A Molecular Base for Cell Sorting at Embryonic Boundaries: Contact Inhibition of Cadherin Adhesion by Ephrin/Eph-Dependent Contractility

Developmental Cell

Volumn 27, Issue 1, 2013, Pages 72-87

  Fagotto, François ^a   Rohani, Nazanin ^a   Touret, Anne Sophie ^a   Li, Rui ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; EPHRIN; EPHRIN RECEPTOR; MYOSIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL MEMBRANE; CELL SELECTION; CONTACT INHIBITION; HUMAN; MESODERM; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; PROTEIN EXPRESSION; VERTEBRATE;

ANIMALS; CADHERINS; CELL ADHESION; CELL MEMBRANE; EMBRYONIC INDUCTION; EPHRINS; MESODERM; MYOSINS; NOTOCHORD; RECEPTORS, EPH FAMILY; XENOPUS;

VERTEBRATA;

EID: 84885386354     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.09.004     Document Type: Article

References (42)

1. Adams C.L., Chen Y.T., Smith S.J., Nelson W.J. Mechanisms ofepithelial cell-cell adhesion and cell compaction revealed by high-resolutiontracking of E-cadherin-green fluorescent protein. J.Cell Biol. 1998, 142:1105-1119.
2. Aliee M., Röper J.C., Landsberg K.P., Pentzold C., Widmann T.J., Jülicher F., Dahmann C. Physical mechanisms shaping the Drosophila dorsoventral compartment boundary. Curr. Biol. 2012, 22:967-976.
3. Cavey M., Rauzi M., Lenne P.F., Lecuit T. A two-tiered mechanism for stabilization and immobilization of E-cadherin. Nature 2008, 453:751-756.
4. Charras G., Paluch E. Blebs lead the way: how to migrate without lamellipodia. Nat. Rev. Mol. Cell Biol. 2008, 9:730-736.
5. Chen X., Gumbiner B.M. Paraxial protocadherin mediates cell sorting and tissue morphogenesis by regulating C-cadherin adhesion activity. J.Cell Biol. 2006, 174:301-313.
6. Cooke J.E., Kemp H.A., Moens C.B. EphA4 is required for cell adhesion and rhombomere-boundary formation in the zebrafish. Curr. Biol. 2005, 15:536-542.
7. Domingo C., Keller R. Induction of notochord cell intercalation behavior and differentiation by progressive signals in the gastrula of Xenopus laevis. Development 1995, 121:3311-3321.
8. Durbin L., Brennan C., Shiomi K., Cooke J., Barrios A., Shanmugalingam S., Guthrie B., Lindberg R., Holder N. Eph signaling is required for segmentation and differentiation of the somites. Genes Dev. 1998, 12:3096-3109.
9. Fagotto F., Brown C.M. Detection of nuclear β-catenin in Xenopus embryos. Methods Mol. Biol. 2008, 469:363-380.
10. Foty R.A., Steinberg M.S. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 2005, 278:255-263.
11. Harris A.K. Is Cell sorting caused by differences in the work of intercellular adhesion? A critique of the Steinberg hypothesis. J.Theor. Biol. 1976, 61:267-285.
12. Heasman J., Crawford A., Goldstone K., Garner-Hamrick P., Gumbiner B., McCrea P., Kintner C., Noro C.Y., Wylie C. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 1994, 79:791-803.
13. Heasman J., Ginsberg D., Geiger B., Goldstone K., Pratt T., Yoshida-Noro C., Wylie C. A functional test for maternally inherited cadherin inXenopus shows its importance in cell adhesion at the blastula stage. Development 1994, 120:49-57.
14. Huveneers S., Oldenburg J., Spanjaard E., van der Krogt G., Grigoriev I., Akhmanova A., Rehmann H., de Rooij J. Vinculin associates with endothelial VE-cadherin junctions to control force-dependent remodeling. J.Cell Biol. 2012, 196:641-652.
15. Keller R., Cooper M.S., Danilchik M., Tibbetts P., Wilson P.A. Cell intercalation during notochord development in Xenopus laevis. J.Exp. Zool. 1989, 251:134-154.
16. Kemp H.A., Cooke J.E., Moens C.B. EphA4 and EfnB2a maintain rhombomere coherence by independently regulating intercalation of progenitor cells in the zebrafish neural keel. Dev. Biol. 2009, 327:313-326.
17. Krieg M., Arboleda-Estudillo Y., Puech P.H., Käfer J., Graner F., Müller D.J., Heisenberg C.P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 2008, 10:429-436.
