The Journal of Cell Biology, Vol 134, 149-163, Copyright © 1996 by The Rockefeller University Press

ARTICLES

armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila

HA Muller and E Wieschaus
Department of Molecular Biology, Princeton University, Princeton, New Jersey 08540, USA.

Cellularization of the Drosophila embryo results in the formation of a cell monolayer with many characteristics of a polarized epithelium. We have used antibodies specific to cellular junctions and nascent plasma membranes to study the formation of the zonula adherens (ZA) in relation to the establishment of basolateral membrane polarity. The same approach was then used as a test system to identify X-linked zygotically active genes required for ZA formation. We show that ZA formation begins during cellularization and that the basolateral membrane domain is established at mid-gastrulation. By creating deficiencies for defined regions of the X chromosome, we have identified genes that are required for the formation of the ZA and the generation of basolateral membrane polarity. We show that embryos mutant for both stardust (sdt) and bazooka (baz) fail to form a ZA. In addition to the failure to establish the ZA, the formation of the monolayered epithelium is disrupted after cellularization, resulting in formation of a multilayered cell sheet by mid-gastrulation. SEM analysis of mutant embryos revealed a conversion of cells exhibiting epithelial characteristics into cells exhibiting mesenchymal characteristics. To investigate how mutations that affect an integral component of the ZA itself influence ZA formation, we examined embryos with reduced maternal and zygotic supply of wild-type Arm protein. These embryos, like embryos mutant for both sdt and baz, exhibit an early disruption of ZA formation. These results suggest that early stages in the assembly of the ZA are critical for the stability of the polarized blastoderm epithelium.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

• Kaplan, N. A., Liu, X., Tolwinski, N. S. (2009). Epithelial Polarity: Interactions Between Junctions and Apical-Basal Machinery. Genetics 183: 897-904 [Abstract] [Full Text]  
• Cavey, M., Lecuit, T. (2009). Molecular Bases of Cell-Cell Junctions Stability and Dynamics. Cold Spring Harb. Perspect. Biol. 1: a002998-a002998 [Abstract] [Full Text]  
• Kim, S., Gailite, I., Moussian, B., Luschnig, S., Goette, M., Fricke, K., Honemann-Capito, M., Grubmuller, H., Wodarz, A. (2009). Kinase-activity-independent functions of atypical protein kinase C in Drosophila. J. Cell Sci. 122: 3759-3771 [Abstract] [Full Text]  
• Sawyer, J. K., Harris, N. J., Slep, K. C., Gaul, U., Peifer, M. (2009). The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction. JCB 186: 57-73 [Abstract] [Full Text]  
• Coureuil, M., Mikaty, G., Miller, F., Lecuyer, H., Bernard, C., Bourdoulous, S., Dumenil, G., Mege, R.-M., Weksler, B. B., Romero, I. A., Couraud, P.-O., Nassif, X. (2009). Meningococcal Type IV Pili Recruit the Polarity Complex to Cross the Brain Endothelium. Science 325: 83-87 [Abstract] [Full Text]  
• Amin, N., Khan, A., St. Johnston, D., Tomlinson, I., Martin, S., Brenman, J., McNeill, H. (2009). LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc. Natl. Acad. Sci. USA 106: 8941-8946 [Abstract] [Full Text]  
• McGill, M. A., McKinley, R.F. A., Harris, T. J.C. (2009). Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions. JCB 185: 787-796 [Abstract] [Full Text]  
• Pouille, P.-A., Ahmadi, P., Brunet, A.-C., Farge, E. (2009). Mechanical Signals Trigger Myosin II Redistribution and Mesoderm Invagination in Drosophila Embryos. Sci Signal 2: ra16-ra16 [Abstract] [Full Text]  
• Harris, K. P., Tepass, U. (2008). Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. JCB 183: 1129-1143 [Abstract] [Full Text]  
