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DE-Cadherin is required for intercellular motility during Drosophila oogenesis.

Niewiadomska P, Godt D, Tepass U - J. Cell Biol. (1999)

Bottom Line: Removing DE-cadherin from either the follicle cells or the germline cells blocks migration of border cells and centripetal cells on the surface of germline cells.The speed of migration depends on the level of DE-cadherin expression, as border cells migrate more slowly when DE-cadherin activity is reduced.Finally, we show that the upregulation of DE-cadherin expression in border cells depends on the activity of the Drosophila C/EBP transcription factor that is essential for border cell migration.

View Article: PubMed Central - PubMed

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

ABSTRACT
Cadherins are involved in a variety of morphogenetic movements during animal development. However, it has been difficult to pinpoint the precise function of cadherins in morphogenetic processes due to the multifunctional nature of cadherin requirement. The data presented here indicate that homophilic adhesion promoted by Drosophila E-cadherin (DE-cadherin) mediates two cell migration events during Drosophila oogenesis. In Drosophila follicles, two groups of follicle cells, the border cells and the centripetal cells migrate on the surface of germline cells. We show that the border cells migrate as an epithelial patch in which two centrally located cells retain epithelial polarity and peripheral cells are partially depolarized. Both follicle cells and germline cells express DE-cadherin, and border cells and centripetal cells strongly upregulate the expression of DE-cadherin shortly before and during their migration. Removing DE-cadherin from either the follicle cells or the germline cells blocks migration of border cells and centripetal cells on the surface of germline cells. The function of DE-cadherin in border cells appears to be specific for migration as the formation of the border cell cluster and the adhesion between border cells are not disrupted in the absence of DE-cadherin. The speed of migration depends on the level of DE-cadherin expression, as border cells migrate more slowly when DE-cadherin activity is reduced. Finally, we show that the upregulation of DE-cadherin expression in border cells depends on the activity of the Drosophila C/EBP transcription factor that is essential for border cell migration.

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Expression of  Crumbs in border cells of  wild-type ovaries. (A) Crumbs  is found at the apical cell  surface in all follicle cells.  At early stage 8 anterior polar cells have upregulated  Crumbs expression (arrow).  Crumbs protein is also seen  in the cytoplasm of the polar  cells. (B) Follicle cells next to  the polar cells upregulate  Crumbs during stage 8. (C)  At early stage 9 when a rosette cell initiates migration  (arrow), Crumbs has a nonpolarized distribution in rosette cells. D and D′ show  two confocal sections of the  same cluster during mid  migration. In polar cells  Crumbs is concentrated at  the apical cell surface (arrow  in D′) and not found at the  lateral cell surface that contacts the rosette cells (arrow  in D). In rosette cells Crumbs accumulates at the contact sides between neighboring rosette cells and is found in a punctate pattern at  the interface of rosette cells and nurse cells (arrowheads). (E) At stage 10 when the border cells are in contact with the oocyte Crumbs  distribution in rosette cells is again restricted to the apical surface. Bars: (A–D′) 10 μm; (E) 10 μm.
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Figure 3: Expression of Crumbs in border cells of wild-type ovaries. (A) Crumbs is found at the apical cell surface in all follicle cells. At early stage 8 anterior polar cells have upregulated Crumbs expression (arrow). Crumbs protein is also seen in the cytoplasm of the polar cells. (B) Follicle cells next to the polar cells upregulate Crumbs during stage 8. (C) At early stage 9 when a rosette cell initiates migration (arrow), Crumbs has a nonpolarized distribution in rosette cells. D and D′ show two confocal sections of the same cluster during mid migration. In polar cells Crumbs is concentrated at the apical cell surface (arrow in D′) and not found at the lateral cell surface that contacts the rosette cells (arrow in D). In rosette cells Crumbs accumulates at the contact sides between neighboring rosette cells and is found in a punctate pattern at the interface of rosette cells and nurse cells (arrowheads). (E) At stage 10 when the border cells are in contact with the oocyte Crumbs distribution in rosette cells is again restricted to the apical surface. Bars: (A–D′) 10 μm; (E) 10 μm.

Mentions: To further analyze border cell structure we examined border cells with antibodies recognizing the Crumbs protein, a marker for the apical membrane of epithelial cells including the follicular epithelium (Tepass and Knust, 1990; Tepass et al., 1990). Crumbs is expressed in the border cells during migration (Fig. 3). Similar to DE-cadherin, increased levels of Crumbs are seen in the polar cells and in surrounding follicle cells before border cells segregate from the epithelium (Fig. 3, A and B). Upon segregation of the border cells Crumbs distribution depolarizes in rosette cells (Fig. 3, C and D). Crumbs is highly expressed at the interface of adjacent rosette cells, and at lower levels at the interface of rosette cells and nurse cells, a pattern similar to DE-cadherin. Crumbs remains restricted to the apical surface of polar cells during migration. Crumbs is not found at the lateral surface of polar cells or at the cell surface of the rosette cells that are in contact with the polar cells (Fig. 3, D and D′). At the end of migration when the border cell cluster contacts the oocyte, the apical surface of the polar cells faces the oocyte. The distribution of Crumbs in the rosette cells becomes restricted again to the apical cell surface before these cells become confluent with the ingrowing centripetal cells (Fig. 3 E). These results indicate that polar cells and, to a lesser degree, rosette cells retain epithelial polarization during migration. Fig. 4 summarizes the expression and distribution of molecular markers that together with the morphology of the border cells suggest that these cells form a migrating epithelial patch rather than a mesenchymal cluster. Our findings suggest that only the rosette cells are actively migrating and that the polar cells are carried by the rosette cells during the migration process.


