Eph/Ephrin signalling maintains eye field segregation from adjacent neural plate territories during forebrain morphogenesis

Development (Cambridge)

Volumn 140, Issue 20, 2013, Pages 4193-4202

  Cavodeassi, Florencia ^a,b   Ivanovitch, Kenzo ^a   Wilson, Stephen W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Eye field; Morphogenesis; Neural plate; Zebrafish

Indexed keywords

EPHRIN; EPHRIN RECEPTOR; F ACTIN; MYOSIN II;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY LABELING; ARTICLE; BRAIN DEVELOPMENT; CELL ADHESION; CELL TRANSPLANTATION; DEVELOPMENTAL STAGE; EMBRYO; EYE DEVELOPMENT; FOREBRAIN; FRONTAL EYE FIELD; GASTRULATION; GENOTYPE; IMAGINAL DISC; MICROINJECTION; MUTANT; NEUROECTODERM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TELENCEPHALON; ZEBRA FISH;

EYE FIELD; MORPHOGENESIS; NEURAL PLATE; ZEBRAFISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; DIENCEPHALON; EPHRINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MORPHOGENESIS; NEURAL PLATE; PROSENCEPHALON; RECEPTORS, EPH FAMILY; SIGNAL TRANSDUCTION; TELENCEPHALON; ZEBRAFISH;

EID: 84884921388     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.097048     Document Type: Article

References (57)