• Pope, K. L., Harris, T. J. C. (2008). Control of cell flattening and junctional remodeling during squamous epithelial morphogenesis in Drosophila. Development 135: 2227-2238 [Abstract] [Full Text]  
• Sokac, A. M., Wieschaus, E. (2008). Zygotically controlled F-actin establishes cortical compartments to stabilize furrows during Drosophila cellularization. J. Cell Sci. 121: 1815-1824 [Abstract] [Full Text]  
• Homem, C. C. F., Peifer, M. (2008). Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 135: 1005-1018 [Abstract] [Full Text]  
• Benchabane, H., Hughes, E. G., Takacs, C. M., Baird, J. R., Ahmed, Y. (2008). Adenomatous polyposis coli is present near the minimal level required for accurate graded responses to the Wingless morphogen. Development 135: 963-971 [Abstract] [Full Text]  
• Sfakianos, J., Togawa, A., Maday, S., Hull, M., Pypaert, M., Cantley, L., Toomre, D., Mellman, I. (2007). Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. JCB 179: 1133-1140 [Abstract] [Full Text]  
• Blankenship, J. T., Fuller, M. T., Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120: 3099-3110 [Abstract] [Full Text]  
• Dominguez-Gimenez, P., Brown, N. H., Martin-Bermudo, M. D. (2007). Integrin-ECM interactions regulate the changes in cell shape driving the morphogenesis of the Drosophila wing epithelium. J. Cell Sci. 120: 1061-1071 [Abstract] [Full Text]  
• Fox, D. T., Peifer, M. (2007). Abelson kinase (Abl) and RhoGEF2 regulate actin organization during cell constriction in Drosophila. Development 134: 567-578 [Abstract] [Full Text]  
• van Rossum, A. G.S.H., Aartsen, W. M., Meuleman, J., Klooster, J., Malysheva, A., Versteeg, I., Arsanto, J.-P., Le Bivic, A., Wijnholds, J. (2006). Pals1/Mpp5 is required for correct localization of Crb1 at the subapical region in polarized Muller glia cells. Hum Mol Genet 15: 2659-2672 [Abstract] [Full Text]  
• Yamanaka, T., Horikoshi, Y., Izumi, N., Suzuki, A., Mizuno, K., Ohno, S. (2006). Lgl mediates apical domain disassembly by suppressing the PAR-3-aPKC-PAR-6 complex to orient apical membrane polarity. J. Cell Sci. 119: 2107-2118 [Abstract] [Full Text]  
• Suzuki, A., Ohno, S. (2006). The PAR-aPKC system: lessons in polarity.. J. Cell Sci. 119: 979-987 [Abstract] [Full Text]  
• Bayraktar, J., Zygmunt, D., Carthew, R. W. (2006). Par-1 kinase establishes cell polarity and functions in Notch signaling in the Drosophila embryo. J. Cell Sci. 119: 711-721 [Abstract] [Full Text]  
• Pilot, F., Philippe, J.-M., Lemmers, C., Chauvin, J.-P., Lecuit, T. (2006). Developmental control of nuclear morphogenesis and anchoring by charleston, identified in a functional genomic screen of Drosophila cellularisation. Development 133: 711-723 [Abstract] [Full Text]  
• Kuo, C. T., Jan, L. Y., Jan, Y. N. (2005). Dendrite-specific remodeling of Drosophila sensory neurons requires matrix metalloproteases, ubiquitin-proteasome, and ecdysone signaling. Proc. Natl. Acad. Sci. USA 102: 15230-15235 [Abstract] [Full Text]  
• Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H., Wieschaus, E. F. (2005). folded gastrulation, cell shape change and the control of myosin localization. Development 132: 4165-4178 [Abstract] [Full Text]  
• von Stein, W., Ramrath, A., Grimm, A., Muller-Borg, M., Wodarz, A. (2005). Direct association of Bazooka/PAR-3 with the lipid phosphatase PTEN reveals a link between the PAR/aPKC complex and phosphoinositide signaling. Development 132: 1675-1686 [Abstract] [Full Text]  
• Harris, T. J.C., Peifer, M. (2004). Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. JCB 167: 135-147 [Abstract] [Full Text]  
• Sotillos, S., Diaz-Meco, M. T., Caminero, E., Moscat, J., Campuzano, S. (2004). DaPKC-dependent phosphorylation of Crumbs is required for epithelial cell polarity in Drosophila. JCB 166: 549-557 [Abstract] [Full Text]  
