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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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Expression of DE-cadherin in border cells of  wild-type ovaries. (A–C) Arrows point to border cells.  (A) At early stage 9 border  cells have accumulated high  levels of DE-cadherin before migration is initiated.  (B) Border cells expressing  elevated levels of DE-cadherin migrate on a straight  path through the center of  the follicle towards the oocyte during stage 9. (C) After  border cells have reached the  oocyte that fills the posterior  half of a follicle at stage 10a,  they maintain high levels of  DE-cadherin expression for  some time and move slightly  dorsally. (D–I) show high  resolution images of DE-cadherin (red) expression in border cells. (F–H) show follicles that are counterstained  for Fasciclin III (green) that  serves as a marker for the  two polar cells. Fasciclin III  accumulates at the contact  surface between polar cells.  (D) Stage 6. Anterior polar  cells contain more DE-cadherin than neighboring follicle cells. Polar cells are constricted apically (arrow) and  have a rounded shape. DE-cadherin is concentrated at the zonula adherens. (E) Stage 8. Follicle cells adjacent to polar cells have upregulated DE-cadherin expression (arrows). (F) Early stage 9. Same follicle as in A. DE-cadherin distribution in follicle cells adjacent to polar cells (the rosette cells)  has depolarized. (G) Early stage 9. Migration is initiated by a rosette cell penetrating between nurse cells (arrow). (H) Late stage 9.  Same follicle as in B. During migration polar cells have a central position and are surrounded by rosette cells. Highest concentration of  DE-cadherin is seen at the contact surfaces between rosette cells and polar cells and between rosette cells. Lower amounts of DE-cadherin are seen at the interface of rosette cells and nurse cells in a punctate pattern (arrow). (I) Stage 10a. Border cells have established  contact to the surface of the oocyte (white line). The polar cells are centrally located and their constricted apical surface contacts the oocyte (see also Peifer et al., 1993). (J–L′) show distribution of DE-cadherin (red) and F-actin (green) in border cells at stage 9. F-actin is  concentrated in the periphery of the border cell cluster. (J) Border cells at the onset of migration and (K) during mid migration. Note  the round centrally located polar cells with constricted apical cell surfaces that are rich in DE-cadherin and F-actin. (L) and (L′) show  two confocal sections of the same cluster. The arrows in L′ point to the constricted apical surfaces of the polar cells. Anterior is to the  left in all panels. Bars: (A–C) 50 μm; (D–G, J–L′) 10 μm; (H and I) 10 μm.
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Figure 2: Expression of DE-cadherin in border cells of wild-type ovaries. (A–C) Arrows point to border cells. (A) At early stage 9 border cells have accumulated high levels of DE-cadherin before migration is initiated. (B) Border cells expressing elevated levels of DE-cadherin migrate on a straight path through the center of the follicle towards the oocyte during stage 9. (C) After border cells have reached the oocyte that fills the posterior half of a follicle at stage 10a, they maintain high levels of DE-cadherin expression for some time and move slightly dorsally. (D–I) show high resolution images of DE-cadherin (red) expression in border cells. (F–H) show follicles that are counterstained for Fasciclin III (green) that serves as a marker for the two polar cells. Fasciclin III accumulates at the contact surface between polar cells. (D) Stage 6. Anterior polar cells contain more DE-cadherin than neighboring follicle cells. Polar cells are constricted apically (arrow) and have a rounded shape. DE-cadherin is concentrated at the zonula adherens. (E) Stage 8. Follicle cells adjacent to polar cells have upregulated DE-cadherin expression (arrows). (F) Early stage 9. Same follicle as in A. DE-cadherin distribution in follicle cells adjacent to polar cells (the rosette cells) has depolarized. (G) Early stage 9. Migration is initiated by a rosette cell penetrating between nurse cells (arrow). (H) Late stage 9. Same follicle as in B. During migration polar cells have a central position and are surrounded by rosette cells. Highest concentration of DE-cadherin is seen at the contact surfaces between rosette cells and polar cells and between rosette cells. Lower amounts of DE-cadherin are seen at the interface of rosette cells and nurse cells in a punctate pattern (arrow). (I) Stage 10a. Border cells have established contact to the surface of the oocyte (white line). The polar cells are centrally located and their constricted apical surface contacts the oocyte (see also Peifer et al., 1993). (J–L′) show distribution of DE-cadherin (red) and F-actin (green) in border cells at stage 9. F-actin is concentrated in the periphery of the border cell cluster. (J) Border cells at the onset of migration and (K) during mid migration. Note the round centrally located polar cells with constricted apical cell surfaces that are rich in DE-cadherin and F-actin. (L) and (L′) show two confocal sections of the same cluster. The arrows in L′ point to the constricted apical surfaces of the polar cells. Anterior is to the left in all panels. Bars: (A–C) 50 μm; (D–G, J–L′) 10 μm; (H and I) 10 μm.

