The cellular basis of tissue separation

Development (Cambridge)

Volumn 141, Issue 17, 2014, Pages 3303-3318

  Fagotto, François ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cell cell adhesion; Differential adhesion hypothesis; Embryonic boundaries; Ephrin Eph signaling; Morphogenesis

Indexed keywords

EPHRIN; EPHRIN RECEPTOR;

CELL ADHESION; CELL AGGREGATION; CELL CONTACT; CELL POPULATION; CELL SELECTION; CELL SURFACE; EMBRYO DEVELOPMENT; MOLECULE; MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEPARATION TECHNIQUE; TISSUES;

CELL-CELL ADHESION; DIFFERENTIAL ADHESION HYPOTHESIS; EMBRYONIC BOUNDARIES; EPHRIN/EPH SIGNALING; MORPHOGENESIS;

ANIMALS; BIOPHYSICAL PHENOMENA; BODY PATTERNING; CELL ADHESION; CELL COMMUNICATION; CELLS; HUMANS; MORPHOGENESIS;

EID: 84906236649     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.090332     Document Type: Review

References (128)

1. Aliee, M., Röper, J.-C., Landsberg, K. P., Pentzold, C., Widmann, T. J., Jülicher, F. and Dahmann, C. (2012). Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr. Biol. 22, 967-976.
2. Altabef, M., Clarke, J. D. and Tickle, C. (1997). Dorso-ventral ectodermal compartments and origin of apical ectodermal ridge in developing chick limb. Development 124, 4547-4556.
3. Amack, J. D. and Manning, M. L. (2012). Knowing the boundaries: extending the differential adhesion hypothesis in embryonic cell sorting. Science 338, 212-215.
4. Baker, C. V. and Bronner-Fraser, M. (2001). Vertebrate cranial placodes I. Embryonic induction. Dev. Biol. 232, 1-61.
5. Barrios, A., Poole, R. J., Durbin, L., Brennan, C., Holder, N. and Wilson, S. W. (2003). Eph/Ephrin signaling regulates the mesenchymal-to-epithelial transition of the paraxial mesoderm during somite morphogenesis. Curr. Biol. 13, 1571-1582.
6. Batlle, E. and Wilkinson, D. G. (2012). Molecular mechanisms of cell segregation and boundary formation in development and tumorigenesis. Cold Spring Harb. Perspect. Biol. 4, a008227.
7. Baum, B. and Georgiou, M. (2011). Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 192, 907-917.
8. Brieher, W. M. and Yap, A. S. (2013). Cadherin junctions and their cytoskeleton(s). Curr. Opin. Cell Biol. 25, 39-46.
9. Brodland, G. W. (2002). The Differential Interfacial Tension Hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues. J. Biomech. Eng. 124, 188-197.
10. Calzolari, S., Terriente, J. and Pujades, C. (2014). Cell segregation in the vertebrate hindbrain relies on actomyosin cables located at the interhombomeric boundaries. EMBO J. 33, 686-701.
11. Carmona-Fontaine, C., Matthews, H. K., Kuriyama, S., Moreno, M., Dunn, G. A., Parsons, M., Stern, C. D. and Mayor, R. (2008). Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 456, 957-961.
12. Cavey, M. and Lecuit, T. (2009). Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb. Perspect. Biol. 1, a002998.
13. Chang, L.-H., Chen, P., Lien, M.-T., Ho, Y.-H., Lin, C.-M., Pan, Y.-T., Wei, S.-Y. and Hsu, J.-C. (2011). Differential adhesion and actomyosin cable collaborate to drive Echinoid-mediated cell sorting. Development 138, 3803-3812.
14. Chen, X. and Gumbiner, B. M. (2006). Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J. Cell Biol. 174, 301-313.
15. Chen, X., Koh, E., Yoder, M. and Gumbiner, B. M. (2009). A protocadherincadherin-FLRT3 complex controls cell adhesion and morphogenesis. PLoS ONE 4, e8411.
16. Cooke, J. E. and Moens, C. B. (2002). Boundary formation in the hindbrain: Eph only it were simple. Trends Neurosci. 25, 260-267.
17. Cooke, J. E., Kemp, H. A. and Moens, C. B. (2005). EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish. Curr. Biol. 15, 536-542.
