellular morphogenesis. Trends Cell Biol. 22, 536-545.
51. Schötz, E.-M., Burdine, R. D., Jülicher, F., Steinberg, M. S., Heisenberg, C.-P. and Foty, R. A. (2008). Quantitative differences in tissue surface tension influence zebrafish germ layer positioning. HFSP J. 2, 42-56.
52. Sens, P. and Turner, M. S. (2006). Budded membrane microdomains as tension regulators. Phys. Rev. E 73, 031918.
53. Sivasankar, S., Brieher, W., Lavrik, N., Gumbiner, B. and Leckband, D. (1999). Direct molecular force measurements of multiple adhesive interactions between cadherin ectodomains. Proc. Natl. Acad. Sci. USA 96, 11820-11824.
54. Steinberg, M. S. (1963). Reconstruction of tissues by dissociated cells. Science 141, 401-408.
55. Steinberg, M. S. (1978). Specific cell ligands and the differential adhesion hypothesis: How do they fit together?. In Specificity of Embryological Interactions (Receptors and Recognition, Series B, Vol.4, pp. 97-130) (ed. D. R. Garrod). London: Chapman & Hall.
56. Stewart, M. P., Helenius, J., Toyoda, Y., Ramanathan, S. P., Muller, D. J. and Hyman, A. A. (2011). Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469, 226-230.
57. Stirbat, T. V., Mgharbel, A., Bodennec, S., Ferri, K., Mertani, H. C., Rieu, J.-P. and Delanoe-Ayari, H. (2013). Fine tuning of tissues' viscosity and surface tension through contractility suggests a new role for a-catenin. PLoS ONE 8, e52554.
58. Tabdanov, E., Borghi, N., Brochard-Wyart, F., Dufour, S. and Thiery, J.-P. (2009). Role of E-cadherin in membrane-cortex interaction probed by nanotube extrusion. Biophys. J. 96, 2457-2465.
59. Tinevez, J.-Y., Schulze, U., Salbreux, G., Roensch, J., Joanny, J.-F. and Paluch, E. (2009). Role of cortical tension in bleb growth. Proc. Natl. Acad. Sci. USA 106, 18581-18586.
60. Toret, C. P., Collins, C. and Nelson, W. J. (2014). An Elmo-Dock complex locally controls Rho GTPases and actin remodeling during cadherin-mediated adhesion. J. Cell Biol. 207, 577-587.
61. Yamada, S. and Nelson, W. J. (2007). Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell cell adhesion. J. Cell Biol. 178, 517-527.
62. Youssef, J., Nurse, A. K., Freund, L. B. and Morgan, J. R. (2011). Quantification of the forces driving self-assembly of three-dimensional microtissues. Proc. Natl. Acad. Sci. USA 108, 6993-6998.
63. Zaidel-Bar, R. (2013). Cadherin adhesome at a glance. J. Cell Sci. 126, 373-378.