Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis
Open accessAbstract
Analysis of the mechanisms that control epithelial polarization has revealed that cues for polarization are mediated by transmembrane proteins that operate at the apical, lateral, or basal surface of epithelial cells. Whereas for any given epithelial cell type only one or two polarization systems have been identified to date, we report here that the follicular epithelium in Drosophila ovaries uses three different polarization mechanisms, each operating at one of the three main epithelial surface domains. The follicular epithelium arises through a mesenchymal–epithelial transition. Contact with the basement membrane provides an initial polarization cue that leads to the formation of a basal membrane domain. Moreover, we use mosaic analysis to show that Crumbs (Crb) is required for the formation and maintenance of the follicular epithelium. Crb localizes to the apical membrane of follicle cells that is in contact with germline cells. Contact to the germline is required for the accumulation of Crb in follicle cells. Discs Lost (Dlt), a cytoplasmic PDZ domain protein that was shown to interact with the cytoplasmic tail of Crb, overlaps precisely in its distribution with Crb, as shown by immunoelectron microscopy. Crb localization depends on Dlt, whereas Dlt uses Crb-dependent and -independent mechanisms for apical targeting. Finally, we show that the cadherin–catenin complex is not required for the formation of the follicular epithelium, but only for its maintenance. Loss of cadherin-based adherens junctions caused by armadillo (β-catenin) mutations results in a disruption of the lateral spectrin and actin cytoskeleton. Also Crb and the apical spectrin cytoskeleton are lost from armadillo mutant follicle cells. Together with previous data showing that Crb is required for the formation of a zonula adherens, these findings indicate a mutual dependency of apical and lateral polarization mechanisms.
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Experiments in Drosophila have shown that mutations in junctional proteins affect junction formation and disturb epithelial polarity, and polarity mutants affect junction formation.
“Indeed, experiments in Drosophila have shown that mutations in junctional proteins not only affect junction formation but also disturb epithelial polarity, whereas polarity mutants have a profound effect on junction formation as well (Cox et al, 1996;Muller and Wieschaus, 1996;Tanentzapf et al, 2000).”
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Müller, H. A., & Wieschaus, E. (1996) · The Journal of cell biology · doi:10.1083/jcb.134.1.149 · Cited by 384 · see citing works
Cox, R. T., Kirkpatrick, C., & Peifer, M. (1996) · The Journal of cell biology · doi:10.1083/jcb.134.1.133 · Cited by 300 · cited 5× · see citing works
“Embryos mutant for the intermediate allele armXP33 show a dramatic and rapid collapse of the ectodermal epithelium at gastrulation after the blastoderm epithelium has been established (Cox et al., 1996; Müller and Wieschaus, 1996).”
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Research works printed but not linked: 67
- Baumgartner S. Littleton J.T. Broadie K. Bhat M.A. Harbecke R. Lengyel J.A. Chiquet-Ehrismann R. Prokop A. Bellen H.J. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function Cell. 87 1996 1059 1068 8978610
- Bhat M.A. Izaddoost S. Lu Y. Cho K.O. Choi K.W. Bellen H. Discs Lost, a novel multi-PDZ domain protein, establishes and maintains epithelial polarity Cell. 96 1999 633 645 10102271
- Bilder D. Li M. Perrimon N. Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors Science. 289 2000 113 116 10884224
- Brook W.J. Ostafichuk L.M. Piorecky J. Wilkinson M.D. Hodgetts D.J. Russell M.A. Gene expression during imaginal disc regeneration detected using enhancer-sensitive P-elements Development (Camb.). 117 1993 1287 1297 8404531