DE-Cadherin is required for intercellular motility during Drosophila oogenesis.

Niewiadomska P, Godt D, Tepass U - J. Cell Biol. (1999)

Expression of  Crumbs in border cells of  wild-type ovaries. (A) Crumbs  is found at the apical cell  surface in all follicle cells.  At early stage 8 anterior polar cells have upregulated  Crumbs expression (arrow).  Crumbs protein is also seen  in the cytoplasm of the polar  cells. (B) Follicle cells next to  the polar cells upregulate  Crumbs during stage 8. (C)  At early stage 9 when a rosette cell initiates migration  (arrow), Crumbs has a nonpolarized distribution in rosette cells. D and D′ show  two confocal sections of the  same cluster during mid  migration. In polar cells  Crumbs is concentrated at  the apical cell surface (arrow  in D′) and not found at the  lateral cell surface that contacts the rosette cells (arrow  in D). In rosette cells Crumbs accumulates at the contact sides between neighboring rosette cells and is found in a punctate pattern at  the interface of rosette cells and nurse cells (arrowheads). (E) At stage 10 when the border cells are in contact with the oocyte Crumbs  distribution in rosette cells is again restricted to the apical surface. Bars: (A–D′) 10 μm; (E) 10 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2132905&req=5

Figure 3: Expression of Crumbs in border cells of wild-type ovaries. (A) Crumbs is found at the apical cell surface in all follicle cells. At early stage 8 anterior polar cells have upregulated Crumbs expression (arrow). Crumbs protein is also seen in the cytoplasm of the polar cells. (B) Follicle cells next to the polar cells upregulate Crumbs during stage 8. (C) At early stage 9 when a rosette cell initiates migration (arrow), Crumbs has a nonpolarized distribution in rosette cells. D and D′ show two confocal sections of the same cluster during mid migration. In polar cells Crumbs is concentrated at the apical cell surface (arrow in D′) and not found at the lateral cell surface that contacts the rosette cells (arrow in D). In rosette cells Crumbs accumulates at the contact sides between neighboring rosette cells and is found in a punctate pattern at the interface of rosette cells and nurse cells (arrowheads). (E) At stage 10 when the border cells are in contact with the oocyte Crumbs distribution in rosette cells is again restricted to the apical surface. Bars: (A–D′) 10 μm; (E) 10 μm.
Mentions: To further analyze border cell structure we examined border cells with antibodies recognizing the Crumbs protein, a marker for the apical membrane of epithelial cells including the follicular epithelium (Tepass and Knust, 1990; Tepass et al., 1990). Crumbs is expressed in the border cells during migration (Fig. 3). Similar to DE-cadherin, increased levels of Crumbs are seen in the polar cells and in surrounding follicle cells before border cells segregate from the epithelium (Fig. 3, A and B). Upon segregation of the border cells Crumbs distribution depolarizes in rosette cells (Fig. 3, C and D). Crumbs is highly expressed at the interface of adjacent rosette cells, and at lower levels at the interface of rosette cells and nurse cells, a pattern similar to DE-cadherin. Crumbs remains restricted to the apical surface of polar cells during migration. Crumbs is not found at the lateral surface of polar cells or at the cell surface of the rosette cells that are in contact with the polar cells (Fig. 3, D and D′). At the end of migration when the border cell cluster contacts the oocyte, the apical surface of the polar cells faces the oocyte. The distribution of Crumbs in the rosette cells becomes restricted again to the apical cell surface before these cells become confluent with the ingrowing centripetal cells (Fig. 3 E). These results indicate that polar cells and, to a lesser degree, rosette cells retain epithelial polarization during migration. Fig. 4 summarizes the expression and distribution of molecular markers that together with the morphology of the border cells suggest that these cells form a migrating epithelial patch rather than a mesenchymal cluster. Our findings suggest that only the rosette cells are actively migrating and that the polar cells are carried by the rosette cells during the migration process.

Bottom Line: Removing DE-cadherin from either the follicle cells or the germline cells blocks migration of border cells and centripetal cells on the surface of germline cells.The speed of migration depends on the level of DE-cadherin expression, as border cells migrate more slowly when DE-cadherin activity is reduced.Finally, we show that the upregulation of DE-cadherin expression in border cells depends on the activity of the Drosophila C/EBP transcription factor that is essential for border cell migration.

View Article: PubMed Central - PubMed

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

ABSTRACT
Cadherins are involved in a variety of morphogenetic movements during animal development. However, it has been difficult to pinpoint the precise function of cadherins in morphogenetic processes due to the multifunctional nature of cadherin requirement. The data presented here indicate that homophilic adhesion promoted by Drosophila E-cadherin (DE-cadherin) mediates two cell migration events during Drosophila oogenesis. In Drosophila follicles, two groups of follicle cells, the border cells and the centripetal cells migrate on the surface of germline cells. We show that the border cells migrate as an epithelial patch in which two centrally located cells retain epithelial polarity and peripheral cells are partially depolarized. Both follicle cells and germline cells express DE-cadherin, and border cells and centripetal cells strongly upregulate the expression of DE-cadherin shortly before and during their migration. Removing DE-cadherin from either the follicle cells or the germline cells blocks migration of border cells and centripetal cells on the surface of germline cells. The function of DE-cadherin in border cells appears to be specific for migration as the formation of the border cell cluster and the adhesion between border cells are not disrupted in the absence of DE-cadherin. The speed of migration depends on the level of DE-cadherin expression, as border cells migrate more slowly when DE-cadherin activity is reduced. Finally, we show that the upregulation of DE-cadherin expression in border cells depends on the activity of the Drosophila C/EBP transcription factor that is essential for border cell migration.

Show MeSH
Related in: MedlinePlus