18. Dahmann, C. and Basler, K. (1999). Compartment boundaries: at the edge of development. Trends Genet. 15, 320-326.
19. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
20. Domingo, C. and Keller, R. (2000). Cells remain competent to respond to mesoderm-inducing signals present during gastrulation in Xenopus laevis. Dev. Biol. 225, 226-240.
21. Duguay, D., Foty, R. A. and Steinberg, M. S. (2003). Cadherin-mediated cell adhesion and tissue segregation: qualitative and quantitative determinants. Dev. Biol. 253, 309-323.
22. Durbin, L., Brennan, C., Shiomi, K., Cooke, J., Barrios, A., Shanmugalingam, S., Guthrie, B., Lindberg, R. and Holder, N. (1998). Eph signaling is required for segmentation and differentiation of the somites. Genes Dev. 12, 3096-3109.
23. Edelman, G. M. (1986). Cell adhesion molecules in the regulation of animal form and tissue pattern. Annu. Rev. Cell Biol. 2, 81-116.
24. Fagotto, F., Rohani, N., Touret, A.-S. and Li, R. (2013). A molecular base for cell sorting at embryonic boundaries: contact inhibition of cadherin adhesion by ephrin/Eph-dependent contractility. Dev. Cell 27, 72-87.
25. Fausto-Sterling, A. and Hsieh, L. (1987). In vitro culture of Drosophila imaginal disc cells: aggregation, sorting out, and differentiative abilities. Dev. Biol. 120, 284-293.
26. Foty, R. A. and Steinberg, M. S. (2004). Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 48, 397-409.
27. Foty, R. A. and Steinberg, M. S. (2005). The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278, 255-263.
28. Fraser, S., Keynes, R. and Lumsden, A. (1990). Segmentation in the chick embryo hindbrain is defined by cell lineage restrictions. Nature 344, 431-435.
29. Garcia-Bellido, A., Ripoll, P. and Morata, G. (1973). Developmental compartmentalisation of the wing disk of Drosophila. Nature 245, 251-253.
30. Godt, D. and Tepass, U. (1998). Drosophila oocyte localization is mediated by differential cadherin-based adhesion. Nature 395, 387-391.
31. Goguen, B. N., Hoffman, B. D., Sellers, J. R., Schwartz, M. A. and Imperiali, B. (2011). Light-triggered myosin activation for probing dynamic cellular processes. Angew. Chemie 50, 5667-5670.
32. Gumbiner, B. M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
33. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
34. Gumbiner, B. M. and McCrea, P. D. (1993). Catenins as mediators of the cytoplasmic functions of cadherins. J. Cell Sci. 1993 Suppl. 17, 155-158.
35. Halbleib, J. M. and Nelson, W. J. (2006). Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199-3214.
36. 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.
37. Herszterg, S., Leibfried, A., Bosveld, F., Martin, C. and Bellaiche, Y. (2013). Interplay between the dividing cell and its neighbors regulates adherens junction formation during cytokinesis in epithelial tissue. Dev. Cell 24, 256-270.
38. Holtfreter, J. (1939). Gewebsaffinität, ein Mittel der embryonalen Formbildung. Arch. Exp. Zellforsch. Gewebeszücht 23, 169-209.
39. Inoue, T., Tanaka, T., Takeichi, M., Chisaka, O., Nakamura, S. and Noriko, O. (2001). Role of cadherins in maintaining the compartment boundary between the cortex and striatum during development. Development 128, 561-569.
40. Inuzuka, H., Miyatani, S. and Takeichi, M. (1991). R-cadherin: a novel Ca(2+)-dependent cell-cell adhesion molecule expressed in the retina. Neuron 7, 69-79.
41. Karaulanov, E., Böttcher, R. T., Stannek, P., Wu, W., Rau, M., Ogata, S., Cho, K. W. Y. and Niehrs, C. (2009). Unc5B interacts with FLRT3 and Rnd1 to modulate cell adhesion in Xenopus embryos. PLoS ONE 4, e5742.