• Lecuit, T. (2004). Junctions and vesicular trafficking during Drosophila cellularization. J. Cell Sci. 117: 3427-3433 [Abstract] [Full Text]  
• Schumacher, S., Gryzik, T., Tannebaum, S., Muller, H.-A. J. (2004). The RhoGEF Pebble is required for cell shape changes during cell migration triggered by the Drosophila FGF receptor Heartless. Development 131: 2631-2640 [Abstract] [Full Text]  
• Straight, S. W., Shin, K., Fogg, V. C., Fan, S., Liu, C.-J., Roh, M., Margolis, B. (2004). Loss of PALS1 Expression Leads to Tight Junction and Polarity Defects. Mol. Biol. Cell 15: 1981-1990 [Abstract] [Full Text]  
• Rolls, M. M., Albertson, R., Shih, H.-P., Lee, C.-Y., Doe, C. Q. (2003). Drosophila aPKC regulates cell polarity and cell proliferation in neuroblasts and epithelia. JCB 163: 1089-1098 [Abstract] [Full Text]  
• Nance, J., Munro, E. M., Priess, J. R. (2003). C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130: 5339-5350 [Abstract] [Full Text]  
• Pagliarini, R. A., Xu, T. (2003). A Genetic Screen in Drosophila for Metastatic Behavior. Science 302: 1227-1231 [Abstract] [Full Text]  
• Hong, Y., Ackerman, L., Jan, L. Y., Jan, Y.-N. (2003). Distinct roles of Bazooka and Stardust in the specification of Drosophila photoreceptor membrane architecture. Proc. Natl. Acad. Sci. USA 100: 12712-12717 [Abstract] [Full Text]  
• Nam, S.-C., Choi, K.-W. (2003). Interaction of Par-6 and Crumbs complexes is essential for photoreceptor morphogenesis in Drosophila. Development 130: 4363-4372 [Abstract] [Full Text]  
• Roh, M. H., Margolis, B. (2003). Composition and function of PDZ protein complexes during cell polarization. Am. J. Physiol. Renal Physiol. 285: F377-F387 [Abstract] [Full Text]  
• Doerflinger, H., Benton, R., Shulman, J. M., Johnston, D. S. (2003). The role of PAR-1 in regulating the polarised microtubule cytoskeleton in the Drosophila follicular epithelium. Development 130: 3965-3975 [Abstract] [Full Text]  
• Geldmacher-Voss, B., Reugels, A. M., Pauls, S., Campos-Ortega, J. A. (2003). A 90{degrees} rotation of the mitotic spindle changes the orientation of mitoses of zebrafish neuroepithelial cells. Development 130: 3767-3780 [Abstract] [Full Text]  
• Medina, E., Williams, J., Klipfell, E., Zarnescu, D., Thomas, G., Le Bivic, A. (2002). Crumbs interacts with moesin and {beta}Heavy-spectrin in the apical membrane skeleton of Drosophila. JCB 158: 941-951 [Abstract] [Full Text]  
• Roh, M. H., Makarova, O., Liu, C.-J., Shin, , Lee, S., Laurinec, S., Goyal, M., Wiggins, R., Margolis, B. (2002). The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. JCB 157: 161-172 [Abstract] [Full Text]  
• Cox, D. N., Seyfried, S. A., Jan, L. Y., Jan, Y. N. (2001). Bazooka and atypical protein kinase C are required to regulate oocyte differentiation in the Drosophila ovary. Proc. Natl. Acad. Sci. USA 98: 14475-14480 [Abstract] [Full Text]  
• Tolwinski, N. S., Wieschaus, E. (2001). Armadillo nuclear import is regulated by cytoplasmic anchor Axin and nuclear anchor dTCF/Pan. Development 128: 2107-2117 [Abstract] [Full Text]  
• Tang, A., Neufeld, T., Rubin, G., Muller, H. (2001). Transcriptional regulation of cytoskeletal functions and segmentation by a novel maternal pair-rule gene, lilliputian. Development 128: 801-813 [Abstract]  
• Oda, H, Tsukita, S (2001). Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114: 493-501 [Abstract]  
• Tanentzapf, G., Smith, C., McGlade, J., Tepass, U. (2000). Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis. JCB 151: 891-904 [Abstract] [Full Text]  
• Wodarz, A., Ramrath, A., Grimm, A., Knust, E. (2000). Drosophila Atypical Protein Kinase C Associates with Bazooka and Controls Polarity of Epithelia and Neuroblasts. JCB 150: 1361-1374 [Abstract] [Full Text]  
