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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 expression in border cells is required for  their migration between the nurse cells. (A–C) Double staining  of stage 10 follicles with DE-cadherin (red) and the nuclear border cell marker DC/EBP (green). Arrows point to border cell  clusters. (A) In a wild-type follicle the border cell cluster that expresses DE-cadherin and DC/EBP has reached the oocyte. (B)  shows a shg mutant follicle cell clone that encompasses most of  the follicle cells, except for a small patch of DE-cadherin positive  cells at the posterior pole (arrowheads). The germline cells express DE-cadherin. A shg mutant border cell cluster expressing  DC/EBP has formed that has not moved between the nurse cells  towards the oocyte. The cluster is located between nurse cells  and the follicular epithelium close to the anterior tip of the follicle. (C) Close-up of the shg mutant border cell cluster shown in  B. (D–F) Triple staining of stage 10 follicles for Armadillo (red)  that is expressed in the same pattern as DE-cadherin, for the polar cell marker Fasciclin-III (FasIII; also red), and the nuclear  marker Picogreen (green). Arrows point to border cell clusters.  (D) In the wild-type follicle the border cell cluster has reached  the oocyte. (E) shows a shg mutant follicle cell clone derived  from shg mutant follicle stem cells that comprises all follicle cells,  including the border cells, as indicated by the absence of Armadillo. Red staining in anterior and posterior polar cells is due to  expression of Fasciclin III. The anterior polar cells are part of the  border cell cluster that has not migrated to the oocyte but remained attached to follicle cells close to the anterior pole of the  follicle. (F) Closeup of the shg mutant border cell cluster shown  in (E). Bars: (A, B, D, and E) 100 μm; (C and F) 10 μm.
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Figure 5: DE-cadherin expression in border cells is required for their migration between the nurse cells. (A–C) Double staining of stage 10 follicles with DE-cadherin (red) and the nuclear border cell marker DC/EBP (green). Arrows point to border cell clusters. (A) In a wild-type follicle the border cell cluster that expresses DE-cadherin and DC/EBP has reached the oocyte. (B) shows a shg mutant follicle cell clone that encompasses most of the follicle cells, except for a small patch of DE-cadherin positive cells at the posterior pole (arrowheads). The germline cells express DE-cadherin. A shg mutant border cell cluster expressing DC/EBP has formed that has not moved between the nurse cells towards the oocyte. The cluster is located between nurse cells and the follicular epithelium close to the anterior tip of the follicle. (C) Close-up of the shg mutant border cell cluster shown in B. (D–F) Triple staining of stage 10 follicles for Armadillo (red) that is expressed in the same pattern as DE-cadherin, for the polar cell marker Fasciclin-III (FasIII; also red), and the nuclear marker Picogreen (green). Arrows point to border cell clusters. (D) In the wild-type follicle the border cell cluster has reached the oocyte. (E) shows a shg mutant follicle cell clone derived from shg mutant follicle stem cells that comprises all follicle cells, including the border cells, as indicated by the absence of Armadillo. Red staining in anterior and posterior polar cells is due to expression of Fasciclin III. The anterior polar cells are part of the border cell cluster that has not migrated to the oocyte but remained attached to follicle cells close to the anterior pole of the follicle. (F) Closeup of the shg mutant border cell cluster shown in (E). Bars: (A, B, D, and E) 100 μm; (C and F) 10 μm.

Mentions: Border cell clusters in which all cells lack DE-cadherin do not migrate between nurse cells towards the oocyte. We examined a total of 62 shg mutant follicle cell clones. shg mutant border cell clusters formed in all clones and segregated from the follicular epithelium as revealed, for example, by the expression of the border cell specific marker DC/EBP (Fig. 5, A–C). shg mutant clusters contain a normal number of DC/EBP positive border cells (8.3; n = 15) as compared with wild-type clusters (8.0; n = 40), and show an overall normal cell arrangement with a pair of Fasciclin III positive central polar cells (Fig. 5, D–F). In all follicles examined, the border cell cluster was located between follicular epithelium and nurse cells indicating that shg mutant border cell clusters cannot penetrate between nurse cells. The clusters were located either near the anterior tip of the follicle or at the boundary between the first and second nurse cell. These findings indicate that DE-cadherin expression in border cells is required for border cell migration.