42. Katsamba, P., Carroll, K., Ahlsen, G., Bahna, F., Vendome, J., Posy, S., Rajebhosale, M., Price, S., Jessell, T. M., Ben-Shaul, A. et al. (2009). Linking molecular affinity and cellular specificity in cadherin-mediated adhesion. Proc. Natl. Acad. Sci. USA 106, 11594-11599.
43. Keller, R., Cooper, M. S., Danilchik, M., Tibbetts, P. and Wilson, P. (1989). Cell intercalation during notochord development in Xenopus laevis. J. Exp. Zool. 251, 134-154.
44. Keller, R., Davidson, L., Edlund, A., Elul, T., Ezin, M., Shook, D. and Skoglund, P. (2000). Mechanisms of convergence and extension by cell intercalation. Phil. Trans. R. Soc. Lond. B Biol. Sci. 355, 897-922.
45. Kemler, R. (1993). From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9, 317-321.
46. Kemp, H. A., Cooke, J. E. and Moens, C. B. (2009). EphA4 and EfnB2a maintain rhombomere coherence by independently regulating intercalation of progenitor cells in the zebrafish neural keel. Dev. Biol. 327, 313-326.
47. 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, 4681-4690.
48. Kim, S.-H., Jen, W.-C., De Robertis, E. M. and Kintner, C. (2000). The protocadherin PAPC establishes segmental boundaries during somitogenesis in Xenopus embryos. Curr. Biol. 10, 821-830.
49. Kraft, B., Berger, C. D., Wallkamm, V., Steinbeisser, H. and Wedlich, D. (2012). Wnt-11 and Fz7 reduce cell adhesion in convergent extension by sequestration of PAPC and C-cadherin. J. Cell Biol. 198, 695-709.
50. Krens, S. F. G., Mollmert, S. and Heisenberg, C.-P. (2011). Enveloping cell-layer differentiation at the surface of zebrafish germ-layer tissue explants. Proc. Natl. Acad. Sci. USA 108, E9-E10.
51. 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.
52. Ladoux, B., Anon, E., Lambert, M., Rabodzey, A., Hersen, P., Buguin, A., Silberzan, P. and Mege, R. M. (2010). Strength dependence of cadherinmediated adhesions. Biophys. J. 98, 534-542.
53. Landsberg, K. P., Farhadifar, R., Ranft, J., Umetsu, D., Widmann, T. J., Bittig, T., Said, A., Jülicher, F. and Dahmann, C. (2009). Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 19, 1950-1955.
54. Laplante, C. and Nilson, L. A. (2006). Differential expression of the adhesion molecule Echinoid drives epithelial morphogenesis in Drosophila. Development 133, 3255-3264.
55. Laplante, C. and Nilson, L. A. (2011). Asymmetric distribution of Echinoid defines the epidermal leading edge during Drosophila dorsal closure. J. Cell Biol. 192, 335-348.
56. Lawrence, P. A. and Green, S. M. (1975). The anatomy of a compartment border. The intersegmental boundary in Oncopeltus. J. Cell Biol. 65, 373-382.
57. le Duc, Q., Shi, Q., Blonk, I., Sonnenberg, A., Wang, N., Leckband, D. and de Rooij, J. (2010). Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin IIdependent manner. J. Cell Biol. 189, 1107-1115.
58. 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.
59. Lin, H.-P., Chen, H.-M., Wei, S.-Y., Chen, L.-Y., Chang, L.-H., Sun, Y.-J., Huang, S.-Y. and Hsu, J.-C. (2007). Cell adhesion molecule Echinoid associates with unconventional myosin VI/Jaguar motor to regulate cell morphology during dorsal closure in Drosophila. Dev. Biol. 311, 423-433.
60. Lisabeth, E. M., Falivelli, G. and Pasquale, E. B. (2013). Eph receptor signaling and ephrins. Cold Spring Harb. Perspect. Biol. 5, a009159.
61. 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.
62. Maghzal, N., Vogt, E., Reintsch, W., Fraser, J. S. and Fagotto, F. (2010). The tumor-associated EpCAM regulates morphogenetic movements through intracellular signaling. J. Cell Biol. 191, 645-659.