- Byers T.J. Dubreuil R. Branton D. Kiehart D.P. Goldstein L.S. Drosophila spectrin. II. Conserved features of the α-subunit are revealed by analysis of cDNA clones and fusion proteins J. Cell Biol 105 1987 2103 2110 2824526 PMC2114868
- Cooley L. Theurkauf W.E. Cytoskeletal functions during Drosophila oogenesis Science. 266 1994 590 596 7939713
- Costa M. Raich W. Agbunag C. Leung B. Hardin J. Priess J.R. A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo J. Cell Biol 141 1998 297 308 9531567 PMC2132712
- De Lorenzo C. Strand D. Mechler B.M. Requirement of Drosophila l(2)gl function for survival of the germline cells and organization of the follicle cells in a columnar epithelium during oogenesis Int. J. Dev. Biol. 43 1999 207 217 10410900
- den Hollander A.I. ten Brink J.B. de Kok Y.J. van Soest S. van den Born L.I. van Driel M.A. van de Pol D.J. Payne A.M. Bhattacharya S.S. Kellner U. Mutations in a human homologue of Drosophila Crb cause retinitis pigmentosa (RP12) Nat. Genet. 23 1999 217 221 10508521
- Detrick R.J. Dickey D. Kintner C.R. The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos Neuron. 4 1990 493 506 2322458
- Drubin D.G. Nelson W.J. Origins of Cell Polarity Cell. 84 1996 335 344 8608587
- Duffy J.B. Harrison D.A. Perrimon N. Identifying loci required for follicular patterning using directed mosaics Development (Camb.). 125 1998 2263 2271 9584125
- Eaton S. Simons K. Apical, basal, and lateral cues for epithelial polarization Cell 82 1995 5 8 7606785
- Fujimori T. Miyatani S. Takeichi M. Ectopic expression of N-cadherin perturbs histogenesis in Xenopus embryos Development (Camb.). 110 1990 97 104 2081473
- Godt D. Laski F.A. Mechanisms of cell rearrangement and cell recruitment in Drosophila ovary morphogenesis and the requirement of bric a brac Development (Camb.). 121 1995 173 187 7867498
- Godt D. Tepass U. Drosophila oocyte localization is mediated by differential cadherin-based adhesion Nature. 395 1998 387 391 9759729
- Golic K.G. Site-specific recombination between homologous chromosomes in Drosophila Science. 252 1991 958 961 2035025
- Goode S. Perrimon N. Inhibition of patterned cell shape change and cell invasion by Discs large during Drosophila oogenesis Genes Dev. 11 1997 2532 2544 9334318 PMC316565
- Goode S. Wright D. Mahowald A.P. The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity Development (Camb.). 116 1992 177 192 1483386
- Goode S. Morgan M. Liang Y.P. Mahowald A.P. Brainiac encodes a novel, putative secreted protein that cooperates with Grk TGF alpha in the genesis of the follicular epithelium Dev. Biol. 178 1996 35 50a 8812107
- Goode S. Melnick M. Chou T.B. Perrimon N. The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis Development (Camb.). 122 1996 3863 3879b 9012507
- Grawe F. Wodarz A. Lee B. Knust E. Skaer H. The Drosophila genes crumbs and stardust are involved in the biogenesis of adherens junctions Development (Camb.). 122 1996 951 959 8631272
- Haag T.A. Haag N.P. Lekven A.C. Hartenstein V. The role of cell adhesion molecules in Drosophila heart morphogenesisfaint sausage, shotgun/DE-cadherin, and laminin A are required for discrete stages in heart development Dev. Biol 208 1999 56 69 10075841
- Huelsken J. Vogel R. Brinkmann V. Erdmann B. Birchmeier C. Birchmeier W. Requirement for β-catenin in anterior-posterior axis formation in mice J. Cell Biol 148 2000 567 578 10662781 PMC2174807
- Ito K. Awano W. Suzuki K. Hiromi Y. Yamamoto D. The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells Development (Camb.). 124 1997 761 771 9043058
- Iwai Y. Usui T. Hirano S. Steward R. Takeichi M. Uemura T. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS Neuron 19 1997 77 89 9247265
- King, R.C. 1970. Ovarian Development in Drosophila melanogaster. Academic Press, New York, NY.
