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Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis.

Tanentzapf G, Smith C, McGlade J, Tepass U - J. Cell Biol. (2000)

Bottom Line: Loss of cadherin-based adherens junctions caused by armadillo (beta-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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Toronto, Toronto, Ontario, Canada M5S 3G5.

ABSTRACT
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 (beta-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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IEM of Dlt in the FE and in embryonic ectoderm and epidermis. (A) Schematic of the apicolateral region of an epithelial cell after the junctional complex composed of a ZA and a septate junction has formed. The marginal zone of the apical membrane domain is an area of cell–cell contact that is found apical to the ZA (Tepass 1996). (B and C) Dlt is found throughout the apical membrane of follicle cells, but is concentrated just apical to the ZA (between arrowheads) in the marginal zone. The higher concentration of Dlt in the marginal zone is particularly apparent when the signal intensity is low as in C, where the signal is confined to the marginal zone. (D, E, and G) Examples of Dlt (D and E) and Crb (G) immunolabeling in ectodermal cells of stage 11 embryos. Labeling for Dlt and Crb are confined to the apical surface and concentrated at the marginal zone immediately apical to the ZA (between arrowheads). (F) Dlt is found apical to the ZA (arrowheads) in stage 16 embryos after the septate junction has formed (arrows). Bars, 100 μm.
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Figure 3: IEM of Dlt in the FE and in embryonic ectoderm and epidermis. (A) Schematic of the apicolateral region of an epithelial cell after the junctional complex composed of a ZA and a septate junction has formed. The marginal zone of the apical membrane domain is an area of cell–cell contact that is found apical to the ZA (Tepass 1996). (B and C) Dlt is found throughout the apical membrane of follicle cells, but is concentrated just apical to the ZA (between arrowheads) in the marginal zone. The higher concentration of Dlt in the marginal zone is particularly apparent when the signal intensity is low as in C, where the signal is confined to the marginal zone. (D, E, and G) Examples of Dlt (D and E) and Crb (G) immunolabeling in ectodermal cells of stage 11 embryos. Labeling for Dlt and Crb are confined to the apical surface and concentrated at the marginal zone immediately apical to the ZA (between arrowheads). (F) Dlt is found apical to the ZA (arrowheads) in stage 16 embryos after the septate junction has formed (arrows). Bars, 100 μm.

Mentions: To clarify the subcellular localization of Dlt, we determined the distribution of Dlt in the FE and in the embryonic ectoderm and epidermis by IEM (Fig. 3). IEM reveals that Dlt, similar to Crb (Tepass 1996), is confined to the apical membrane. Within the apical membrane, Dlt accumulates at the marginal zone, an area of cell–cell contact apical to the ZA, and shows a lower concentration throughout the apical surface (Fig. 3). The signal for Dlt at the ZA or basally to it does not exceed background levels, and no signal is observed at septate junctions (Fig. 3 F). These findings suggest that Dlt does not physically interact with Neurexin IV at the septate junction, and further corroborates the notion that Dlt and Crb form a complex at the apical membrane of epithelial cells.


Apical, lateral, and basal polarization cues contribute to the development of the follicular epithelium during Drosophila oogenesis.

Tanentzapf G, Smith C, McGlade J, Tepass U - J. Cell Biol. (2000)

IEM of Dlt in the FE and in embryonic ectoderm and epidermis. (A) Schematic of the apicolateral region of an epithelial cell after the junctional complex composed of a ZA and a septate junction has formed. The marginal zone of the apical membrane domain is an area of cell–cell contact that is found apical to the ZA (Tepass 1996). (B and C) Dlt is found throughout the apical membrane of follicle cells, but is concentrated just apical to the ZA (between arrowheads) in the marginal zone. The higher concentration of Dlt in the marginal zone is particularly apparent when the signal intensity is low as in C, where the signal is confined to the marginal zone. (D, E, and G) Examples of Dlt (D and E) and Crb (G) immunolabeling in ectodermal cells of stage 11 embryos. Labeling for Dlt and Crb are confined to the apical surface and concentrated at the marginal zone immediately apical to the ZA (between arrowheads). (F) Dlt is found apical to the ZA (arrowheads) in stage 16 embryos after the septate junction has formed (arrows). Bars, 100 μm.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169434&req=5

Figure 3: IEM of Dlt in the FE and in embryonic ectoderm and epidermis. (A) Schematic of the apicolateral region of an epithelial cell after the junctional complex composed of a ZA and a septate junction has formed. The marginal zone of the apical membrane domain is an area of cell–cell contact that is found apical to the ZA (Tepass 1996). (B and C) Dlt is found throughout the apical membrane of follicle cells, but is concentrated just apical to the ZA (between arrowheads) in the marginal zone. The higher concentration of Dlt in the marginal zone is particularly apparent when the signal intensity is low as in C, where the signal is confined to the marginal zone. (D, E, and G) Examples of Dlt (D and E) and Crb (G) immunolabeling in ectodermal cells of stage 11 embryos. Labeling for Dlt and Crb are confined to the apical surface and concentrated at the marginal zone immediately apical to the ZA (between arrowheads). (F) Dlt is found apical to the ZA (arrowheads) in stage 16 embryos after the septate junction has formed (arrows). Bars, 100 μm.
Mentions: To clarify the subcellular localization of Dlt, we determined the distribution of Dlt in the FE and in the embryonic ectoderm and epidermis by IEM (Fig. 3). IEM reveals that Dlt, similar to Crb (Tepass 1996), is confined to the apical membrane. Within the apical membrane, Dlt accumulates at the marginal zone, an area of cell–cell contact apical to the ZA, and shows a lower concentration throughout the apical surface (Fig. 3). The signal for Dlt at the ZA or basally to it does not exceed background levels, and no signal is observed at septate junctions (Fig. 3 F). These findings suggest that Dlt does not physically interact with Neurexin IV at the septate junction, and further corroborates the notion that Dlt and Crb form a complex at the apical membrane of epithelial cells.

Bottom Line: Loss of cadherin-based adherens junctions caused by armadillo (beta-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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Toronto, Toronto, Ontario, Canada M5S 3G5.

ABSTRACT
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 (beta-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.

Show MeSH