63. Maghzal, N., Kayali, H. A., Rohani, N., Kajava, A. V. and Fagotto, F. (2013). EpCAM controls actomyosin contractility and cell adhesion by direct inhibition of PKC. Dev. Cell 27, 263-277.
64. Maitre, J.-L., Berthoumieux, H., Krens, S. F. G., Salbreux, G., Julicher, 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.
65. Major, R. J. and Irvine, K. D. (2006). Localization and requirement for Myosin II at the dorsal-ventral compartment boundary of the Drosophila wing. Dev. Dyn. 235, 3051-3058.
66. 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.
67. Martinez-Arias, A. and Lawrence, P. A. (1985). Parasegments and compartments in the Drosophila embryo. Nature 313, 639-642.
68. Matsuzaki, F., Mége, R. M., Jaffe, S. H., Friedlander, D. R., Gallin, W. J., Goldberg, J. I., Cunningham, B. A. and Edelman, G. M. (1990). cDNAs of cell adhesion molecules of different specificity induce changes in cell shape and border formation in cultured S180 cells. J. Cell Biol. 110, 1239-1252.
69. McKeown, S. J., Wallace, A. S. and Anderson, R. B. (2013). Expression and function of cell adhesion molecules during neural crest migration. Dev. Biol. 373, 244-257.
70. Medina, A., Swain, R. K., Kuerner, K.-M. and Steinbeisser, H. (2004). Xenopus paraxial protocadherin has signaling functions and is involved in tissue separation. EMBO J. 23, 3249-3258.
71. Mellitzer, G., Xu, Q. and Wilkinson, D. (1999). Eph receptors and ephrins restrict cell intermingling and communication. Nature 400, 77-81.
72. Monier, B., Pélissier-Monier, A., Brand, A. H. and Sanson, B. (2010). An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nat. Cell Biol. 12, 60-65.
73. Morckel, A. R., Lusic, H., Farzana, L., Yoder, J. A., Deiters, A. and Nascone-Yoder, N. M. (2012). A photoactivatable small-molecule inhibitor for lightcontrolled spatiotemporal regulation of Rho kinase in live embryos. Development 139, 437-442.
74. Moscona, A. and Moscona, H. (1952). The dissociation and aggregation of cells from organ rudiments of the early chick embryo. J. Anat. 86, 287-301.
75. Murai, K. K. and Pasquale, E. B. (2003). 'Eph'ective signaling: forward, reverse and crosstalk. J. Cell Sci. 116, 2823-2832.
76. Nagafuchi, A., Ishihara, S. and Tsukita, S. (1994). The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-alpha catenin fusion molecules. J. Cell Biol. 127, 235-245.
77. Niessen, C. M. and Gumbiner, B. M. (2002). Cadherin-mediated cell sorting not determined by binding or adhesion specificity. J. Cell Biol. 156, 389-400.
78. 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.
79. Nose, A., Nagafuchi, A. and Takeichi, M. (1988). Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993-1001.
80. Oates, A. C., Lackmann, M., Power, M.-A., Brennan, C., Down, L. M., Do, C., Evans, B., Holder, N. and Boyd, A. W. (1999). An early developmental role for eph-ephrin interaction during vertebrate gastrulation. Mech. Dev. 83, 77-94.
81. Oda, H. and Takeichi, M. (2011). Evolution: structural and functional diversity of cadherin at the adherens junction. J. Cell Biol. 193, 1137-1146.
82. Oliveri, P., Tu, Q. and Davidson, E. H. (2008). Global regulatory logic for specification of an embryonic cell lineage. Proc. Natl. Acad. Sci. USA 105, 5955-5962.
83. Ounkomol, C., Yamada, S. and Heinrich, V. (2010). Single-cell adhesion tests against functionalized microspheres arrayed on AFM cantilevers confirm heterophilic E-and N-cadherin binding. Biophys. J. 99, L100-L102.
84. Park, E. C., Cho, G.-S., Kim, G.-H., Choi, S.-C. and Han, J.-K. (2011). The involvement of Eph-Ephrin signaling in tissue separation and convergence during Xenopus gastrulation movements. Dev. Biol. 350, 441-450.
