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The Role of DE-Cadherin During Cellularization, Germ Layer Formation and Early Neurogenesis in the Drosophila Embryo

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The Role of DE-Cadherin During Cellularization, Germ Layer Formation and Early Neurogenesis in the Drosophila Embryo View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Developmental Biology 270 (2004) 350–363 www.elsevier.com/locate/ydbio The role of DE-cadherin during cellularization, germ layer formation and early neurogenesis in the Drosophila embryo Fay Wang, Karin Dumstrei, Thomas Haag, and Volker Hartenstein* Department of Molecular Cell and Developmental Biology, University of California Los Angeles, Los Angeles, CA 90095, USA Received for publication 24 November 2003; revised 4 March 2004; accepted 5 March 2004 Available online 15 April 2004 Abstract The Drosophila E-cadherin homolog, DE-cadherin, is expressed and required in all epithelial tissues throughout embryogenesis. Due to a strong maternal component of DE-cadherin, its early function during embryogenesis has remained elusive. The expression of a dominant negative DE-cadherin construct (UAS-DE-cadex) using maternally active driver lines allowed us to analyze the requirements for DE-cadherin during this early phase of development. Maternally expressed DE-cadex result in phenotype with variable expressivity. Most severely affected embryos have abnormalities in epithelialization of the blastoderm, resulting in loss of the blastodermal cells’ apico-basal polarity and monolayered structure. Another phenotypic class forms a rather normal blastoderm, but shows abnormalities in proliferation and morphogenetic movements during gastrulation and neurulation. Mitosis of the mesoderm occurs prematurely before invagination, and proliferation in the ectoderm, normally a highly ordered process, occurs in a random pattern. Mitotic spindles of ectodermal cells, normally aligned horizontally, frequently occurred vertically or at an oblique angle. This finding further supports recent findings indicating that, in the wild-type ectoderm, the zonula adherens is required for the horizontal orientation of mitotic spindles. Proliferation defects in DE-cadex- expressing embryos are accompanied by the loss of epithelial structure of ectoderm and neuroectoderm. These germ layers form irregular double or triple layers of rounded cells that lack zonula adherens. In the multilayered neuroectoderm, epidermal precursors, neuroblasts and ganglion mother cells occurred intermingled, attesting to the pivotal role of DE-cadherin in delamination and polarized division of neuroblasts. By contrast, the overall number and spacing of neuroblasts was grossly normal, indicating that DE-cadherin-mediated adhesion is less important for cell–cell interaction controlling the ratio of epidermal vs. neural progenitors. D 2004 Elsevier Inc. All rights reserved. Keywords: DE-cadherin; Shotgun; Blastoderm; Gastrulation; Neuroectoderm Introduction even physically linked to cadherins (Dumstrei et al., 2002; Hazan and Norton, 1998; Hoschuetzky et al., 1994), these Cell adhesion molecules of the cadherin family play a adhesion molecules have also been implicated in specific pivotal role during morphogenesis in the developing em- cell–cell interactions governing cell fate and differentiation. bryo. Cadherins are required for the stability of epithelial To gain insight into the role of E-cadherin during layers, as well as movements of epithelial cells, mesenchy- morphogenesis, we followed an in vivo approach using mal cells and outgrowing neurites (Redies, 2000; Tepass, the Drosophila embryo as a model system. Drosophila 1999; Tepass et al., 2000). The differential expression of has two classical cadherins, DE-cadherin (encoded by the different cadherins allows for cell sorting, a process involved gene shotgun; Tepass et al., 1996; Uemura et al., 1996), and in the setting up of boundaries and segregation of different DN-cadherin (Iwai et al., 1997). Classical cadherins are tissues. Because many receptor molecules are close to or defined not only by possessing several characteristic cad- herin repeats in their extracellular domain, but also binding to the actin cytoskeleton via a highly conserved complex of * Corresponding author. Department of Molecular Cell and Develop- adapters, including h-catenin (Drosophila homolog Arma- mental Biology, University of California Los Angeles, Room 4214, Life Sciences Building, 621 Charles E. Young Dr. S., Los Angeles, CA 90095. dillo; Peifer and Wieschaus, 1990), a-catenin (Imamura Fax: +1-310-206-3987. et al., 1999; Oda et al., 1993), vinculin and a-actinin (Hazan E-mail address: [email protected] (V. Hartenstein). et al., 1997; Watabe-Uchida et al., 1998; Weiss et al., 1998). 