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JOURNAL ARTICLES
A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis
M. Peifer, S. Orsulic, D. Sweeton, E. Wieschaus
Development 1993 118: 1191-1207;

Summary

The epithelial sheet is a structural unit common to many tissues. Its organization appears to depend on the function of the multi-protein complexes that form adherens junctions. Elegant cell biological experiments have provided support for hypotheses explaining the function of adherens junctions and of their components. These systems, however, lack the ability to test function within an entire organism during development. The realization that the product of the Drosophila segment polarity gene armadillo is related to the vertebrate adhesive junction components plakoglobin and beta-catenin led to the suggestion that armadillo might provide a genetic handle to study adhesive junction structure and function. An examination of the potential function of Armadillo in cell-cell adhesive junctions was initiated using the Drosophila ovary as the model system. We examined the distribution of Armadillo in the Drosophila ovary and demonstrated that this localization often parallels the location of cell-cell adhesive junctions. The consequences of removing armadillo function from the germ-line cells of the ovary were also examined. Germ-line armadillo mutations appear to disrupt processes requiring cell adhesion and integrity of the actin cytoskeleton, consistent with a role for Armadillo in cell-cell adhesive junctions. We have also used armadillo mutations to examine the effects on ovarian development of altering the stereotyped cell arrangements of the ovary. The implications of these results for the role of adhesive junctions during development are discussed.

Reference

    1. Baker N. E.
    (1988) Embryonic and imaginal requirements for wingless, a segment polarity gene in Drosophila. Dev. Biol 125, 96–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Brower D. L.,
    2. Smith R. J.,
    3. Wilcox M.
    (1981) Differentiation within the gonads of Drosophila revealed by immunofluorescence. J. Embryol. Exp. Morph 63, 233–242
    OpenUrlPubMedWeb of Science
    1. Carroll S. B.,
    2. White J. S.
    (1989) The role of the hairy gene during Drosophila morphogenesis: stripes in imaginal discs. Genes Dev 3, 906–916
    OpenUrl
    1. Chou T.-B.,
    2. Perrimon N.
    (1992) Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643–653
    OpenUrlAbstract/FREE Full Text
    1. Cooley L.,
    2. Verheyen E.,
    3. Ayers K.
    (1992) chickadee encodes a profilin required for intracellular cytoplasm transport during Drosophila oogenesis. Cell 69, 173–184
    OpenUrlCrossRefPubMedWeb of Science
    1. Cowin P.,
    2. Kapprell H.-P.,
    3. Franke W. W.,
    4. Tamkun J.,
    5. Hynes R. O.
    (1986) Plakoglobin: A protein common to different kinds of intercellular junctions. Cell 46, 1063–1073
    OpenUrlCrossRefPubMedWeb of Science
    1. Ephrussi A.,
    2. Dickinson L. K.,
    3. Lehmann R.
    (1991) oskar RNA organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37–50
    OpenUrlCrossRefPubMedWeb of Science
    1. Franke W. W.,
    2. Kapprell H.-P.,
    3. Cowin P.
    (1987) Plakoglobin is a component of the subplasmalemmal coat of lens cells. Eur. J. Cell Biol 43, 301–315
    OpenUrlPubMedWeb of Science
    1. Franke W. W.,
    2. Goldschmidt M. D.,
    3. Zimbelmann R.,
    4. Mueller H. M.,
    5. Schiller D. L.,
    6. Cowin P.
    (1989) Molecular cloning and amino acid sequence of human plakoglobin, the common junctional plaque protein. Proc. Nat. Acad. Sci. USA 86, 4027–4031