- Klebes A. Knust E. A conserved motif in crumbs is required for E-cadherin localization and zonula adherens formation in Drosophila Curr. Biol 10 2000 76 85 10662667
- Lee J.K. Brandin E. Branton D. Goldstein L.S. α-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster Development (Camb.). 124 1997 353 362 9053311
- Lehmann R. Nusslein-Volhard C. Abdominal segmentation, pole cell formation, and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila Cell. 47 1986 141 152 3093084
- Mahowald A.P. Ultrastructural observations on oogenesis in Drosophila J. Morphol. 137 1972 29 48 4338127
- Manfruelli P. Arquier N. Hanratty W.P. Semeriva M. The tumor suppressor gene, lethal(2)giant larvae (1(2)g1), is required for cell shape change of epithelial cells during Drosophila development Development. 122 1996 2283 2294 8681808
- Margolis J. Spradling A. Identification and behavior of epithelial stem cells in the Drosophila ovary Development (Camb.). 121 1995 3797 3807 8582289
- Müller H.A. Genetic control of epithelial cell polaritylessons from Drosophila Dev. Dyn 218 2000 52 67 10822259
- Müller H.A. Hausen P. Epithelial cell polarity in early Xenopus development Dev. Dyn 202 1995 405 420 7626797
- Niewiadomska P. Godt D. Tepass U. DE-cadherin is required for intercellular motility during Drosophila oogenesis J. Cell Biol. 144 1999 533 547 9971747 PMC2132905
- Nelson S.H. McClay D.R. Cell polarity in sea urchin embryosreorientation of cells occurs quickly in aggregates Dev. Biol. 127 1988 235 247 3288526
- Oda H. Uemura T. Shiomi K. Nagafuchi A. Tsukita S. Takeichi M. Identification of a Drosophila homologue of α-catenin and its association with the Armadillo protein J. Cell Biol. 121 1993 1133 1140 8501118 PMC2119693
- Oda H. Uemura T. Harada Y. Iwai Y. Takeichi M. A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion Dev. Biol. 165 1994 716 726 7958432
- Oda H. Uemura T. Takeichi M. Phenotypic analysis of null mutants of DE-cadherin and Armadillo in Drosophila ovaries reveals distinct aspects of their functions in cell adhesion and cytoskeletal organization Genes to Cells 2 1997 29 40 9112438
- Ojakian G.K. Schwimmer R. The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells J. Cell Biol 107 1988 2377 2387 3198692 PMC2115640
- Patel N.H. Snow P.M. Goodman C.S. Characterization and cloning of fasciclin IIIa glycoprotein expressed on a subset of neurons and axon pathways in Drosophila Cell. 48 1987 975 988 3548998
- Peifer M. The product of the Drosophila segment polarity gene armadillo is part of a protein complex resembling the vertebrate adherens junction J. Cell Sci. 105 1993 993 1000 8227220
- Peifer M. Wieschaus E. The segment polarity gene armadillo encodes a functionally modular protein that is the Drosophila homolog of human plakoglobin Cell. 63 1990 1167 1176 2261639
- Peifer M. Orsulic S. Sweeton D. Wieschaus E. A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis Development (Camb.). 118 1993 681 691 8269848
- Raich W.B. Agbunag C. Hardin J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming Curr. Biol 9 1999 1139 1146 10531027
- Reeve W.J. Ziomek C.A. Distribution of microvilli on dissociated blastomeres from mouse embryosevidence for surface polarization at compaction J Embryol. Exp. Morphol 62 1981 339 350 7276817
- Riggleman B. Schedl P. Wieschaus E. Spatial expression of the Drosophila segment polarity gene armadillo is posttranscriptionally regulated by wingless Cell. 63 1990 549 560 2225066
- Spradling A.C. Developmental genetics of oogenesis Bate M. Martinez-Arias A. The Development of Drosophila melanogaster 1993 1 70 Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York
- Tepass U. Crumbs, a component of the apical membrane, is required for zonula adherens formation in primary epithelia of Drosophila Dev. Biol. 177 1996 217 225 8660889
- Tepass U. Epithelial differentiation in Drosophila Bioessays. 19 1997 673 682 9264249
