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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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DE-cadherin is  required for centripetal cell  movement. Follicles are double stained for DE-cadherin  (A–F) and F-actin (A′–F′).  (A and A′) In an early stage  10b wild-type follicle centripetal cells strongly elongate  apical-basally, develop protrusive ends that penetrate  between oocyte and nurse  cells, and migrate along the  surface of the oocyte towards  the border cells. Strongest  concentration of DE-cadherin is seen in the leading  edges of the centripetal cells.  (B and B′) At late stage 10b,  when cytoplasmic actin fibers  have formed in the nurse  cells, the invaded centripetal  cells form a thin layer covering the anterior surface of  the oocyte in a wild-type follicle. (C and C′) Mid-stage  10b follicle with a shgR69 mutant follicle cell clone that  comprises all follicle cells.  Some shg mutant centripetal  cells have segregated from  the follicular epithelium but  remain in the periphery of  the follicle. These cells have  a rounded appearance and lack protrusive ends in contrast to wild-type centripetal cells (see inset). (D and D′) The late stage 10b follicle has a shg mutant mosaic follicular epithelium. DE-cadherin negative centripetal cells (arrowhead) show no invasive behavior in contrast to the DE-cadherin positive centripetal cells (arrow) that are elongated and migrated between oocyte and nurse cells. However,  the migrating DE-cadherin positive centripetal cells form a thicker layer than in wild-type follicles. (E and E′) Stage 10b follicle with a  shg mutant germline. Centripetal cells that show an elevated level of DE-cadherin expression did not move between germline cells. (F  and F′) Stage 10b follicle with a shg mutant germline. Centripetal cells moved between oocyte and nurse cells forming clumps of cells  with abnormal morphology. Anterior is to the left in all panels. Bar, 100 μm.
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Figure 10: DE-cadherin is required for centripetal cell movement. Follicles are double stained for DE-cadherin (A–F) and F-actin (A′–F′). (A and A′) In an early stage 10b wild-type follicle centripetal cells strongly elongate apical-basally, develop protrusive ends that penetrate between oocyte and nurse cells, and migrate along the surface of the oocyte towards the border cells. Strongest concentration of DE-cadherin is seen in the leading edges of the centripetal cells. (B and B′) At late stage 10b, when cytoplasmic actin fibers have formed in the nurse cells, the invaded centripetal cells form a thin layer covering the anterior surface of the oocyte in a wild-type follicle. (C and C′) Mid-stage 10b follicle with a shgR69 mutant follicle cell clone that comprises all follicle cells. Some shg mutant centripetal cells have segregated from the follicular epithelium but remain in the periphery of the follicle. These cells have a rounded appearance and lack protrusive ends in contrast to wild-type centripetal cells (see inset). (D and D′) The late stage 10b follicle has a shg mutant mosaic follicular epithelium. DE-cadherin negative centripetal cells (arrowhead) show no invasive behavior in contrast to the DE-cadherin positive centripetal cells (arrow) that are elongated and migrated between oocyte and nurse cells. However, the migrating DE-cadherin positive centripetal cells form a thicker layer than in wild-type follicles. (E and E′) Stage 10b follicle with a shg mutant germline. Centripetal cells that show an elevated level of DE-cadherin expression did not move between germline cells. (F and F′) Stage 10b follicle with a shg mutant germline. Centripetal cells moved between oocyte and nurse cells forming clumps of cells with abnormal morphology. Anterior is to the left in all panels. Bar, 100 μm.

Mentions: The centripetal cells are a second migratory cell population in Drosophila follicles that expresses high levels of DE-cadherin during migration (Fig. 10, A and B). During stage 10b of oogenesis the anterior most columnar follicle cells, the centripetal cells undergo a strong apical-basal cell elongation while penetrating between nurse cells and oocyte. Their leading apical edges that penetrate between the oocyte and the nurse cells are rich in DE-cadherin and F-actin (Fig. 10, A–B′). The centripetal cells migrate along the surface of the oocyte towards the border cells. They make lateral contact with the border cells later during oogenesis to form a confluent epithelium that covers the anterior side of the oocyte.