18. Landsberg K.P., Farhadifar R., Ranft J., Umetsu D., Widmann T.J., Bittig T., Said A., Jülicher F., Dahmann C. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Curr. Biol. 2009, 19:1950-1955.
19. Lee C.H., Gumbiner B.M. Disruption of gastrulation movements in Xenopus by a dominant-negative mutant for C-cadherin. Dev. Biol. 1995, 171:363-373.
20. Maghzal N., Vogt E., Reintsch W., Fraser J.S., Fagotto F. The tumor-associated EpCAM regulates morphogenetic movements through intracellular signaling. J.Cell Biol. 2010, 191:645-659.
21. Maître J.L., Berthoumieux H., Krens S.F., Salbreux G., Jülicher F., Paluch E., Heisenberg C.P. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 2012, 338:253-256.
22. Manning M.L., Foty R.A., Steinberg M.S., Schoetz E.M. Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl. Acad. Sci. USA 2010, 107:12517-12522.
23. Medina A., Swain R.K., Kuerner K.M., Steinbeisser H. Xenopus paraxial protocadherin has signaling functions and is involved in tissue separation. EMBO J. 2004, 23:3249-3258.
24. Monier B., Pelissier-Monier A., Brand A.H., Sanson B. An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nat. Cell Biol. 2010, 12:60-65.
25. Moore S.W., Keller R.E., Koehl M.A. The dorsal involuting marginal zone stiffens anisotropically during its convergent extension in the gastrula of Xenopus laevis. Development 1995, 121:3131-3140.
26. Park E.C., Cho G.S., Kim G.H., Choi S.C., Han J.K. The involvement of Eph-Ephrin signaling in tissue separation and convergence during Xenopus gastrulation movements. Dev. Biol. 2011, 350:441-450.
27. Puklin-Faucher E., Sheetz M.P. The mechanical integrin cycle. J.Cell Sci. 2009, 122:179-186.
28. Ratheesh A., Yap A.S. A bigger picture: classical cadherins and the dynamic actin cytoskeleton. Nat. Rev. Mol. Cell Biol. 2012, 13:673-679.
29. Reintsch W.E., Habring-Mueller A., Wang R.W., Schohl A., Fagotto F. beta-Catenin controls cell sorting at the notochord-somite boundary independently of cadherin-mediated adhesion. J.Cell Biol. 2005, 170:675-686.
30. Rohani N., Canty L., Luu O., Fagotto F., Winklbauer R. EphrinB/EphB signaling controls embryonic germ layer separation by contact-induced cell detachment. PLoS Biol. 2011, 9:e1000597.
31. Schohl A., Fagotto F. β-catenin, MAPK and Smad signaling during early Xenopus development. Development 2002, 129:37-52.
32. Schwartz M.A., DeSimone D.W. Cell adhesion receptors in mechanotransduction. Curr. Op. Cell Biol. 2008, 20:551-556.
33. Steinberg M.S. Does differential adhesion govern self-assembly processes in histogenesis? Equilibrium configurations and the emergence ofa hierarchy among populations of embryonic cells. J.Exp. Zool. 1970, 173:395-433.
34. Steinberg M.S., McNutt P.M. Cadherins and their connections: adhesion junctions have broader functions. Curr. Opin. Cell Biol. 1999, 11:554-560.
35. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 1995, 7:619-627.
36. Tepass U. Genetic analysis of cadherin function in animal morphogenesis. Curr. Opin. Cell Biol. 1999, 11:540-548.
37. Tepass U., Hartenstein V. The development of cellular junctions in the Drosophila embryo. Dev. Biol. 1994, 161:563-596.
38. Vasioukhin V., Bauer C., Yin M., Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 2000, 100:209-219.
39. Wacker S., Grimm K., Joos T., Winklbauer R. Development and control of tissue separation at gastrulation in Xenopus. Dev. Biol. 2000, 224:428-439.
40. Watanabe T., Sato Y., Saito D., Tadokoro R., Takahashi Y. EphrinB2 coordinates the formation of a morphological boundary and cell epithelialization during somite segmentation. Proc. Natl. Acad. Sci. USA 2009, 106:7467-7472.
41. Winklbauer R. Cell adhesion in amphibian gastrulation. Int. Rev. Cell Mol. Biol. 2009, 278:215-275.
42. Yonemura S., Wada Y., Watanabe T., Nagafuchi A., Shibata M. alpha-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 2010, 12:533-542.