    OpenUrlAbstract/FREE Full Text
    1. Golic K. G.
    (1991) Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958–961
    OpenUrlAbstract/FREE Full Text
    1. Herrenknecht K.,
    2. Ozawa M.,
    3. Eckerskorn C.,
    4. Lottspeich F.,
    5. Kemler R.
    (1991) The uvomorulin-anchorage protein-catenin is a vinculin homologue. Proc. Nat. Acad. Sci. USA 88, 9156–9160
    OpenUrlAbstract/FREE Full Text
    1. Hirano S.,
    2. Kimoto N.,
    3. Shimoyama Y.,
    4. Hirohashi S.,
    5. Takeichi M.
    (1992) Identification of a neural-catenin as a key regulator of cadherin function and multicellular organization. Cell 70, 293–301
    OpenUrlCrossRefPubMedWeb of Science
    1. Ingham P. W.,
    2. Martinez-Arias A.
    (1992) Boundaries and fields in early embryos. Cell 68, 221–235
    OpenUrlCrossRefPubMedWeb of Science
    1. Kemler R.,
    2. Ozawa M.
    (1989) Uvomorulin-catenin complex: Cytoplasmic anchorage of a Ca2+ -dependent cell adhesion molecule. Bioessays 11, 88–91
    OpenUrlCrossRefPubMedWeb of Science
    1. Kim-Ha J.,
    2. Smith J. L.,
    3. Macdonald P. M.
    (1991) oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23–35
    OpenUrlCrossRefPubMedWeb of Science
    1. Klingensmith J.,
    2. Noll E.,
    3. Perrimon N.
    (1989) The segment polarity phenotype of Drosophila involves differential tendencies toward transformation and cell death. Dev. Biol 134, 130–145
    OpenUrlCrossRefPubMedWeb of Science
    1. Knudsen K. A.,
    2. Wheelock M. J.
    (1992) Plakoglobin, or an 83 kD homologue distinct from-catenin, interacts with E-cadherin and N-cadherin. J. Cell Biol 118, 671–679
    OpenUrlAbstract/FREE Full Text
    1. Lantz V.,
    2. Ambrosio L.,
    3. Schedl P.
    (1992) The Drosophila orb gene is predicted to encode sex-specific germline RNA-binding proteins and has localized transcripts in ovaries and early embryos. Development 115, 78–88
    OpenUrl
    1. Magee A. I.,
    2. Buxton R. S.
    (1991) Transmembrane molecular assemblies regulated by the greater cadherin family. Curr. Opin. in Cell Biol 3, 854–861
    OpenUrlCrossRefPubMed
    1. Manseau L.,
    2. Schupbach T.
    (1989) The egg came first of course. Trends Genet 5, 400–405
    OpenUrlCrossRefPubMedWeb of Science
    1. McCrea P.,
    2. Turck C.,
    3. Gumbiner B.
    (1991) A homolog of Drosophila armadillo (plakoglobin) associated with the cytoplasmic tail of E-cadherin. Science 25, 1359–1361
    OpenUrl
    1. McNeill H.,
    2. Ozawa M.,
    3. Kemler R.,
    4. Nelson W. J.
    (1990) Novel function of the cell adhesion molecule uvomorulin as an inducer of cell surface polarity. Cell 62, 309–316
    OpenUrlCrossRefPubMedWeb of Science
    1. Miller K. G.,
    2. Field C. M.,
    3. Alberts B. M.
    (1989) Actin-binding proteins from Drosophila embryos: a complex network of interacting proteins detected by F-actin affinity chromatagraphy. J. Cell Biol 109, 2963–2975
    OpenUrlAbstract/FREE Full Text
    1. Nagafuchi A.,
    2. Takeichi M.
    (1989) Transmembrane control of cadherin-mediated cell adhesion: a 94 kDa protein functionally associated with a specific region of the cytoplasmic domain of E-cadherin. Cell Regulation 1, 37–44
    OpenUrlPubMedWeb of Science
    1. Nagafuchi A.,
    2. Shirayoshi Y.,
    3. Okazaki K.,
    4. Yasuda K.,
    5. Takeichi M.
    (1987) Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 329, 341–343
    OpenUrlCrossRefPubMed
    1. Nagafuchi A.,
    2. Takeichi M.,
    3. Tsukita S.
    (1991) The 102 kd cadherin-associated protein: similarity to vinculin and post-transcriptional regulation of expression. Cell 65, 849–857
