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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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Upregulation of  shg expression in border cells  depends on slbo. A′–D′ are  close-ups of the border cell  clusters shown in A–D. (A  and A′) shg RNA expression  in a wild-type follicle, and (B  and B′) a homozygous slbo1  mutant follicle at stage 9 was  detected by in situ hybridization using a digoxygenin-labeled shg cDNA probe.  The migrating border cell  cluster in the wild-type follicle shows high concentration  of shg transcript in all border  cells. In the slbo mutant follicle the border cell cluster remained at the anterior tip.  shg expression in the border  cells has not been upregulated, and is much lower than  in wild-type. The two polar  cells show a higher level of  shg expression than the rosette cells (B′). (C and D′)  Protein expression as revealed by anti-DE-cadherin  staining in a wild-type follicle  (C and C′) and a homozygous slbo1 mutant follicle (D  and D′) at stage 9. The slbo  mutant border cell cluster expresses a much lower level of  DE-cadherin than the wild-type cluster. The two polar  cells express higher levels of  DE-cadherin than the surrounding rosette cells in both  genotypes. (E–F′) Double  staining of slbo1 mutant follicles with anti-DE-cadherin  (E and F) and the polar cell  specific marker Fasciclin III  (E′ and F′). Migratory activity of border cells (arrows) in stage 10b slbo1 mutant follicles is accompanied by upregulation of DE-cadherin expression. Arrowheads in F point to polar cells. Anterior is to the left in all panels. Bars: (A–D) 50 μm; (A′–D′) 20 μm; (E–F′)  20 μm.
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Figure 9: Upregulation of shg expression in border cells depends on slbo. A′–D′ are close-ups of the border cell clusters shown in A–D. (A and A′) shg RNA expression in a wild-type follicle, and (B and B′) a homozygous slbo1 mutant follicle at stage 9 was detected by in situ hybridization using a digoxygenin-labeled shg cDNA probe. The migrating border cell cluster in the wild-type follicle shows high concentration of shg transcript in all border cells. In the slbo mutant follicle the border cell cluster remained at the anterior tip. shg expression in the border cells has not been upregulated, and is much lower than in wild-type. The two polar cells show a higher level of shg expression than the rosette cells (B′). (C and D′) Protein expression as revealed by anti-DE-cadherin staining in a wild-type follicle (C and C′) and a homozygous slbo1 mutant follicle (D and D′) at stage 9. The slbo mutant border cell cluster expresses a much lower level of DE-cadherin than the wild-type cluster. The two polar cells express higher levels of DE-cadherin than the surrounding rosette cells in both genotypes. (E–F′) Double staining of slbo1 mutant follicles with anti-DE-cadherin (E and F) and the polar cell specific marker Fasciclin III (E′ and F′). Migratory activity of border cells (arrows) in stage 10b slbo1 mutant follicles is accompanied by upregulation of DE-cadherin expression. Arrowheads in F point to polar cells. Anterior is to the left in all panels. Bars: (A–D) 50 μm; (A′–D′) 20 μm; (E–F′) 20 μm.

Mentions: A number of genes have been implicated in border cell migration most notably the gene slbo that encodes a C/EBP transcription factor (Montell et al., 1992). In follicles mutant for strong slbo alleles the border cell cluster forms but does not migrate. Among genes or genetic markers that are expressed in border cells some depend on slbo, as for example btl that encodes a Drosophila FGF-receptor homologue, while others do not (Murphy et al., 1995). To study interactions between shg and slbo, we analyzed the shg/DE-cadherin expression in slbo mutant follicles (Fig. 9). In anterior polar cells both shg transcript and protein are upregulated in slbo mutants similar to wild-type. This result is not surprising as shg/DE-cadherin expression in polar cells increases before slbo is expressed at stage 8. In rosette cells, on the other hand, transcript and protein concentrations remain at the same level as in the follicular epithelium (Fig. 9, A–D) whereas in wild-type a dramatic increase in shg expression is seen as described above. In contrast, Crumbs expression in slbo mutant follicles is elevated in all border cells as in wild-type (data not shown). This finding indicates that the upregulation of shg/DE-cadherin expression in rosette cells at the transcriptional level depends on DC/EBP.


