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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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Disruption of border cell migration in shg mutant germ- line clones. Stage 10 follicles are double stained with DE-cadherin (left panels) and the nuclear marker Picogreen (right panels). Arrows point to border cell clusters. (A) Wild-type follicle  with the border cell cluster attached to the oocyte. (B) shg mutant germline clone with a normally located oocyte. The border  cell cluster has not invaded between the nurse cells but remained  directly beneath the follicular epithelium close to the anterior  pole. (C) shg mutant germline clone with a centrally located oocyte. Two border cell clusters have formed, one at each pole of  the follicle, which have not migrated towards the oocyte. (D)  Two optical sections of the same shg mutant germline clone that  has a centrally located oocyte. From the two border cell clusters  one has moved and reached the oocyte (upper section). Note that  the border cell cluster is in contact with the follicular epithelium.  The other one has not moved away from its original polar position  (lower section). Anterior is to the left in all panels. Bar, 100 μm.
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Figure 7: Disruption of border cell migration in shg mutant germ- line clones. Stage 10 follicles are double stained with DE-cadherin (left panels) and the nuclear marker Picogreen (right panels). Arrows point to border cell clusters. (A) Wild-type follicle with the border cell cluster attached to the oocyte. (B) shg mutant germline clone with a normally located oocyte. The border cell cluster has not invaded between the nurse cells but remained directly beneath the follicular epithelium close to the anterior pole. (C) shg mutant germline clone with a centrally located oocyte. Two border cell clusters have formed, one at each pole of the follicle, which have not migrated towards the oocyte. (D) Two optical sections of the same shg mutant germline clone that has a centrally located oocyte. From the two border cell clusters one has moved and reached the oocyte (upper section). Note that the border cell cluster is in contact with the follicular epithelium. The other one has not moved away from its original polar position (lower section). Anterior is to the left in all panels. Bar, 100 μm.

Mentions: DE-cadherin like other classic cadherins is a homophilic adhesion molecule (Oda et al., 1994). The lack of DE-cadherin in border cells prevents penetration and migration of border cells between nurse cells. This suggests that DE-cadherin on the surface of border cells might directly interact with DE-cadherin expressed by nurse cells to promote migration. To examine this possibility we generated follicles that contain a shgR69 mutant germline (Fig. 7; see Materials and Methods). Follicles with a shg mutant germ-line show a variety of defects including a mislocalization of the oocyte similar to follicle cell clones (Oda et al., 1997; White et al., 1998; Godt and Tepass, 1998; González-Reyes and St. Johnston, 1998b). All follicles eventually degenerate. Among the examined 99 shg germline clones with normally localized oocyte there was no follicle in which the border cell cluster had penetrated between nurse cells. Instead, the border cell clusters always remain attached to the follicular epithelium. Typically, they are found at the boundary between the first and second nurse cell as shown in Fig. 7 B. Sometimes, they move even further posteriorly, and a single case was observed where the border cells had reached the oocyte.


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

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

Disruption of border cell migration in shg mutant germ- line clones. Stage 10 follicles are double stained with DE-cadherin (left panels) and the nuclear marker Picogreen (right panels). Arrows point to border cell clusters. (A) Wild-type follicle  with the border cell cluster attached to the oocyte. (B) shg mutant germline clone with a normally located oocyte. The border  cell cluster has not invaded between the nurse cells but remained  directly beneath the follicular epithelium close to the anterior  pole. (C) shg mutant germline clone with a centrally located oocyte. Two border cell clusters have formed, one at each pole of  the follicle, which have not migrated towards the oocyte. (D)  Two optical sections of the same shg mutant germline clone that  has a centrally located oocyte. From the two border cell clusters  one has moved and reached the oocyte (upper section). Note that  the border cell cluster is in contact with the follicular epithelium.  The other one has not moved away from its original polar position  (lower section). Anterior is to the left in all panels. Bar, 100 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2132905&req=5

Figure 7: Disruption of border cell migration in shg mutant germ- line clones. Stage 10 follicles are double stained with DE-cadherin (left panels) and the nuclear marker Picogreen (right panels). Arrows point to border cell clusters. (A) Wild-type follicle with the border cell cluster attached to the oocyte. (B) shg mutant germline clone with a normally located oocyte. The border cell cluster has not invaded between the nurse cells but remained directly beneath the follicular epithelium close to the anterior pole. (C) shg mutant germline clone with a centrally located oocyte. Two border cell clusters have formed, one at each pole of the follicle, which have not migrated towards the oocyte. (D) Two optical sections of the same shg mutant germline clone that has a centrally located oocyte. From the two border cell clusters one has moved and reached the oocyte (upper section). Note that the border cell cluster is in contact with the follicular epithelium. The other one has not moved away from its original polar position (lower section). Anterior is to the left in all panels. Bar, 100 μm.
Mentions: DE-cadherin like other classic cadherins is a homophilic adhesion molecule (Oda et al., 1994). The lack of DE-cadherin in border cells prevents penetration and migration of border cells between nurse cells. This suggests that DE-cadherin on the surface of border cells might directly interact with DE-cadherin expressed by nurse cells to promote migration. To examine this possibility we generated follicles that contain a shgR69 mutant germline (Fig. 7; see Materials and Methods). Follicles with a shg mutant germ-line show a variety of defects including a mislocalization of the oocyte similar to follicle cell clones (Oda et al., 1997; White et al., 1998; Godt and Tepass, 1998; González-Reyes and St. Johnston, 1998b). All follicles eventually degenerate. Among the examined 99 shg germline clones with normally localized oocyte there was no follicle in which the border cell cluster had penetrated between nurse cells. Instead, the border cell clusters always remain attached to the follicular epithelium. Typically, they are found at the boundary between the first and second nurse cell as shown in Fig. 7 B. Sometimes, they move even further posteriorly, and a single case was observed where the border cells had reached 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