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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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Expression of Crb and Dlt in wild-type ovaries. (A) Crb is first detected in follicle cells located between region 2b and the stage 1 follicle that will form the interfollicular stalk (arrow) and in the FE of the stage 1 follicle. Note that interfollicular stalk cells lose Crb rapidly (arrowhead), but that Crb expression is maintained in the FE, where it associates with the apical membrane. (B) Dlt shows the same distribution as Crb in early stages of oogenesis. (C) Expression of Dlt at stage 9 of oogenesis. Dlt is expressed in the FE and the border cells (arrow). In germline cells, Dlt is found at a contact site between nurse cells (arrowheads). (D) Dlt is found at the apical surface of follicle cells, but is absent from the oocyte membrane that is associated with large amounts of F-actin (D′). (D″) A merged image of D and D′. By contrast, Crb strongly accumulates in the oocyte membrane, as was shown previously (Niewiadomska et al. 1999).
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Figure 2: Expression of Crb and Dlt in wild-type ovaries. (A) Crb is first detected in follicle cells located between region 2b and the stage 1 follicle that will form the interfollicular stalk (arrow) and in the FE of the stage 1 follicle. Note that interfollicular stalk cells lose Crb rapidly (arrowhead), but that Crb expression is maintained in the FE, where it associates with the apical membrane. (B) Dlt shows the same distribution as Crb in early stages of oogenesis. (C) Expression of Dlt at stage 9 of oogenesis. Dlt is expressed in the FE and the border cells (arrow). In germline cells, Dlt is found at a contact site between nurse cells (arrowheads). (D) Dlt is found at the apical surface of follicle cells, but is absent from the oocyte membrane that is associated with large amounts of F-actin (D′). (D″) A merged image of D and D′. By contrast, Crb strongly accumulates in the oocyte membrane, as was shown previously (Niewiadomska et al. 1999).

Mentions: Crb is initially expressed in all follicle cells at stage 1 of oogenesis, but its expression becomes rapidly restricted to the cells of the FE, and is not maintained in the interfollicular stalk (Fig. 2 A; Tepass and Knust 1990). Crb is found in the apical membrane of the cells of the FE (Fig. 2 A), similar to many other Drosophila epithelia (Tepass et al. 1990; Tepass and Knust 1990). Dlt shows a similar temporal and spatial distribution as Crb in follicle cells (Fig. 2, B–D), suggesting that both proteins might interact physically in follicle cells as they do in embryonic epithelia (Bhat et al. 1999; Klebes and Knust 2000). Dlt also associates in vitro with Neurexin IV, a transmembrane component of the septate junction (Baumgartner et al. 1996; Bhat et al. 1999). The septate junction, which blocks paracellular diffusion similar to the chordate tight junction, is located basally to the ZA (Mahowald 1972; Tepass and Hartenstein 1994a,Tepass and Hartenstein 1994b). To reconcile these data, it was proposed that Dlt interacts with Crb apically to the ZA, with the ZA, and with Neurexin IV basally to the ZA (Bhat et al. 1999).


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)

Expression of Crb and Dlt in wild-type ovaries. (A) Crb is first detected in follicle cells located between region 2b and the stage 1 follicle that will form the interfollicular stalk (arrow) and in the FE of the stage 1 follicle. Note that interfollicular stalk cells lose Crb rapidly (arrowhead), but that Crb expression is maintained in the FE, where it associates with the apical membrane. (B) Dlt shows the same distribution as Crb in early stages of oogenesis. (C) Expression of Dlt at stage 9 of oogenesis. Dlt is expressed in the FE and the border cells (arrow). In germline cells, Dlt is found at a contact site between nurse cells (arrowheads). (D) Dlt is found at the apical surface of follicle cells, but is absent from the oocyte membrane that is associated with large amounts of F-actin (D′). (D″) A merged image of D and D′. By contrast, Crb strongly accumulates in the oocyte membrane, as was shown previously (Niewiadomska et al. 1999).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2169434&req=5

Figure 2: Expression of Crb and Dlt in wild-type ovaries. (A) Crb is first detected in follicle cells located between region 2b and the stage 1 follicle that will form the interfollicular stalk (arrow) and in the FE of the stage 1 follicle. Note that interfollicular stalk cells lose Crb rapidly (arrowhead), but that Crb expression is maintained in the FE, where it associates with the apical membrane. (B) Dlt shows the same distribution as Crb in early stages of oogenesis. (C) Expression of Dlt at stage 9 of oogenesis. Dlt is expressed in the FE and the border cells (arrow). In germline cells, Dlt is found at a contact site between nurse cells (arrowheads). (D) Dlt is found at the apical surface of follicle cells, but is absent from the oocyte membrane that is associated with large amounts of F-actin (D′). (D″) A merged image of D and D′. By contrast, Crb strongly accumulates in the oocyte membrane, as was shown previously (Niewiadomska et al. 1999).
Mentions: Crb is initially expressed in all follicle cells at stage 1 of oogenesis, but its expression becomes rapidly restricted to the cells of the FE, and is not maintained in the interfollicular stalk (Fig. 2 A; Tepass and Knust 1990). Crb is found in the apical membrane of the cells of the FE (Fig. 2 A), similar to many other Drosophila epithelia (Tepass et al. 1990; Tepass and Knust 1990). Dlt shows a similar temporal and spatial distribution as Crb in follicle cells (Fig. 2, B–D), suggesting that both proteins might interact physically in follicle cells as they do in embryonic epithelia (Bhat et al. 1999; Klebes and Knust 2000). Dlt also associates in vitro with Neurexin IV, a transmembrane component of the septate junction (Baumgartner et al. 1996; Bhat et al. 1999). The septate junction, which blocks paracellular diffusion similar to the chordate tight junction, is located basally to the ZA (Mahowald 1972; Tepass and Hartenstein 1994a,Tepass and Hartenstein 1994b). To reconcile these data, it was proposed that Dlt interacts with Crb apically to the ZA, with the ZA, and with Neurexin IV basally to the ZA (Bhat et al. 1999).

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