    OpenUrlCrossRefPubMedWeb of Science
    1. Nose A.,
    2. Nagafuchi A.,
    3. Takeichi M.
    (1988) Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993–1001
    OpenUrlCrossRefPubMedWeb of Science
    1. Nusslein-Volhard C.,
    2. Frohnhöfer H.G.,
    3. Lehmann R.
    (1987) Determination of anterior-posterior polarity in Drosophila. Science 238, 1675–1681
    OpenUrlAbstract/FREE Full Text
    1. Ozawa M.,
    2. Baribault H.,
    3. Kemler R.
    (1989) The cytoplasmic domain of the cell adhesion molecule uvomorulin associates with three independent proteins structurally related in different species. EMBO J 8, 1711–1717
    OpenUrlPubMedWeb of Science
    1. Ozawa M.,
    2. Ringwald M.,
    3. Kemler R.
    (1990) Uvomorulin-catenin complex formation is regulated by a specific domain in the cytoplasmic region of the cell adhesion molecule. Proc. Nat. Acad. Sci USA 87, 4246–4250
    OpenUrlAbstract/FREE Full Text
    1. Peifer M.,
    2. Wieschaus E.
    (1990) The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin. Cell 63, 1167–1178
    OpenUrlCrossRefPubMedWeb of Science
    1. Peifer M.,
    2. Rauskolb C.,
    3. Williams M.,
    4. Riggleman B.,
    5. Wieschaus E.
    (1991) The segment polarity gene armadillo affects the wingless signaling pathway in both embryonic and adult pattern formation. Development 111, 1028–1043
    OpenUrl
    1. Peifer M.,
    2. McCrea P. D.,
    3. Green K. J.,
    4. Wieschaus E.,
    5. Gumbiner B. M.
    (1992) The vertebrate adhesive junction proteins-catenin and plakoglobin and the Drosophila segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol 118, 681–691
    OpenUrlAbstract/FREE Full Text
    1. Riggleman B.,
    2. Schedl P.,
    3. Wieschaus E.
    (1990) Spatial expression of the Drosophila segment polarity gene armadillo is post-transcriptionally regulated by wingless. Cell 63, 549–560
    OpenUrlCrossRefPubMedWeb of Science
    1. Ruohola H.,
    2. Bremer K. A.,
    3. Baker D.,
    4. Swedlow J. R.,
    5. Jan L. Y.,
    6. Jan Y. N.
    (1991) Role of the neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66, 433–449
    OpenUrlCrossRefPubMedWeb of Science
    1. Salomon D.,
    2. Ayalon O.,
    3. Patel-King R.,
    4. Hynes R. O.,
    5. Geiger B.
    (1992) Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci 102, 7–17
    OpenUrlAbstract/FREE Full Text
    1. Schupbach T.,
    2. Wieschaus E.
    (1991) Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129, 1119–1136
    OpenUrlAbstract/FREE Full Text
    1. Stevens L. M.,
    2. Frohhöfer H. G.,
    3. Klingler M.,
    4. Nusslein-Volhard C.
    (1990) Localized requirement for torso-like expression in follicle cells for development of terminal anlagen of the Drosophila embryo. Nature 346, 660–663
    OpenUrlCrossRefPubMed
    1. Suter B.,
    2. Steward R.
    (1991) The role of the Bicaudal-D protein and its phosphorylation in Drosophila oocyte differentiation. Cell 67, 917–926
    OpenUrlCrossRefPubMedWeb of Science
    1. Takeichi M.
    (1991) Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451–1455
    OpenUrlAbstract/FREE Full Text
    1. Tautz D.,
    2. Pfeifle C.
    (1989) A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98, 81–85
    OpenUrlCrossRefPubMedWeb of Science
    1. Zusman S.,
    2. Coulter D.,
    3. Gergen J. P.
    (1985) Lethal mutations induced in the proximal X-chromosome of Drosophila melanogaster using P-M hybrid dysgenesis. Dros. Inf. Serv 61, 217–218
    OpenUrl
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JOURNAL ARTICLES
A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis
M. Peifer, S. Orsulic, D. Sweeton, E. Wieschaus
Development 1993 118: 1191-1207;
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