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. Amack, J. D. and Manning, M. L. (2012). Knowing the boundaries: extending the differential adhesion hypothesis in embryonic cell sorting. Science 338, 212-215.
3. Arvanitis, D. and Davy, A. (2008). Eph/ephrin signaling: networks. Genes Dev. 22, 416-429.
4. Arvanitis, D. N., Béhar, A., Tryoen-Tóth, P., Bush, J. O., Jungas, T. H., Vitale, N. and Davy, A. (2013). Ephrin B1 maintains apical adhesion of neural progenitors. Development 140, 2082-2092.
5. Bailey, T. J., El-Hodiri, H., Zhang, L., Shah, R., Mathers, P. H. and Jamrich, M. (2004). Regulation of vertebrate eye development by Rx genes. Int. J. Dev. Biol. 48, 761-770.
6. 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.
7. Beccari, L., Marco-Ferreres, R. and Bovolenta, P. (2013). The logic of gene regulatory networks in early vertebrate forebrain patterning. Mech. Dev. 130, 95-111.
8. Bielen, H. and Houart, C. (2012). BMP signaling protects telencephalic fate by repressing eye identity and its Cxcr4-dependent morphogenesis. Dev. Cell 23, 812-822.
9. Brown, K. E., Keller, P. J., Ramialison, M., Rembold, M., Stelzer, E. H., Loosli, F. and Wittbrodt, J. (2010). Nlcam modulates midline convergence during anterior neural plate morphogenesis. Dev. Biol. 339, 14-25.
10. Cavodeassi, F. and Houart, C. (2012). Brain regionalization: of signaling centers and boundaries. Dev. Neurobiol. 72, 218-233.
11. Cavodeassi, F., Carreira-Barbosa, F., Young, R. M., Concha, M. L., Allende, M. L., Houart, C., Tada, M. and Wilson, S. W. (2005). Early stages of zebrafish eye formation require the coordinated activity of Wnt11, Fz5, and the Wnt/betacatenin pathway. Neuron 47, 43-56.
12. Cerveny, K. L., Cavodeassi, F., Turner, K. J., de Jong-Curtain, T. A., Heath, J. K. and Wilson, S. W. (2010). The zebrafish flotte lotte mutant reveals that the local retinal environment promotes the differentiation of proliferating precursors emerging from their stem cell niche. Development 137, 2107-2115.
13. Cooke, J. E., Xu, Q., Wilson, S. W. and Holder, N. (1997). Characterisation of five novel zebrafish Eph-related receptor tyrosine kinases suggests roles in patterning the neural plate. Dev. Genes Evol. 206, 515-531.
14. Cooke, J., Moens, C., Roth, L., Durbin, L., Shiomi, K., Brennan, C., Kimmel, C., Wilson, S. and Holder, N. (2001). Eph signalling functions downstream of Val to regulate cell sorting and boundary formation in the caudal hindbrain. Development 128, 571-580.
15. 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.
16. Dahmann, C., Oates, A. C. and Brand, M. (2011). Boundary formation and maintenance in tissue development. Nat. Rev. Genet. 12, 43-55.
17. 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.
18. Durbin, L., Sordino, P., Barrios, A., Gering, M., Thisse, C., Thisse, B., Brennan, C., Green, A., Wilson, S. and Holder, N. (2000). Anteroposterior patterning is required within segments for somite boundary formation in developing zebrafish. Development 127, 1703-1713.
19. Janes, P. W., Griesshaber, B., Atapattu, L., Nievergall, E., Hii, L. L., Mensinga, A., Chheang, C., Day, B. W., Boyd, A. W., Bastiaens, P. I. et al. (2011). Eph receptor function is modulated by heterooligomerization of A and B type Eph receptors. J. Cell Biol. 195, 1033-1045.
20. Janes, P. W., Nievergall, E. and Lackmann, M. (2012). Concepts and consequences of Eph receptor clustering. Semin. Cell Dev. Biol. 23, 43-50.
21. Jülich, D., Hwee Lim, C., Round, J., Nicolaije, C., Schroeder, J., Davies, A., Geisler, R., Lewis, J., Jiang, Y. J., Holley, S. A.; Tübingen 2000 Screen Consortium (2005). beamter/deltaC and the role of Notch ligands in the zebrafish somite segmentation, hindbrain neurogenesis and hypochord differentiation. Dev. Biol. 286, 391-404.
22. Jülich, D., Mould, A. P., Koper, E. and Holley, S. A. (2009). Control of extracellular matrix assembly along tissue boundaries via Integrin and Eph/Ephrin signaling. Development 136, 2913-2921.
23. Kai, M., Heisenberg, C. P. and Tada, M. (2008). Sphingosine-1-phosphate receptors regulate individual cell behaviours underlying the directed migration of prechordal plate progenitor cells during zebrafish gastrulation. Development 135, 3043-3051.
24. Kardash, E., Reichman-Fried, M., Maitre, J. L., Boldajipour, B., Papusheva, E., Messerschmidt, E. M., Heisenberg, C. P. and Raz, E. (2010). A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat. Cell Biol. 12, 47-53.
25. Kiecker, C. and Lumsden, A. (2012). The role of organizers in patterning the nervous system. Annu. Rev. Neurosci. 35, 347-367.
26. Kullander, K. and Klein, R. (2002). Mechanisms and functions of Eph and ephrin signalling. Nat. Rev. Mol. Cell Biol. 3, 475-486.
27. Lackmann, M. and Boyd, A. W. (2008). Eph, a protein family coming of age: more confusion, insight, or complexity? Sci. Signal. 1, re2.
28. 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.