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

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

Upregulation of  shg expression in border cells  depends on slbo. A′–D′ are  close-ups of the border cell  clusters shown in A–D. (A  and A′) shg RNA expression  in a wild-type follicle, and (B  and B′) a homozygous slbo1  mutant follicle at stage 9 was  detected by in situ hybridization using a digoxygenin-labeled shg cDNA probe.  The migrating border cell  cluster in the wild-type follicle shows high concentration  of shg transcript in all border  cells. In the slbo mutant follicle the border cell cluster remained at the anterior tip.  shg expression in the border  cells has not been upregulated, and is much lower than  in wild-type. The two polar  cells show a higher level of  shg expression than the rosette cells (B′). (C and D′)  Protein expression as revealed by anti-DE-cadherin  staining in a wild-type follicle  (C and C′) and a homozygous slbo1 mutant follicle (D  and D′) at stage 9. The slbo  mutant border cell cluster expresses a much lower level of  DE-cadherin than the wild-type cluster. The two polar  cells express higher levels of  DE-cadherin than the surrounding rosette cells in both  genotypes. (E–F′) Double  staining of slbo1 mutant follicles with anti-DE-cadherin  (E and F) and the polar cell  specific marker Fasciclin III  (E′ and F′). Migratory activity of border cells (arrows) in stage 10b slbo1 mutant follicles is accompanied by upregulation of DE-cadherin expression. Arrowheads in F point to polar cells. Anterior is to the left in all panels. Bars: (A–D) 50 μm; (A′–D′) 20 μm; (E–F′)  20 μm.
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Figure 9: Upregulation of shg expression in border cells depends on slbo. A′–D′ are close-ups of the border cell clusters shown in A–D. (A and A′) shg RNA expression in a wild-type follicle, and (B and B′) a homozygous slbo1 mutant follicle at stage 9 was detected by in situ hybridization using a digoxygenin-labeled shg cDNA probe. The migrating border cell cluster in the wild-type follicle shows high concentration of shg transcript in all border cells. In the slbo mutant follicle the border cell cluster remained at the anterior tip. shg expression in the border cells has not been upregulated, and is much lower than in wild-type. The two polar cells show a higher level of shg expression than the rosette cells (B′). (C and D′) Protein expression as revealed by anti-DE-cadherin staining in a wild-type follicle (C and C′) and a homozygous slbo1 mutant follicle (D and D′) at stage 9. The slbo mutant border cell cluster expresses a much lower level of DE-cadherin than the wild-type cluster. The two polar cells express higher levels of DE-cadherin than the surrounding rosette cells in both genotypes. (E–F′) Double staining of slbo1 mutant follicles with anti-DE-cadherin (E and F) and the polar cell specific marker Fasciclin III (E′ and F′). Migratory activity of border cells (arrows) in stage 10b slbo1 mutant follicles is accompanied by upregulation of DE-cadherin expression. Arrowheads in F point to polar cells. Anterior is to the left in all panels. Bars: (A–D) 50 μm; (A′–D′) 20 μm; (E–F′) 20 μm.
Mentions: A number of genes have been implicated in border cell migration most notably the gene slbo that encodes a C/EBP transcription factor (Montell et al., 1992). In follicles mutant for strong slbo alleles the border cell cluster forms but does not migrate. Among genes or genetic markers that are expressed in border cells some depend on slbo, as for example btl that encodes a Drosophila FGF-receptor homologue, while others do not (Murphy et al., 1995). To study interactions between shg and slbo, we analyzed the shg/DE-cadherin expression in slbo mutant follicles (Fig. 9). In anterior polar cells both shg transcript and protein are upregulated in slbo mutants similar to wild-type. This result is not surprising as shg/DE-cadherin expression in polar cells increases before slbo is expressed at stage 8. In rosette cells, on the other hand, transcript and protein concentrations remain at the same level as in the follicular epithelium (Fig. 9, A–D) whereas in wild-type a dramatic increase in shg expression is seen as described above. In contrast, Crumbs expression in slbo mutant follicles is elevated in all border cells as in wild-type (data not shown). This finding indicates that the upregulation of shg/DE-cadherin expression in rosette cells at the transcriptional level depends on DC/EBP.

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