- Tepass U. Knust E. Phenotypic and developmental analysis of mutations at the crumbs locus, a gene required for the development of epithelia in Drosophila melanogaster Roux's Arch. Dev. Biol. 199 1990 189 206 28306104
- Tepass U. Hartenstein V. Development of intercellular junctions in the Drosophila embryo Dev. Biol. 161 1994 563 596a 8314002
- Tepass U. Hartenstein V. Epithelium formation of the Drosophila midgut depends on interactions between endoderm and mesoderm Development 120 1994 579 590b 8162857
- Tepass U. Theres C. Knust E. crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia Cell 61 1990 787 799 2344615
- Tepass U. Gruszynski de Feo E. Haag T.A. Omatyar L. Török T. Hartenstein V. shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neuroectoderm and other morphogenetically active epithelia Genes Dev 10 1996 672 685 8598295
- Thomas G.H. Kiehart D.P. βHeavy-Spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis Development (Camb.). 120 1994 2039 2050 7925008
- Thomas G.H. Zarnescu D.C. Juedes A.E. Bales M.A. Londergan A. Korte C.C. Kiehart D.P. Drosophila βHeavy-spectrin is essential for development and contributes to specific cell fates in the eye Development (Camb.) 125 1998 2125 2134 9570776
- Uemura T. Oda H. Kraut R. Hayashi S. Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo Genes Dev 10 1996 659 671 8598294
- Vega-Salas D.E. Salas P.J. Gundersen D. Rodriguez-Boulan E. Formation of the apical pole of epithelial (Madin-Darby canine kidney) cellspolarity of an apical protein is independent of tight junctions while segregation of a basolateral marker requires cell–cell interactions J. Cell Biol 104 1987 905 916 3558485 PMC2114453
- Wodarz A. Grawe F. Knust E. CRUMBS is involved in the control of apical protein targeting during Drosophila epithelial development Mech. Dev. 44 1993 175 187 8155580
- Wodarz A. Hinz U. Engelbert M. Knust E. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila Cell. 82 1995 67 76 7606787
- Woodruff R.I. Tilney L.G. Intercellular bridges between epithelial cells in the Drosophila ovarian folliclea possible aid to localized signaling Dev. Biol. 200 1998 82 91 9698458
- Xu T. Harrison S.D. Mosaic analysis using FLP recombinase Goldstein L.S.B. Fyrberg E.A. Drosophila melanogaster: Practical Uses in Cell and Molecular Biology 1994 655 682 Academic Press San Diego, CA 7707974
- Yarnitzky T. Volk T. Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo Dev. Biol 169 1995 609 618 7781902
- Yeaman C. Grindstaff K.K. Nelson W.J. New perspectives on mechanisms involved in generating epithelial cell polarity Physiol. Rev. 79 1999 73 98 9922368
- Zarnescu D.C. Thomas G.H. Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila J. Cell Biol. 146 1999 1075 1086 10477760 PMC2169487
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- Authors
- Tanentzapf, G., Smith, C., McGlade, J., & Tepass, U.
- Affiliations
- University of Toronto (CA)
- Venue
- The Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2000-11-13
- Volume
- 151
- Issue
- 4
- Pages
- 891-904
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2169434
- OpenAlex
- W2078657639
- Cited by
- 199
- References
- 2
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 3 · 2023: 4 · 2022: 7 · 2021: 3 · 2020: 6 · 2019: 11 · 2018: 2 · 2017: 5 · 2016: 4 · 2015: 15 · 2014: 10 · 2013: 7 · 2012: 14
- FWCI
- 3.98
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Hippo pathway signaling and YAP/TAZ
- Keywords
- epithelial polarization, follicular epithelium, Drosophila oogenesis, Crumbs, mesenchymal-epithelial transition, basement membrane, apical membrane, spectrin cytoskeleton, adherens junctions, cadherin-catenin complex, armadillos, mosaic analysis
- MeSH terms
- Amino Acid Sequence, Animals, Cell Differentiation, Drosophila melanogaster, Epithelial Cells, Female, Ovarian Follicle, Membrane Proteins, Mesoderm, Molecular Sequence Data, Oogenesis, Cell Polarity, Insect Proteins, Drosophila Proteins
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