Abstract
ABSTRACT Morphogenetic movements of epithelia during development underlie the normal elaboration of the final body plan. The tissue integrity critical for these movements is conferred by anchorage of the cytoskeleton to the membrane at sites of cell adhesion, mediated by adherens junctions, initially spot and later belt-like, zonular structures, which encircle the apical side of the cell. Loss-offunction mutations in the Drosophila genes crumbs and stardust lead to the loss of cell polarity in most ectodermally derived epithelia, followed in some, such as the epidermis, by extensive apoptosis. Here we show that both mutants fail to establish proper zonulae adherentes in the epidermis. Our results suggest that the two genes are involved in different aspects of this process. Further, they are compatible with the hypothesis that crumbs delimits the apical border, where the zonula adherens usually forms and where Crumbs protein is normally most abundant. In contrast, stardust seems to be required at an earlier stage for the assembly of the spot adherens junctions. In both mutants, the defects observed at the ultrastructural level are preceded by a misdistribution of Armadillo and DEcadherin, the homologues of β-catenin and E-cadherin, respectively, which are two constituents of the vertebrate adherens junctions. Strikingly, expansion of the apical membrane domain in epidermal cells by overexpression of crumbs also abolishes the formation of adherens junctions and results in the disruption of tissue integrity, but without loss of membrane polarity. This result supports the view that membrane polarity is independent of the formation of adherens junctions in epidermal cells.
References
43
Referenced
151
{'volume-title': 'Drosophila, a Laboratory Handbook', 'year': '1990', 'author': 'Ashburner', 'key': '2025021322382020600_DEVELOP_122_3_951C1'}
/ Drosophila, a Laboratory Handbook by Ashburner (1990)10.1083/jcb.120.3.757
/ J. Cell Biol / Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/ βcatenin complex in cells transformed with a temperature-sensitive v-SRC gene by Behrens (1993)10.1242/dev.118.2.401
/ Development / Targeted gene expression as a means of altering cell fates and generating dominant phenotypes by Brand (1993)10.1016/0012-1606(88)90399-5
/ Dev. Biol / Mutations at the fat locus interfere with cell proliferation control and epithelial morphogenesis in Drosophila by Bryant (1988)10.1016/S0968-0004(00)89057-X
/ Trends Biochem. Sci / Epithelial differentiation in the mouse preimplantation embryo: making adhesive cell contacts for the first time by Collins (1995)10.1007/BF00848457
/ Roux’s Arch. Dev. Biol / Intercellular junctions during development and in tissue cultures of Drosophila melanogaster by Eichenberger-Glinz (1979)10.1016/0092-8674(95)90045-4
/ Cell / Apical, basal and lateral cues for epithelial polarisation by Eaton (1995)10.1007/978-94-011-2354-9_4
/ In Epithelial Organisation and Development / Trophectoderm biogenesis in the preimplantation mouse embryo by Fleming (1992)10.1007/978-94-011-2354-9_1
/ In Epithelial organisation and development / Intercellular junctions and cell adhesion in epithelial cells by Garrod (1992)10.1016/0896-6273(93)90068-3
/ Neuron / Proteins associated with the cytoplasmic surface of adhesion molecules by Gumbiner (1993)10.1016/0092-8674(94)90174-0
/ Cell / The basic-helix-loophelix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes by Hinz (1994)10.1016/0955-0674(94)90125-2
/ Curr. Opinion Cell Biol / Membrane interactions with the actin cytoskeleton by Hitt (1994)10.1083/jcb.127.6.2061
/ J Cell Biol / E-cadherin and APC compete for the interaction with β-catenin and the cytoskeleton by Huelsken (1994)10.1007/978-3-540-35803-9_1
/ In: Drosophila. Genetic mosaics and cell differentiation (Gehring ed / Gynandromorph fate maps by Janning (1978)10.1016/0168-9525(93)90250-L
/ Trends Genet / From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion by Kemler (1993)10.1016/0168-9525(90)90010-4
/ Trends Genet / Control of epithelial development in Drosophila by Knust (1994)10.1073/pnas.91.17.8263
/ Proc. Natl. Acad. Sci. USA / E-cadherin null mutant embryos fail to form a trophectoderm epithelium by Larue (1994)10.1126/science.1439807
/ Science / Cytoskeleton-plasma membrane interactions by Luna (1992)10.1083/jcb.118.3.703
/ J. Cell Biol / Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phophorylation in metastatic fibroblasts by Matsuyoshi (1992)10.1016/0092-8674(90)90368-O
/ Cell / Novel function of cell adhesion molecule uvomorulin as an inducer of cell surface polarity by McNeill (1990)10.1002/aja.1002020410
