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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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Migration of shg mutant mosaic border cell clusters.  Stage 9 follicles were stained with anti-DE-cadherin (red) and  the nuclear marker Picogreen (green). (A) A wild-type follicle  showing a migrating border cell cluster. (B) Closeup of the border cell cluster shown in A. All border cells express DE-cadherin.  (C) shg mutant follicle cell clone covering part of the follicular  epithelium. (E) Closeup of the mosaic border cell cluster shown  in C. The migrating border cell cluster contains DE-cadherin positive cells at the front, and DE-cadherin negative cells trailing behind. D shows another example of a mosaic border cell cluster  with the DE-cadherin expressing border cells moving ahead. F  shows a shg mutant mosaic border cell cluster in which the DE-cadherin positive cells have started migrating between the nurse  cells and the shg mutant cells are still located at the anterior end  of the follicle. Anterior is to the left in all panels. Bars: (A and C)  100 μm; (B, D, E, and F) 20 μm.
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Figure 6: Migration of shg mutant mosaic border cell clusters. Stage 9 follicles were stained with anti-DE-cadherin (red) and the nuclear marker Picogreen (green). (A) A wild-type follicle showing a migrating border cell cluster. (B) Closeup of the border cell cluster shown in A. All border cells express DE-cadherin. (C) shg mutant follicle cell clone covering part of the follicular epithelium. (E) Closeup of the mosaic border cell cluster shown in C. The migrating border cell cluster contains DE-cadherin positive cells at the front, and DE-cadherin negative cells trailing behind. D shows another example of a mosaic border cell cluster with the DE-cadherin expressing border cells moving ahead. F shows a shg mutant mosaic border cell cluster in which the DE-cadherin positive cells have started migrating between the nurse cells and the shg mutant cells are still located at the anterior end of the follicle. Anterior is to the left in all panels. Bars: (A and C) 100 μm; (B, D, E, and F) 20 μm.

Mentions: A few border cell clusters (n = 11) were found that contained DE-cadherin positive and negative cells (Fig. 6). These clusters emerged in mosaic follicles in which the clone boundary separating DE-cadherin positive and negative cells runs along the anterior tip of the follicle from where the border cells derive. These clusters, which contained 3–5 DE-cadherin positive and 2–4 DE-cadherin negative cells, migrated between the nurse cells towards the oocyte. The DE-cadherin expressing cells were always found at the leading edge of the cluster while the cells that lack DE-cadherin were trailing behind (Fig. 6, D–F). This cell behavior suggests that the DE-cadherin positive cells are actively migrating whereas the DE-cadherin negative cells are pulled along. It also indicates that DE-cadherin is not essential for maintaining adhesion between border cells during migration despite its prominent accumulation between these cells. These results indicate that in border cells DE-cadherin might have a specific role in cell migration.


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

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

Migration of shg mutant mosaic border cell clusters.  Stage 9 follicles were stained with anti-DE-cadherin (red) and  the nuclear marker Picogreen (green). (A) A wild-type follicle  showing a migrating border cell cluster. (B) Closeup of the border cell cluster shown in A. All border cells express DE-cadherin.  (C) shg mutant follicle cell clone covering part of the follicular  epithelium. (E) Closeup of the mosaic border cell cluster shown  in C. The migrating border cell cluster contains DE-cadherin positive cells at the front, and DE-cadherin negative cells trailing behind. D shows another example of a mosaic border cell cluster  with the DE-cadherin expressing border cells moving ahead. F  shows a shg mutant mosaic border cell cluster in which the DE-cadherin positive cells have started migrating between the nurse  cells and the shg mutant cells are still located at the anterior end  of the follicle. Anterior is to the left in all panels. Bars: (A and C)  100 μm; (B, D, E, and F) 20 μm.
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Figure 6: Migration of shg mutant mosaic border cell clusters. Stage 9 follicles were stained with anti-DE-cadherin (red) and the nuclear marker Picogreen (green). (A) A wild-type follicle showing a migrating border cell cluster. (B) Closeup of the border cell cluster shown in A. All border cells express DE-cadherin. (C) shg mutant follicle cell clone covering part of the follicular epithelium. (E) Closeup of the mosaic border cell cluster shown in C. The migrating border cell cluster contains DE-cadherin positive cells at the front, and DE-cadherin negative cells trailing behind. D shows another example of a mosaic border cell cluster with the DE-cadherin expressing border cells moving ahead. F shows a shg mutant mosaic border cell cluster in which the DE-cadherin positive cells have started migrating between the nurse cells and the shg mutant cells are still located at the anterior end of the follicle. Anterior is to the left in all panels. Bars: (A and C) 100 μm; (B, D, E, and F) 20 μm.
Mentions: A few border cell clusters (n = 11) were found that contained DE-cadherin positive and negative cells (Fig. 6). These clusters emerged in mosaic follicles in which the clone boundary separating DE-cadherin positive and negative cells runs along the anterior tip of the follicle from where the border cells derive. These clusters, which contained 3–5 DE-cadherin positive and 2–4 DE-cadherin negative cells, migrated between the nurse cells towards the oocyte. The DE-cadherin expressing cells were always found at the leading edge of the cluster while the cells that lack DE-cadherin were trailing behind (Fig. 6, D–F). This cell behavior suggests that the DE-cadherin positive cells are actively migrating whereas the DE-cadherin negative cells are pulled along. It also indicates that DE-cadherin is not essential for maintaining adhesion between border cells during migration despite its prominent accumulation between these cells. These results indicate that in border cells DE-cadherin might have a specific role in cell migration.

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