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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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Reduced motility  of border cells in a weak shg  mutant. X-gal staining of follicles at late stage 9 (A and  D), at stage 10a (B and E)  and stage 10b (C and F) reveals lacZ expression of the  shgP34-1 P-element insertion  in border cells (arrows) and  centripetal cells (arrowheads). (A–C) shgP34-1/CyO  follicles show normal border  cell migration. The border  cell cluster is attached to the  oocyte in all three follicles.  (D–F) shgP34-1/shgR6 mutant follicles. D and F show border cell clusters that have migrated between nurse cells but have not reached the  oocyte. E shows a border cell cluster that has not penetrated between nurse cells but remained in contact with the follicular epithelium.  Anterior is to the left in all panels. Bar, 100 μm.
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Figure 8: Reduced motility of border cells in a weak shg mutant. X-gal staining of follicles at late stage 9 (A and D), at stage 10a (B and E) and stage 10b (C and F) reveals lacZ expression of the shgP34-1 P-element insertion in border cells (arrows) and centripetal cells (arrowheads). (A–C) shgP34-1/CyO follicles show normal border cell migration. The border cell cluster is attached to the oocyte in all three follicles. (D–F) shgP34-1/shgR6 mutant follicles. D and F show border cell clusters that have migrated between nurse cells but have not reached the oocyte. E shows a border cell cluster that has not penetrated between nurse cells but remained in contact with the follicular epithelium. Anterior is to the left in all panels. Bar, 100 μm.

Mentions: The level of DE-cadherin expression in border cells is extremely high compared with most other cells in ovaries or elsewhere. To address the question whether the high levels of DE-cadherin expression are required to sustain normal migration we reduced DE-cadherin activity in follicles. We examined border cells in animals that carry the heteroallelic combination shgP34-1/shgR6. shgP34-1 is an allele of moderate strength that causes complete embryonic lethality with an intermediate cuticle phenotype (Tepass et al., 1996). shgR6 is a homozygous viable shg allele that displays an adult wing phenotype. shgP34-1/shgR6 animals are semiviable and ovaries show a substantial reduction in levels of DE-cadherin expression (Godt and Tepass, 1998; data not shown). In shgP34-1/shgR6 follicles border cell migration is in many cases substantially delayed (Fig. 8; Table I). In contrast to shgR69 mutant follicles, ∼65% of border cell clusters that had not reached the oocyte at stage 10 in shgP34-1/shgR6 mutant follicles were located between nurse cells and only 35% of the clusters did not penetrate between nurse cells. Thus, in shgP34-1/shgR6 mutant follicles most clusters migrate along their normal route but many clusters show a substantial decrease in the speed of migration suggesting that the level of DE-cadherin expression determines the speed of border cell migration.


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

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

Reduced motility  of border cells in a weak shg  mutant. X-gal staining of follicles at late stage 9 (A and  D), at stage 10a (B and E)  and stage 10b (C and F) reveals lacZ expression of the  shgP34-1 P-element insertion  in border cells (arrows) and  centripetal cells (arrowheads). (A–C) shgP34-1/CyO  follicles show normal border  cell migration. The border  cell cluster is attached to the  oocyte in all three follicles.  (D–F) shgP34-1/shgR6 mutant follicles. D and F show border cell clusters that have migrated between nurse cells but have not reached the  oocyte. E shows a border cell cluster that has not penetrated between nurse cells but remained in contact with the follicular epithelium.  Anterior is to the left in all panels. Bar, 100 μm.
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Related In: Results  -  Collection

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Figure 8: Reduced motility of border cells in a weak shg mutant. X-gal staining of follicles at late stage 9 (A and D), at stage 10a (B and E) and stage 10b (C and F) reveals lacZ expression of the shgP34-1 P-element insertion in border cells (arrows) and centripetal cells (arrowheads). (A–C) shgP34-1/CyO follicles show normal border cell migration. The border cell cluster is attached to the oocyte in all three follicles. (D–F) shgP34-1/shgR6 mutant follicles. D and F show border cell clusters that have migrated between nurse cells but have not reached the oocyte. E shows a border cell cluster that has not penetrated between nurse cells but remained in contact with the follicular epithelium. Anterior is to the left in all panels. Bar, 100 μm.
Mentions: The level of DE-cadherin expression in border cells is extremely high compared with most other cells in ovaries or elsewhere. To address the question whether the high levels of DE-cadherin expression are required to sustain normal migration we reduced DE-cadherin activity in follicles. We examined border cells in animals that carry the heteroallelic combination shgP34-1/shgR6. shgP34-1 is an allele of moderate strength that causes complete embryonic lethality with an intermediate cuticle phenotype (Tepass et al., 1996). shgR6 is a homozygous viable shg allele that displays an adult wing phenotype. shgP34-1/shgR6 animals are semiviable and ovaries show a substantial reduction in levels of DE-cadherin expression (Godt and Tepass, 1998; data not shown). In shgP34-1/shgR6 follicles border cell migration is in many cases substantially delayed (Fig. 8; Table I). In contrast to shgR69 mutant follicles, ∼65% of border cell clusters that had not reached the oocyte at stage 10 in shgP34-1/shgR6 mutant follicles were located between nurse cells and only 35% of the clusters did not penetrate between nurse cells. Thus, in shgP34-1/shgR6 mutant follicles most clusters migrate along their normal route but many clusters show a substantial decrease in the speed of migration suggesting that the level of DE-cadherin expression determines the speed of border 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