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Published online 13 November 2000. doi:10.1083/jcb.151.4.891
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© The Rockefeller University Press, 0021-9525/2000//891 $5.00
The Journal of Cell Biology, Volume 151, Number 4, , 2000 891-904

Original Article

Apical, Lateral, and Basal Polarization Cues Contribute to the Development of the Follicular Epithelium during Drosophila Oogenesis



Guy Tanentzapfa, Christian Smithb, Jane McGladeb, and Ulrich Tepassa

a Department of Zoology, University of Toronto, Toronto, Ontario, Canada M5S 3G5
b The Hospital of Sick Children, Arthur and Sonia Labatt Brain Tumor Research Center, and Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada M5G 1X8
Department of Zoology, University of Toronto, 25 Harbord Street, Toronto, ON, M5S 3G5.(416) 978-8532(416) 978-5712

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.

Key Words: epithelial polarity • follicular epithelium • Crumbs • Discs Lost • Armadillo

© 2000 The Rockefeller University Press

Abbreviations used in this paper: Arm, Armadillo; Crb, Crumbs; Dlt, Discs Lost; FE, follicular epithelium; IEM, immunoelectron microscopy; ZA, zonula adherens.


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