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

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

DE-cadherin is  required for centripetal cell  movement. Follicles are double stained for DE-cadherin  (A–F) and F-actin (A′–F′).  (A and A′) In an early stage  10b wild-type follicle centripetal cells strongly elongate  apical-basally, develop protrusive ends that penetrate  between oocyte and nurse  cells, and migrate along the  surface of the oocyte towards  the border cells. Strongest  concentration of DE-cadherin is seen in the leading  edges of the centripetal cells.  (B and B′) At late stage 10b,  when cytoplasmic actin fibers  have formed in the nurse  cells, the invaded centripetal  cells form a thin layer covering the anterior surface of  the oocyte in a wild-type follicle. (C and C′) Mid-stage  10b follicle with a shgR69 mutant follicle cell clone that  comprises all follicle cells.  Some shg mutant centripetal  cells have segregated from  the follicular epithelium but  remain in the periphery of  the follicle. These cells have  a rounded appearance and lack protrusive ends in contrast to wild-type centripetal cells (see inset). (D and D′) The late stage 10b follicle has a shg mutant mosaic follicular epithelium. DE-cadherin negative centripetal cells (arrowhead) show no invasive behavior in contrast to the DE-cadherin positive centripetal cells (arrow) that are elongated and migrated between oocyte and nurse cells. However,  the migrating DE-cadherin positive centripetal cells form a thicker layer than in wild-type follicles. (E and E′) Stage 10b follicle with a  shg mutant germline. Centripetal cells that show an elevated level of DE-cadherin expression did not move between germline cells. (F  and F′) Stage 10b follicle with a shg mutant germline. Centripetal cells moved between oocyte and nurse cells forming clumps of cells  with abnormal morphology. Anterior is to the left in all panels. Bar, 100 μm.
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Related In: Results  -  Collection

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Figure 10: DE-cadherin is required for centripetal cell movement. Follicles are double stained for DE-cadherin (A–F) and F-actin (A′–F′). (A and A′) In an early stage 10b wild-type follicle centripetal cells strongly elongate apical-basally, develop protrusive ends that penetrate between oocyte and nurse cells, and migrate along the surface of the oocyte towards the border cells. Strongest concentration of DE-cadherin is seen in the leading edges of the centripetal cells. (B and B′) At late stage 10b, when cytoplasmic actin fibers have formed in the nurse cells, the invaded centripetal cells form a thin layer covering the anterior surface of the oocyte in a wild-type follicle. (C and C′) Mid-stage 10b follicle with a shgR69 mutant follicle cell clone that comprises all follicle cells. Some shg mutant centripetal cells have segregated from the follicular epithelium but remain in the periphery of the follicle. These cells have a rounded appearance and lack protrusive ends in contrast to wild-type centripetal cells (see inset). (D and D′) The late stage 10b follicle has a shg mutant mosaic follicular epithelium. DE-cadherin negative centripetal cells (arrowhead) show no invasive behavior in contrast to the DE-cadherin positive centripetal cells (arrow) that are elongated and migrated between oocyte and nurse cells. However, the migrating DE-cadherin positive centripetal cells form a thicker layer than in wild-type follicles. (E and E′) Stage 10b follicle with a shg mutant germline. Centripetal cells that show an elevated level of DE-cadherin expression did not move between germline cells. (F and F′) Stage 10b follicle with a shg mutant germline. Centripetal cells moved between oocyte and nurse cells forming clumps of cells with abnormal morphology. Anterior is to the left in all panels. Bar, 100 μm.
Mentions: The centripetal cells are a second migratory cell population in Drosophila follicles that expresses high levels of DE-cadherin during migration (Fig. 10, A and B). During stage 10b of oogenesis the anterior most columnar follicle cells, the centripetal cells undergo a strong apical-basal cell elongation while penetrating between nurse cells and oocyte. Their leading apical edges that penetrate between the oocyte and the nurse cells are rich in DE-cadherin and F-actin (Fig. 10, A–B′). The centripetal cells migrate along the surface of the oocyte towards the border cells. They make lateral contact with the border cells later during oogenesis to form a confluent epithelium that covers the anterior side of the oocyte.

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