Tissue cohesion and the mechanics of cell rearrangement

Development (Cambridge)

Volumn 141, Issue 19, 2014, Pages 3672-3682

  David, Robert ^a   Luu, Olivia ^a   Damm, Erich W ^a   Wen, Jason W H ^a   Nagel, Martina ^a   Winklbauer, Rudolf ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cell adhesion; Cell rearrangement; Tissue surface tension; Tissue viscosity

Indexed keywords

CADHERIN; F ACTIN; FICOLL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL CONTACT; CELL FUNCTION; CELL MOTION; CELL REARRANGEMENT; CELL SEPARATION; CONTACT ANGLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONAL TISSUE; GASTRULA; NONHUMAN; SHEAR RATE; SURFACE TENSION; TISSUE VISCOSITY; VISCOSITY; XENOPUS LAEVIS; ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CONFOCAL MICROSCOPY; CYTOLOGY; EMBRYOLOGY; IMAGE PROCESSING; MORPHOGENESIS; PHYSIOLOGY; XENOPUS;

ANIMALS; CELL ADHESION; CELL MOVEMENT; EMBRYO, NONMAMMALIAN; FICOLL; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MORPHOGENESIS; SURFACE TENSION; VISCOSITY; XENOPUS;

EID: 84921758037     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.104315     Document Type: Article

References (49)

1. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
2. Bokoch, G. M. (2003). Biology of the p21-activated kinases. Ann. Rev. Biochem. 72, 743-781.
3. Brodland, G. W., Yang, J. and Sweny, J. (2009). Cellular interfacial and surface tensions determined from aggregate compression tests using a finite element model. HFSP J. 3, 273-281.
4. Clark, A. G., Dierkes, K. and Paluch, E. K. (2013). Monitoring actin cortex thickness in live cells. Biophys. J. 105, 570-580.
5. David, R., Ninomiya, H., Winklbauer, R. and Neumann, A. W. (2009). Tissue surface tension measurement by rigorous axisymmetric drop shape analysis. Colloid. Surf. B Biointerfaces 72, 236-240.
6. David, D. J. V., Tishkina, A. and Harris, T. J. C. (2010). The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137, 1645-1655.
7. 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.
8. Del Río, O.I. and Neumann, A. W. (1997). Axisymmetric Drop Shape Analysis: computational methods for the measurement of interfacial properties from the shape and dimensions of pendant and sessile drops. J. Colloid Interface Sci. 196, 136-147.
9. 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.
10. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
11. Gordon, R., Goel, N. S., Steinberg, M. S. and Wiseman, L. L. (1972). A rheological mechanism sufficient to explain the kinetics of cell sorting. J. Theor. Biol. 37, 43-73.
12. Guevorkian, K., Gonzalez-Rodriguez, D., Carlier, C., Dufour, S. and Brochard- Wyart, F. (2011). Mechanosensitive shivering of model tissues under controlled aspiration. Proc. Natl. Acad. Sci. USA 108, 13387-13392.
13. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
14. Heasman, J., Ginsberg, D., Geiger, B., Goldstone, K., Pratt, T., Yoshida-Noro, C. and Wylie, C. (1994). A functional test for maternally inherited cadherin in Xenopus shows its importance in cell adhesion at the blastula stage. Development 120, 49-57.
15. 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.
16. Keller, R., Shook, D. and Skoglund, P. (2008). The forces that shape embryos: physical aspects of convergent extension by cell intercalation. Phys. Biol. 5, 015007.
17. Kim, S. H., Yamamoto, A., Bouwmeester, T., Agius, E. and Robertis, E. M. (1998). The role of Paraxial Protocadherin in selective adhesion and cell movements of the mesoderm during Xenopus gastrulation. Development 125, 4681-4691.
18. 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.
19. Kurth, T., Berger, J., Wilsch-Bräuninger, M., Kretschmar, S., Cerny, R., Schwarz, H., Löfberg, J., Piendl, T. and Epperlein, H. H. (2010). Electron microscopy of the amphibian model systems Xenopus laevis and Ambystoma mexicanum. Methods Cell Biol. 96, 395-423.
20. 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.
21. Levental, I., Georges, P. C. and Janmey, P. A. (2007). Soft biological materials and their impact on cell function. Soft Matter 3, 299-306.
22. Li, J., Zhang, S., Soto, X., Woolner, S. and Amaya, E. (2013). ERK and phosphoinositide 3-kinase temporally coordinate different modes of actin-based motility during embryonic wound healing. J. Cell Sci. 126, 5005-5017.
23. Luu, O., David, R., Ninomiya, H. and Winklbauer, R. (2011). Large-scale mechanical properties of Xenopus embryonic epithelium. Proc. Natl. Acad. Sci. USA 108, 4000-4005.
24. 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.
25. 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.
26. Marmottant, P., Mgharbel, A., Käfer, J., Audren, B., Rieu, J.-P., Vial, J.-C., van der Sanden, B., Marée, A. F., Graner, F. and Delanoë-Ayari, H. (2009). The role of fluctuations and stress on the effective viscosity of cell aggregates. Proc. Natl. Acad. Sci. USA 106, 17271-17275.
27. Martin, A. C., Kaschube, M. and Wieschaus, E. F. (2009). Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457, 495-499.
28. Mombach, J. C. M., Robert, D., Graner, F., Gillet, G., Thomas, G. L., Idiart, M. and Rieu, J.-P. (2005). Rounding of aggregates of biological cells: experiments and simulations. Physica A 352, 525-534.
29. Moore, S. W., Keller, R. E. and Koehl, M. A. R. (1995). The dorsal involuting marginal zone stiffens anisotropically during its convergent extension in the gastrula of Xenopus laevis. Development 121, 3131-3140.
30. Ninomiya, H. and Winklbauer, R. (2008). Epithelial coating controls mesenchymal shape change through tissue-positioning effects and reduction of surfaceminimizing tension. Nat. Cell Biol. 10, 61-69.
31. Ninomiya, H., Elinson, R. P. and Winklbauer, R. (2004). Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 430, 364-367.
32. Ninomiya, H., David, R., Damm, E. W., Fagotto, F., Niessen, C. M. and Winklbauer, R. (2012). Cadherin-dependent differential cell adhesion in Xenopus causes cell sorting in vitro but not in the embryo. J. Cell Sci. 125, 1877-1883.
33. 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.
34. Rauzi, M., Lenne, P.-F. and Lecuit, T. (2010). Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114.
35. Rieu, J.-P. and Sawada, Y. (2002). Hydrodynamics and cell motion during the rounding of two dimensional hydra cell aggregates. Eur. Phys. J. B 27, 167-172.
36. 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.
37. Shindo, A. and Wallingford, J. B. (2014). PCP and septins Compartmentalize cortical actomyosin to direct collective cell movement. Science 343, 649-652.
38. Skoglund, P., Rolo, A., Chen, X., Gumbiner, B. M. and Keller, R. (2008). Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development 135, 2435-2444.
39. 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.
40. T. V. Stirbat, A. Mgharbel, S. Bodennec, K. Ferri, H. C. Mertani, J.-P. Rieu and H. Delanoë-Ayari (2013). Fine tuning of tissues’ viscosity and surface tension through contractility suggests a new role for α-catenin. PLoS ONE 8, e52554.
41. 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.
42. Valentine, M. T., Perlman, Z. E., Mitchison, T. J. and Weitz, D. A. (2005). Mechanical properties of Xenopus egg cytoplasmic extracts. Biophys. J. 88, 680-689.
43. von Dassow, M. and Davidson, L. A. (2007). Variation and robustness of the mechanics of gastrulation: the role of tissue mechanical properties during morphogenesis. Birth Defects Res. C81, 253-269.
44. von Dassow, M. and Davidson, L. A. (2009). Natural variation in embryo mechanics: gastrulation in Xenopus laevis is highly robust to variation in tissue stiffness. Dev. Dyn. 238, 2-18.
45. Weaire, D. and Rivier, N. (2009). Soaps, cells and statistics – random patterns in two dimensions. Contemp. Phys. 50, 199-239.
46. Winklbauer, R. (1990). Mesodermal cell migration during Xenopus gastrulation. Dev. Biol. 142, 155-168.
47. 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.
48. 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.
49. Zallen, J. A. and Wieschaus, E. (2004). Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 6, 343-355.