Syntenin, a syndecan adaptor and an Arf6 phosphatidylinositol 4,5-bisphosphate effector, is essential for epiboly and gastrulation cell movements in zebrafish.
Lambaerts, Kathleen; Van Dyck, Stijn; Mortier, Evaet al.
2012 • In Journal of Cell Science, 125 (Pt 5), p. 1129-40
[en] Epiboly, the spreading and the thinning of the blastoderm to cover the yolk cell and close the blastopore in fish embryos, is central to the process of gastrulation. Despite its fundamental importance, little is known about the molecular mechanisms that control this coordinated cell movement. By a combination of knockdown studies and rescue experiments in zebrafish (Danio rerio), we show that epiboly relies on the molecular networking of syntenin with syndecan heparan sulphate proteoglycans, which act as co-receptors for adhesion molecules and growth factors. Furthermore, we show that the interaction of syntenin with phosphatidylinositol 4,5-bisphosphate (PIP2) and with the small GTPase ADP-ribosylation factor 6 (Arf6), which regulate the endocytic recycling of syndecan, is necessary for epiboly progression. Analysis of the earliest cellular defects suggests a role for syntenin in the autonomous vegetal expansion of the yolk syncytial layer and the rearrangement of the actin cytoskeleton in extra-embryonic tissues, but not in embryonic cell fate determination. This study identifies the importance of the syntenin-syndecan-PIP2-Arf6 complex for the progression of fish epiboly and establishes its key role in directional cell movements during early development.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Lambaerts, Kathleen
Van Dyck, Stijn
Mortier, Eva
Ivarsson, Ylva
Degeest, Gisele
Luyten, Annouck
Vermeiren, Elke
Peers, Bernard ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
David, Guido
Zimmermann, Pascale
Language :
English
Title :
Syntenin, a syndecan adaptor and an Arf6 phosphatidylinositol 4,5-bisphosphate effector, is essential for epiboly and gastrulation cell movements in zebrafish.
Bass, M. D., Roach, K. A., Morgan, M. R., Mostafavi-Pour, Z., Schoen, T., Muramatsu, T., Mayer, U., Ballestrem, C., Spatz, J. P. and Humphries, M. J. (2007). Syndecan-4-dependent Rac1 regulation determines directional migration in response to the extracellular matrix. J. Cell Biol. 177, 527-538.
Beekman, J. M. and Coffer, P. J. (2008). The ins and outs of syntenin, a multifunctional intracellular adaptor protein. J. Cell Sci. 121, 1349-1355.
Betchaku, T. A. T. J. (1986). Programmed endocytosis during epiboly of Fundulus heteroclitus. Amer. Zool 26, 193-196.
Carvalho, L. and Heisenberg, C. P. (2010). The yolk syncytial layer in early zebrafish development. Trends Cell Biol. 10, 586-592.
Chen, E., Hermanson, S. and Ekker, S. C. (2004). Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103, 1710-1719.
Cheng, J. C., Miller, A. L. and Webb, S. E. (2004). Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev. Dyn. 231, 313-323.
D'Amico, L. A. and Cooper, M. S. (2001). Morphogenetic domains in the yolk syncytial layer of axiating zebrafish embryos. Dev. Dyn. 222, 611-624.
D'Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
Detrich, H. W., Westerfield, M. and Zon, L. I. (2004). The Zebrafish: Cellular and Developmental Biology (Second Edition). Elsevier Academic Press, Amsterdam. Donaldson, J. G. (2003). Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J. Biol. Chem. 278, 41573-41576.
Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Durr, J. and David, G. (1997). Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. USA 94, 13683-13688.
Grootjans, J. J., Reekmans, G., Ceulemans, H. and David, G. (2000). Synteninsyndecan binding requires syndecan-synteny and the co-operation of both PDZ domains of syntenin. J. Biol. Chem. 275, 19933-19941.
Honda, A., Nogami, M., Yokozeki, T., Yamazaki, M., Nakamura, H., Watanabe, H., Kawamoto, K., Nakayama, K., Morris, A. J., Frohman, M. A. et al. (1999). Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99, 521-532.
Jowett, T. (2001). Double in situ hybridization techniques in zebrafish. Methods 23, 345-358.
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
Koo, B. K., Jung, Y. S., Shin, J., Han, I., Mortier, E., Zimmermann, P., Whiteford, J. R., Couchman, J. R., Oh, E. S. and Lee, W. (2006). Structural basis of syndecan- 4 phosphorylation as a molecular switch to regulate signaling. J. Mol. Biol. 355, 651-663.
Koppen, M., Fernandez, B. G., Carvalho, L., Jacinto, A. and Heisenberg, C. P. (2006). Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development 133, 2671-2681.
Krens, S. F., He, S., Lamers, G. E., Meijer, A. H., Bakkers, J., Schmidt, T., Spaink, H. P. and Snaar-Jagalska, B. E. (2008). Distinct functions for ERK1 and ERK2 in cell migration processes during zebrafish gastrulation. Dev. Biol. 319, 370-383.