• Lecuit, T., Wieschaus, E. (2000). Polarized Insertion of New Membrane from a Cytoplasmic Reservoir during Cleavage of the Drosophila Embryo. JCB 150: 849-860 [Abstract] [Full Text]  
• Cox, R. T., McEwen, D. G., Myster, D. L., Duronio, R. J., Loureiro, J., Peifer, M. (2000). A Screen for Mutations That Suppress the Phenotype of Drosophila armadillo, the {beta}-Catenin Homolog. Genetics 155: 1725-1740 [Abstract] [Full Text]  
• Hunter, C., Wieschaus, E. (2000). Regulated Expression of nullo Is Required for the Formation of Distinct Apical and Basal Adherens Junctions in the Drosophila Blastoderm. JCB 150: 391-402 [Abstract] [Full Text]  
• Gumbiner, B. M. (2000). Regulation of Cadherin Adhesive Activity. JCB 148: 399-404 [Full Text]  
• Nakaya, M, Fukui, A, Izumi, Y, Akimoto, K, Asashima, M, Ohno, S (2000). Meiotic maturation induces animal-vegetal asymmetric distribution of aPKC and ASIP/PAR-3 in Xenopus oocytes. Development 127: 5021-5031 [Abstract]  
• Akiyama-Oda, Y, Hotta, Y, Tsukita, S, Oda, H (2000). Mechanism of glia-neuron cell-fate switch in the Drosophila thoracic neuroblast 6-4 lineage. Development 127: 3513-3522 [Abstract]  
• Fremion, F., Astier, M., Zaffran, S., Guillen, A., Homburger, V., Semeriva, M. (1999). The Heterotrimeric Protein Go Is Required for the Formation of Heart Epithelium in Drosophila. JCB 145: 1063-1076 [Abstract] [Full Text]  
• Montesano, R., Soriano, J. V., Hosseini, G., Pepper, M. S., Schramek, H. (1999). Constitutively Active Mitogen-activated Protein Kinase Kinase MEK1 Disrupts Morphogenesis and Induces an Invasive Phenotype in Madin-Darby Canine Kidney Epithelial Cells. Cell Growth Differ. 10: 317-332 [Abstract] [Full Text]  
• Thomas, G., Williams, J. (1999). Dynamic rearrangement of the spectrin membrane skeleton during the generation of epithelial polarity in Drosophila. J. Cell Sci. 112: 2843-2852 [Abstract]  
• Muller, H, Samanta, R, Wieschaus, E (1999). Wingless signaling in the Drosophila embryo: zygotic requirements and the role of the frizzled genes. Development 126: 577-586 [Abstract]  
• Costa, M., Raich, W., Agbunag, C., Leung, B., Hardin, J., Priess, J. R. (1998). A Putative Catenin-Cadherin System Mediates Morphogenesis of the Caenorhabditis elegans Embryo. JCB 141: 297-308 [Abstract] [Full Text]  
• Thomas, G., Zarnescu, D., Juedes, A., Bales, M., Londergan, A, Korte, C., Kiehart, D. (1998). Drosophila betaHeavy-spectrin is essential for development and contributes to specific cell fates in the eye. Development 125: 2125-2134 [Abstract]  
• Balkovetz, D. F., Pollack, A. L., Mostov, K. E. (1997). Hepatocyte Growth Factor Alters the Polarity of Madin-Darby Canine Kidney Cell Monolayers. J. Biol. Chem. 272: 3471-3477 [Abstract] [Full Text]  
• Vincent, A, Blankenship, J., Wieschaus, E (1997). Integration of the head and trunk segmentation systems controls cephalic furrow formation in Drosophila. Development 124: 3747-3754 [Abstract]  
• Hayashi, S., Rubinfeld, B., Souza, B., Polakis, P., Wieschaus, E., Levine, A. J. (1997). A Drosophila homolog of the tumor suppressor gene adenomatous polyposis coli down-regulates beta -catenin but its zygotic expression is not essential for the regulation of Armadillo. Proc. Natl. Acad. Sci. USA 94: 242-247 [Abstract] [Full Text]  
• Roh, M. H., Makarova, O., Liu, C.-J., Shin, , Lee, S., Laurinec, S., Goyal, M., Wiggins, R., Margolis, B. (2002). The Maguk protein, Pals1, functions as an adapter, linking mammalian homologues of Crumbs and Discs Lost. JCB 157: 161-172 [Abstract] [Full Text]  
• Hunter, C., Sung, P., Schejter, E. D., Wieschaus, E. (2002). Conserved Domains of the Nullo Protein Required for Cell-Surface Localization and Formation of Adherens Junctions. Mol. Biol. Cell 13: 146-157 [Abstract] [Full Text]  

Home | Help | Feedback | Subscriptions | Archive | Search | Table of Contents