29. Lee, H. S., Bong, Y. S., Moore, K. B., Soria, K., Moody, S. A. and Daar, I. O. (2006). Dishevelled mediates ephrinB1 signalling in the eye field through the planar cell polarity pathway. Nat. Cell Biol. 8, 55-63.
30. Loosli, F., Staub, W., Finger-Baier, K. C., Ober, E. A., Verkade, H., Wittbrodt, J. and Baier, H. (2003). Loss of eyes in zebrafish caused by mutation of chokh/rx3. EMBO Rep. 4, 894-899.
31. Miao, H. and Wang, B. (2009). Eph/ephrin signaling in epithelial development and homeostasis. Int. J. Biochem. Cell Biol. 41, 762-770.
32. Monier, B., Pelissier-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.
33. Moore, K. B., Mood, K., Daar, I. O. and Moody, S. A. (2004). Morphogenetic movements underlying eye field formation require interactions between the FGF and ephrinB1 signaling pathways. Dev. Cell 6, 55-67.
34. Nair, S. and Schilling, T. F. (2008). Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 322, 89-92.
35. Neff, M. M., Neff, J. D., Chory, J. and Pepper, A. E. (1998). dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J. 14, 387-392.
36. 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.
37. Pasini, A. and Wilkinson, D. G. (2002). Stabilizing the regionalisation of the developing vertebrate central nervous system. BioEssays 24, 427-438.
38. Pasquale, E. B. (2008). Eph-ephrin bidirectional signaling in physiology and disease. Cell 133, 38-52.
39. Raz, E. and Mahabaleshwar, H. (2009). Chemokine signaling in embryonic cell migration: a fisheye view. Development 136, 1223-1229.
40. Rembold, M., Lahiri, K., Foulkes, N. S. and Wittbrodt, J. (2006a). Transgenesis in fish: efficient selection of transgenic fish by co-injection with a fluorescent reporter construct. Nat. Protoc. 1, 1133-1139.
41. Rembold, M., Loosli, F., Adams, R. J. and Wittbrodt, J. (2006b). Individual cell migration serves as the driving force for optic vesicle evagination. Science 313, 1130-1134.
42. Rohani, N., Canty, L., Luu, O., Fagotto, F. and Winklbauer, R. (2011). EphrinB/EphB signaling controls embryonic germ layer separation by contactinduced cell detachment. PLoS Biol. 9, e1000597.
43. Salvucci, O., de la Luz Sierra, M., Martina, J. A., McCormick, P. J. and Tosato, G. (2006). EphB2 and EphB4 receptors forward signaling promotes SDF-1-induced endothelial cell chemotaxis and branching remodeling. Blood 108, 2914-2922.
44. Sharfe, N., Freywald, A., Toro, A., Dadi, H. and Roifman, C. (2002). Ephrin stimulation modulates T cell chemotaxis. Eur. J. Immunol. 32, 3745-3755.
45. Stigloher, C., Ninkovic, J., Laplante, M., Geling, A., Tannhäuser, B., Topp, S., Kikuta, H., Becker, T. S., Houart, C. and Bally-Cuif, L. (2006). Segregation of telencephalic and eye-field identities inside the zebrafish forebrain territory is controlled by Rx3. Development 133, 2925-2935.
46. Tanaka, M., Kamo, T., Ota, S. and Sugimura, H. (2003). Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion. EMBO J. 22, 847-858.
47. Theil, T., Frain, M., Gilardi-Hebenstreit, P., Flenniken, A., Charnay, P. and Wilkinson, D. G. (1998). Segmental expression of the EphA4 (Sek-1) receptor tyrosine kinase in the hindbrain is under direct transcriptional control of Krox-20. Development 125, 443-452.
48. Thisse, C. and Thisse, B. (2005). High throughput expression analysis of zfmodels consortium clones. ZFIN direct data submission. http://zfin.org.
49. Thisse, B., Wright, G. J. and Thisse, C. (2008). Embryonic and larval expression patterns from a large scale screening for novel low affinity extracellular protein interactions. ZFIN direct data submission. http://zfin.org.
50. Viktorin, G., Chiuchitu, C., Rissler, M., Varga, Z. M. and Westerfield, M. (2009). Emx3 is required for the differentiation of dorsal telencephalic neurons. Dev. Dyn. 238, 1984-1998.
51. 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.
52. Westerfield, M. (1993). The Zebrafish Book: a Guide for the Laboratory Use of the Zebrafish (Brachydanio rerio). Eugene, OR: University of Oregon Press.
53. Wilson, S. W. and Houart, C. (2004). Early steps in the development of the forebrain. Dev. Cell 6, 167-181.
54. Winkler, S., Loosli, F., Henrich, T., Wakamatsu, Y. and Wittbrodt, J. (2000). The conditional medaka mutation eyeless uncouples patterning and morphogenesis of the eye. Development 127, 1911-1919.
55. Xu, Q., Holder, N., Patient, R. and Wilson, S. W. (1994). Spatially regulated expression of three receptor tyrosine kinase genes during gastrulation in the zebrafish. Development 120, 287-299.
56. Xu, Q., Alldus, G., Macdonald, R., Wilkinson, D. G. and Holder, N. (1996). Function of the Eph-related kinase rtk1 in patterning of the zebrafish forebrain. Nature 381, 319-322.
57. Xu, Q., Mellitzer, G., Robinson, V. and Wilkinson, D. G. (1999). In vivo cell sorting in complementary segmental domains mediated by Eph receptors and ephrins. Nature 399, 267-271.