85. Pasquale, E. B. (2010). Eph receptors and ephrins in cancer: bidirectional signalling and beyond. Nat. Rev. Cancer 10, 165-180.
86. Patel, S. D., Ciatto, C., Chen, C. P., Bahna, F., Rajebhosale, M., Arkus, N., Schieren, I., Jessell, T. M., Honig, B., Price, S. R. et al. (2006). Type II cadherin ectodomain structures: implications for classical cadherin specificity. Cell 124, 1255-1268.
87. Prakasam, A. K., Maruthamuthu, V. and Leckband, D. E. (2006). Similarities between heterophilic and homophilic cadherin adhesion. Proc. Natl. Acad. Sci. USA 103, 15434-15439.
88. Price, S. R., De Marco Garcia, N. V., Ranscht, B. and Jessell, T. M. (2002). Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109, 205-216.
89. Ratheesh, A. and Yap, A. S. (2012). A bigger picture: classical cadherins and the dynamic actin cytoskeleton. Nat. Rev. Mol. Cell Biol. 13, 673-679.
90. Ratheesh, A., Gomez, G. A., Priya, R., Verma, S., Kovacs, E. M., Jiang, K., Brown, N. H., Akhmanova, A., Stehbens, S. J. and Yap, A. S. (2012). Centralspindlin and alpha-catenin regulate Rho signalling at the epithelial zonula adherens. Nat. Cell Biol. 14, 818-828.
91. Reintsch, W. E., Habring-Mueller, A., Wang, R. W., Schohl, A. and Fagotto, F. (2005). beta-Catenin controls cell sorting at the notochord-somite boundary independently of cadherin-mediated adhesion. J. Cell Biol. 170, 675-686.
92. Rhee, J., Takahashi, Y. U., Saga, Y., Wilson-Rawls, J. and Rawls, A. (2003). The protocadherin PAPC is involved in the organization of the epithelium along the segmental border during mouse somitogenesis. Dev. Biol. 254, 248-261.
93. Rohani, N., Canty, L., Luu, O., Fagotto, F. and Winklbauer, R. (2011). EphrinB/ EphB signaling controls embryonic germ layer separation by contact-induced cell detachment. PLoS Biol. 9, e1000597.
94. Roux, W. (1905). Die Entwicklungsmechanik, ein neuer Zweig der biologischen Wissenschaft. In Vorträge und Aufsätze zur Entwicklungsmechanik der Organismen. Wilhelm Engelmann: Leipzig.
95. San Roman, A. K. and Shivdasani, R. A. (2011). Boundaries, junctions and transitions in the gastrointestinal tract. Exp. Cell Res. 317, 2711-2718.
96. Sanson, B. (2001). Generating patterns from fields of cells. Examples from Drosophila segmentation. EMBO Rep. 2, 1083-1088.
97. Sela-Donenfeld, D. and Wilkinson, D. G. (2005). Eph receptors: two ways to sharpen boundaries. Curr. Biol. 15, R210-R212.
98. Shan, W.-S., Tanaka, H., Phillips, G. R., Arndt, K., Yoshida, M., Colman, D. R. and Shapiro, L. (2000). Functional cis-heterodimers of N-and R-cadherins. J. Cell Biol. 148, 579-590.
99. Shi, Q., Chien, Y.-H. and Leckband, D. (2008). Biophysical properties of cadherin bonds do not predict cell sorting. J. Biol. Chem. 283, 28454-28463.
100. Shih, J. and Keller, R. (1992a). Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116, 901-914.
101. Shih, J. and Keller, R. (1992b). Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. Development 116, 915-930.
102. Shimoyama, Y., Tsujimoto, G., Kitajima, M. and Natori, M. (2000). Identification of three human type-II classic cadherins and frequent heterophilic interactions between different subclasses of type-II classic cadherins. Biochem. J. 349, 159-167.
103. Steinberg, M. S. (1970). Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence of a hierarchy among populations of embryonic cells. J. Exp. Zool. 173, 395-433.
104. Steinberg, M. S. and Takeichi, M. (1994). Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proc. Natl. Acad. Sci. USA 91, 206-209.