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

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

DE-cadherin expression in border cells is required for  their migration between the nurse cells. (A–C) Double staining  of stage 10 follicles with DE-cadherin (red) and the nuclear border cell marker DC/EBP (green). Arrows point to border cell  clusters. (A) In a wild-type follicle the border cell cluster that expresses DE-cadherin and DC/EBP has reached the oocyte. (B)  shows a shg mutant follicle cell clone that encompasses most of  the follicle cells, except for a small patch of DE-cadherin positive  cells at the posterior pole (arrowheads). The germline cells express DE-cadherin. A shg mutant border cell cluster expressing  DC/EBP has formed that has not moved between the nurse cells  towards the oocyte. The cluster is located between nurse cells  and the follicular epithelium close to the anterior tip of the follicle. (C) Close-up of the shg mutant border cell cluster shown in  B. (D–F) Triple staining of stage 10 follicles for Armadillo (red)  that is expressed in the same pattern as DE-cadherin, for the polar cell marker Fasciclin-III (FasIII; also red), and the nuclear  marker Picogreen (green). Arrows point to border cell clusters.  (D) In the wild-type follicle the border cell cluster has reached  the oocyte. (E) shows a shg mutant follicle cell clone derived  from shg mutant follicle stem cells that comprises all follicle cells,  including the border cells, as indicated by the absence of Armadillo. Red staining in anterior and posterior polar cells is due to  expression of Fasciclin III. The anterior polar cells are part of the  border cell cluster that has not migrated to the oocyte but remained attached to follicle cells close to the anterior pole of the  follicle. (F) Closeup of the shg mutant border cell cluster shown  in (E). Bars: (A, B, D, and E) 100 μm; (C and F) 10 μm.
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Figure 5: DE-cadherin expression in border cells is required for their migration between the nurse cells. (A–C) Double staining of stage 10 follicles with DE-cadherin (red) and the nuclear border cell marker DC/EBP (green). Arrows point to border cell clusters. (A) In a wild-type follicle the border cell cluster that expresses DE-cadherin and DC/EBP has reached the oocyte. (B) shows a shg mutant follicle cell clone that encompasses most of the follicle cells, except for a small patch of DE-cadherin positive cells at the posterior pole (arrowheads). The germline cells express DE-cadherin. A shg mutant border cell cluster expressing DC/EBP has formed that has not moved between the nurse cells towards the oocyte. The cluster is located between nurse cells and the follicular epithelium close to the anterior tip of the follicle. (C) Close-up of the shg mutant border cell cluster shown in B. (D–F) Triple staining of stage 10 follicles for Armadillo (red) that is expressed in the same pattern as DE-cadherin, for the polar cell marker Fasciclin-III (FasIII; also red), and the nuclear marker Picogreen (green). Arrows point to border cell clusters. (D) In the wild-type follicle the border cell cluster has reached the oocyte. (E) shows a shg mutant follicle cell clone derived from shg mutant follicle stem cells that comprises all follicle cells, including the border cells, as indicated by the absence of Armadillo. Red staining in anterior and posterior polar cells is due to expression of Fasciclin III. The anterior polar cells are part of the border cell cluster that has not migrated to the oocyte but remained attached to follicle cells close to the anterior pole of the follicle. (F) Closeup of the shg mutant border cell cluster shown in (E). Bars: (A, B, D, and E) 100 μm; (C and F) 10 μm.
Mentions: Border cell clusters in which all cells lack DE-cadherin do not migrate between nurse cells towards the oocyte. We examined a total of 62 shg mutant follicle cell clones. shg mutant border cell clusters formed in all clones and segregated from the follicular epithelium as revealed, for example, by the expression of the border cell specific marker DC/EBP (Fig. 5, A–C). shg mutant clusters contain a normal number of DC/EBP positive border cells (8.3; n = 15) as compared with wild-type clusters (8.0; n = 40), and show an overall normal cell arrangement with a pair of Fasciclin III positive central polar cells (Fig. 5, D–F). In all follicles examined, the border cell cluster was located between follicular epithelium and nurse cells indicating that shg mutant border cell clusters cannot penetrate between nurse cells. The clusters were located either near the anterior tip of the follicle or at the boundary between the first and second nurse cell. These findings indicate that DE-cadherin expression in border cells is required for 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