Lachnit, M., Kur, E. and Driever, W. (2008). Alterations of the cytoskeleton in all three embryonic lineages contribute to the epiboly defect of Pou5f1/Oct4 deficient MZspg zebrafish embryos. Dev. Biol. 315, 1-17.
Lambaerts, K., Wilcox-Adelman, S. A. and Zimmermann, P. (2009). The signaling mechanisms of syndecan heparan sulfate proteoglycans. Curr. Opin. Cell Biol. 21, 662-669.
Latimer, A. and Jessen, J. R. (2010). Extracellular matrix assembly and organization during zebrafish gastrulation. Matrix Biol. 29, 89-96.
Lepage, S. E. and Bruce, A. E. (2010). Zebrafish epiboly: mechanics and mechanisms. Int. J. Dev. Biol. 54, 1213-1228.
Leptin, M. (2005). Gastrulation movements: the logic and the nuts and bolts. Dev. Cell 8, 305-320.
Leskow, F. C., Holloway, B. A., Wang, H., Mullins, M. C. and Kazanietz, M. G. (2006). The zebrafish homologue of mammalian chimerin Rac-GAPs is implicated in epiboly progression during development. Proc. Natl. Acad. Sci. USA 103, 5373-5378.
Luyten, A., Mortier, E., Van Campenhout, C., Taelman, V., Degeest, G., Wuytens, G., Lambaerts, K., David, G., Bellefroid, E. J. and Zimmermann, P. (2008). The postsynaptic density 95/disc-large/zona occludens protein syntenin directly interacts with frizzled 7 and supports noncanonical Wnt signaling. Mol. Biol. Cell 19, 1594-1604.
Matthews, H. K., Marchant, L., Carmona-Fontaine, C., Kuriyama, S., Larrain, J., Holt, M. R., Parsons, M. and Mayor, R. (2008). Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/ RhoA. Development 135, 1771-1780.
Mortier, E., Wuytens, G., Leenaerts, I., Hannes, F., Heung, M. Y., Degeest, G., David, G. and Zimmermann, P. (2005). Nuclear speckles and nucleoli targeting by PIP2-PDZ domain interactions. EMBO J. 24, 2556-2565.
Myers, K. R. and Casanova, J. E. (2008). Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol. 18, 184-192.
Nourry, C., Grant, S. G. and Borg, J. P. (2003). PDZ domain proteins: plug and play! Sci. STKE 2003, RE7.
Radhakrishna, H. and Donaldson, J. G. (1997). ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway. J. Cell Biol. 139, 49-61.
Rohde, L. A. and Heisenberg, C. P. (2007). Zebrafish gastrulation: cell movements, signals, and mechanisms. Int. Rev. Cytol. 261, 159-192.
Roszko, I., Sawada, A. and Solnica-Krezel, L. (2009). Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin. Cell Dev. Biol. 20, 986-997.
Solnica-Krezel, L. (2005). Conserved patterns of cell movements during vertebrate gastrulation. Curr. Biol. 15, R213-R228.
Solnica-Krezel, L. (2006). Gastrulation in zebrafish - all just about adhesion? Curr. Opin. Genet Dev. 16, 433-441.
Solnica-Krezel, L. and Driever, W. (1994). Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly. Development 120, 2443-2455.
Steinfeld, R., Van Den Berghe, H. and David, G. (1996). Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133, 405-416.
Strahle, U. and Jesuthasan, S. (1993). Ultraviolet irradiation impairs epiboly in zebrafish embryos: evidence for a microtubule-dependent mechanism of epiboly. Development 119, 909-919.
Trinkaus, J. P. (1951). A study of the mechanisms of epiboly in the egg of fundulus heteroclitus. J. Exp. Zool. 118, 269-319.
Varnai, P. and Balla, T. (1998). Visualization of phosphoinositides that bind pleckstrin homology domains: calcium- and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510.
Warga, R. M. and Kimmel, C. B. (1990). Cell movements during epiboly and gastrulation in zebrafish. Development 108, 569-580.
Whiteford, J. R. and Couchman, J. R. (2006). A conserved NXIP motif is required for cell adhesion properties of the syndecan-4 ectodomain. J. Biol. Chem. 281, 32156-32163.
Zalik, S. E., Lewandowski, E., Kam, Z. and Geiger, B. (1999). Cell adhesion and the actin cytoskeleton of the enveloping layer in the zebrafish embryo during epiboly. Biochem. Cell Biol. 77, 527-542.
Zimmermann, P., Meerschaert, K., Reekmans, G., Leenaerts, I., Small, J. V., Vandekerckhove, J., David, G. and Gettemans, J. (2002). PIP(2)-PDZ domain binding controls the association of syntenin with the plasma membrane. Mol. Cell 9, 1215-1225.
Zimmermann, P., Zhang, Z., Degeest, G., Mortier, E., Leenaerts, I., Coomans, C., Schulz, J., N'Kuli, F., Courtoy, P. J. and David, G. (2005). Syndecan recycling [corrected] is controlled by syntenin-PIP2 interaction and Arf6. Dev. Cell 9, 377-388.