/ Dev. Dynamics / Epithelial cell polarity in early Xenopus development by Müller (1995)10.1083/jcb.121.5.1133
/ J. Cell Biol / Identification of a Drosophila homologue of α-catenin and its association with the armadillo protein by Oda (1993)10.1006/dbio.1994.1287
/ Dev. Biol / A Drosophila homolog of cadherin associated with Armadillo and essential for embryonic cell-cell adhesion by Oda (1994)10.1242/jcs.105.4.993
/ J. Cell Sci / The product of the segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction by Peifer (1993)10.1016/S0962-8924(00)89015-7
/ Trends Cell Biol / Cell adhesion and signal transduction: the Armadillo connection by Peifer (1995)10.1016/0092-8674(90)90413-9
/ Cell / The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin by Peifer (1990)10.1242/dev.118.4.1191
/ Development / A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis by Peifer (1993)10.1242/dev.120.2.369
/ Development / wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo by Peifer (1994)10.1016/0955-0674(94)90102-3
/ Curr. Opin. Cell Biol / Cadherins and catenins: interactions and functions in embryonic development by Rantsch (1994){'key': '2025021322382020600_DEVELOP_122_3_951C30', 'first-page': '339', 'article-title': 'Distribution of microvilli on dissociated blastomeres from mouse embryos: Evidence for surface polarization at compaction', 'volume': '62', 'author': 'Reeve', 'year': '1981', 'journal-title': 'J. Embryol. Exp. Morph'}
/ J. Embryol. Exp. Morph / Distribution of microvilli on dissociated blastomeres from mouse embryos: Evidence for surface polarization at compaction by Reeve (1981)10.1073/pnas.92.3.855
/ Proc. natl. Acad. Sci. USA / A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development by Riethmacher (1995)10.1126/science.2672330
/ Science / Morphogenesis of the polarized epithelial cell phenotype by Rodriguez-Boulan (1989){'key': '2025021322382020600_DEVELOP_122_3_951C33', 'first-page': '9411012', 'article-title': 'The alimentary canal', 'volume-title': 'In: The development of Drosophila melanogaster', 'author': 'Skaer', 'year': '1993'}
/ In: The development of Drosophila melanogaster / The alimentary canal by Skaer (1993)10.1006/dbio.1994.1054
/ Dev. Biol / The development of cellular junctions in the Drosophila embryo by Tepaß (1994)10.1242/dev.120.3.579
/ Development / The fomation of the midgut epithelium in Drosophila depends on the interaction of endoderm and mesoderm by Tepaß (1994)10.1007/BF01682078
/ Roux’s Arch. Dev. Biol / Phenotypic and developmental analysis of mutations at the crumbs locus, a gene required for the development of epithelia in Drosophila melanogaster by Tepaß (1990)10.1006/dbio.1993.1243
/ Dev. Biol / crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster by Tepaß (1993)10.1016/0092-8674(90)90189-L
/ Cell / crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia by Tepaß (1990){'key': '2025021322382020600_DEVELOP_122_3_951C39', 'article-title': 'Shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphologically active epithelia', 'volume-title': 'Genes Dev. (in press)', 'author': 'Tepaß', 'year': '1996'}
/ Genes Dev. (in press) / Shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphologically active epithelia by Tepaß (1996)10.1002/j.1460-2075.1992.tb05225.x
/ EMBO J / The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions by Volberg (1992)10.1007/BF00444042
/ Roux‘s Arch. Dev. Biol / Specificity of embryonic lethal mutations in Drosophila analysed in germ line clones by Wieschaus (1986)10.1016/0925-4773(93)90066-7
/ Mech. Dev / CRUMBS is involved in the control of apical protein targeting during Drosophila epithelial development by Wodarz (1993)10.1016/0092-8674(95)90053-5
/ Cell / Expression of Crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila by Wodarz (1995)
Dates
Type | When |
---|---|
Created | 4 years, 4 months ago (April 25, 2021, 10:37 p.m.) |
Deposited | 6 months, 2 weeks ago (Feb. 13, 2025, 5:38 p.m.) |
Indexed | 2 months, 1 week ago (June 19, 2025, 7:06 p.m.) |
Issued | 29 years, 5 months ago (March 1, 1996) |
Published | 29 years, 5 months ago (March 1, 1996) |
Published Online | 29 years, 5 months ago (March 1, 1996) |
Published Print | 29 years, 5 months ago (March 1, 1996) |
@article{Grawe_1996, title={The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions}, volume={122}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.122.3.951}, DOI={10.1242/dev.122.3.951}, number={3}, journal={Development}, publisher={The Company of Biologists}, author={Grawe, Ferdi and Wodarz, Andreas and Lee, Bill and Knust, Elisabeth and Skaer, Helen}, year={1996}, month=mar, pages={951–959} }