0012-1606/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ydbio.2004.03.002 F. Wang et al. / Developmental Biology 270 (2004) 350–363 351 In addition, another catenin, p120ctn is found to bind to the mic domain (UAS-DE-cadex; Dumstrei et al., 2003a) and a juxtamembrane region of E-cadherin and it functions as a deletion construct eliminating both extracellular and trans- regulator of E-cadherin-mediated cell adhesion (reviews by membrane domains (UAS-DE-cadcyt). We expressed these Anastasiadis and Reynolds, 2001; Peifer and Yap, 2003). constructs, using several different driver lines including The catenin-mediated link to the cytoskeleton is gener- maternally expressed driver lines, heatshock-Gal4 and ally required for the adhesive function of E-cadherin daughterless-Gal4. The results indicate that DE-cadherin (Nagafuchi and Takeichi, 1988) and most other cadherins. plays an important role in blastoderm formation, gastrula- However, it has been shown recently that the extracellular tion and neurulation. In the blastoderm, both the anchoring and transmembrane domain of VE-cadherin and DE-cad- of nuclei to the membrane and cleavage furrow formation herin is sufficient to provide ‘‘weak’’ adhesion in cultured are disrupted in embryos lacking DE-cadherin function. cells (Navarro et al., 1995; Oda and Tsukita, 1999).Fur- During gastrulation, ventral furrow invagination and its thermore, Daniel and Reynolds (1997) showed that the coordination with mitosis in mesoderm require DE-cad- cadherin-mediated adhesion could be rapidly reduced by herin. Finally, DE-cadherin is essential for the epithelial increasing the tyrosine phosphorylation level of h-catenin. integrity in the neuroectoderm, the ordered delamination of When h-catenin is hyper-phosphorylated, it dissociates neuroblasts and the orientation of mitotic spindles in from cadherin and a-catenin causing the Cadherin Catenin dividing neuroectodermal cells. Complex (CCC) to disassemble from the actin cytoskeleton. Previous studies conducted by us and others have shown that DE-cadherin is expressed and required for the formation Material and methods and maintenance of all Drosophila embryonic epithelia (Tepass et al., 1996; Uemura et al., 1996),aswellas Fly stocks oogenesis (Godt and Tepass, 1998). Eliminating both the maternal and zygotic shg arrests development as early as Oregon R flies were used as the wild-type stock. The during oogenesis. Germline clones, using weak or moderate following Gal4 driver lines and UAS constructs (Brand and shg alleles, result in embryos that show severe defects in all Perrimon, 1993) were used: daughterless-Gal4 (da-Gal4; epithelia (Tepass et al., 1996). On the other hand, taking kindly provided by Dr. J. Campos-Ortega); heatshock-Gal4 away zygotic shg function and leaving the maternal copy of (hs-Gal4), mata4-Gal4-VP16 (Hacker and Perrimon, 1998; the gene intact results in embryos that develop relatively kindly provided by Dr. F. Schweisguth); nanos-Gal4, normal until after neurulation. It is during this time when the NGT40 (Tracey et al., 2000; provided by Bloomington epithelial defects consisting in the loss of apico-basal Stock Center). polarity, cell dissociation and defective cell movement set in. The maternal contribution of shg prohibited us from S2 cell culture and cell adhesion assay analyzing the role of DE-cadherin during early morphoge- netic events, including blastoderm formation, gastrulation S2 cells were cultured in Schneider’s medium supple- and early neurogenesis. Given its dynamic expression in the mented with 10% fetal calf serum. Cells were transiently blastoderm and neuroectoderm, one has to assume that DE- transfected with either prmha-3-DE-cadherin or prmha-3- cadherin plays a pivotal role during these stages. Of partic- DE-cadex using calcium phosphate precipitation as previ- ular interest is the question of how far signaling events in ously described (Nagafuchi et al., 1987; Invitrogen). Expres- between adjacent cells, such as the Notch (N)-Delta (Dl) sion of the transgenes was induced with 0.7 mM CuSO4 after signaling which specifies epidermoblasts, depend on DE- 24 h post-transfection. Following induction of the trans- cadherin-mediated adhesion. Both N and Dl have been genes, cells were placed on a rotator at 30 rpm overnight and shown to be concentrated in the apical–lateral region of checked for aggregation under an inverted microscope. the epithelial membrane where the zonula adherens is located (Fehon et al., 1991; Kooh et al., 1993). It is possible Embryo collection and fixation that the strength of DE-cadherin-mediated adhesion has an effect on the way in which Dl and its receptor N are able to Mata4-Gal4 virgin female flies were selected and crossed interact. Thus, a decrease in DE-cadherin activity might to UAS-DE-cadex male flies. Eggs were collected on yeasted disrupt N–Dl interactions, in which case a neurogenic apple juice agar plates at 29jC and 25jC for 6 h. Embryonic phenotype (neural hyperplasia)
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