105. Straub, B. K., Rickelt, S., Zimbelmann, R., Grund, C., Kuhn, C., Iken, M., Ott, M., Schirmacher, P. and Franke, W. W. (2011). E-N-cadherin heterodimers define novel adherens junctions connecting endoderm-derived cells. J. Cell Biol. 195, 873-887.
106. Takeichi, M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
107. Tepass, U., Godt, D. and Winklbauer, R. (2002). Cell sorting in animal development: signalling and adhesive mechanisms in the formation of tissue boundaries. Curr. Opin. Genet. Dev. 12, 572-582.
108. Theveneau, E. and Mayor, R. (2012). Cadherins in collective cell migration of mesenchymal cells. Curr. Opin. Cell Biol. 24, 677-684.
109. Townes, P. L. and Holtfreter, J. (1955). Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128, 53-120.
110. Ulrich, F., Krieg, M., Schötz, E.-M., Link, V., Castanon, I., Schnabel, V., Taubenberger, A., Mueller, D., Puech, P.-H. and Heisenberg, C.-P. (2005). Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9, 555-564.
111. Vegh, M. and Basler, K. (2003). A genetic screen for hedgehog targets involved in the maintenance of the Drosophila anteroposterior compartment boundary. Genetics 163, 1427-1438.
112. Voss-Böhme, A. and Deutsch, A. (2010). The cellular basis of cell sorting kinetics. J. Theor. Biol. 263, 419-436.
113. Wacker, S., Grimm, K., Joos, T. and Winklbauer, R. (2000). Development and control of tissue separation at gastrulation in Xenopus. Dev. Biol. 224, 428-439.
114. Watanabe, T. and Takahashi, Y. (2010). Tissue morphogenesis coupled with cell shape changes. Curr. Opin. Genet. Dev. 20, 443-447.
115. Watanabe, T., Sato, Y., Saito, D., Tadokoro, R. and Takahashi, Y. (2009). EphrinB2 coordinates the formation of a morphological boundary and cell epithelialization during somite segmentation. Proc. Natl. Acad. Sci. USA 106, 7467-7472.
116. Wilson, H. V. (1907). On some phenomena of coalescence and regeneration in sponges. J. Exp. Zool. 5, 245-258.
117. Wilson, P. and Keller, R. (1991). Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. Development 112, 289-300.
118. Winklbauer, R. (2009). Cell adhesion in amphibian gastrulation. Int. Rev. Cell Mol. Biol. 278, 215-275.
119. Wu, Y. I., Frey, D., Lungu, O. I., Jaehrig, A., Schlichting, I., Kuhlman, B. and Hahn, K. M. (2009). A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461, 104-108.
120. Xu, Q. and Wilkinson, D. G. (2013). Boundary formation in the development of the vertebrate hindbrain. Dev. Biol. 2, 735-745.
121. Xu, Q., Alldus, G., Holder, N. andWilkinson, D. G. (1995). Expression of truncated Sek-1 receptor tyrosine kinase disrupts the segmental restriction of gene expression in the Xenopus and zebrafish hindbrain. Development 121, 4005-4016.
122. Xu, Q., Mellitzer, G., Robinson, V. andWilkinson, D. G. (1999). In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399, 267-271.
123. 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.
124. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005). Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901.
125. Yamagishi, S., Hampel, F., Hata, K., Del Toro, D., Schwark, M., Kvachnina, E., Bastmeyer, M., Yamashita, T., Tarabykin, V., Klein, R. et al. (2011). FLRT2 and FLRT3 act as repulsive guidance cues for Unc5-positive neurons. EMBO J. 30, 2920-2933.
126. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A. and Shibata, M. (2010). alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542.
127. Zecca, M. and Struhl, G. (2002). Subdivision of the Drosophila wing imaginal disc by EGFR-mediated signaling. Development 129, 1357-1368.
128. Zervas, M., Millet, S., Ahn, S. and Joyner, A. L. (2004). Cell behaviors and genetic lineages of the mesencephalon and rhombomere 1. Neuron 43, 345-357.