Mentions: The border cells consist of the two anterior polar cells and an average of 6 additional follicle cells. DE-cadherin expression increases in these cells shortly before they segregate from the follicular epithelium (Fig. 2). Closer examination of migrating border cells revealed that the polar cells behave very differently from the other cells in the cluster. The polar cells upregulate DE-cadherin expression, constrict their apical surfaces, and assume a round shape at stage 4/5, long before the border cell cluster forms (Fig. 2 D). At stage 8, follicle cells next to the polar cells upregulate DE-cadherin expression (Fig. 2 E). At late stage 8, the border cells segregate from the follicular epithelium and DE-cadherin becomes distributed rather uniformly over the surface of the border cells (Fig. 2 F). At early stage 9, border cell migration is initiated by a single border cell that extends a process between nurse cells. This border cell is never a polar cell (Fig. 2, G and J). In fact, here and during the entire migration process the polar cells occupy a central position in the border cell cluster (see also Edwards et al., 1997), and maintain their constricted apical surface and round shapes (Fig. 2, H and J–L′). The polar cells can be specifically addressed with anti–Fasciclin III antibodies (Brower et al., 1980; Patel et al., 1987) that label most prominently the contact surface of the two polar cells (Fig. 2, F and H). The other border cells in the cluster form a single layered rosette that surrounds the polar cells (we will refer to these cells as rosette cells; Fig. 2, H, K, and L). In the migrating border cell cluster the highest concentration of DE-cadherin is found at the contact sites between rosette cells and polar cells and between adjacent rosette cells (Fig. 2 H). At the interface between rosette cells and nurse cells substantially lower amounts of DE-cadherin are seen. Here, DE-cadherin is distributed in a punctate pattern that might represent surface clusters or intracellular vesicles (Fig. 2 H), and might be a consequence of a high turn-over rate of DE-cadherin at the interface between rosette cells and nurse cells. In contrast to DE-cadherin, the highest concentration of F-actin in rosette cells is found in the region of the cytocortex that contacts the nurse cells whereas lower levels of F-actin are seen at contact sites between border cells (Fig. 2, J–L). The high concentration of F-actin in the periphery of the border cell cluster is consistent with a role of actin polymerization in border cell migration (see also Murphy and Montell, 1996; Oda et al., 1997). Our results show that the border cell cluster has a two-dimensional organization and suggest that the polar cells maintain aspects of epithelial polarity during migration.


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

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

Expression of DE-cadherin in border cells of  wild-type ovaries. (A–C) Arrows point to border cells.  (A) At early stage 9 border  cells have accumulated high  levels of DE-cadherin before migration is initiated.  (B) Border cells expressing  elevated levels of DE-cadherin migrate on a straight  path through the center of  the follicle towards the oocyte during stage 9. (C) After  border cells have reached the  oocyte that fills the posterior  half of a follicle at stage 10a,  they maintain high levels of  DE-cadherin expression for  some time and move slightly  dorsally. (D–I) show high  resolution images of DE-cadherin (red) expression in border cells. (F–H) show follicles that are counterstained  for Fasciclin III (green) that  serves as a marker for the  two polar cells. Fasciclin III  accumulates at the contact  surface between polar cells.  (D) Stage 6. Anterior polar  cells contain more DE-cadherin than neighboring follicle cells. Polar cells are constricted apically (arrow) and  have a rounded shape. DE-cadherin is concentrated at the zonula adherens. (E) Stage 8. Follicle cells adjacent to polar cells have upregulated DE-cadherin expression (arrows). (F) Early stage 9. Same follicle as in A. DE-cadherin distribution in follicle cells adjacent to polar cells (the rosette cells)  has depolarized. (G) Early stage 9. Migration is initiated by a rosette cell penetrating between nurse cells (arrow). (H) Late stage 9.  Same follicle as in B. During migration polar cells have a central position and are surrounded by rosette cells. Highest concentration of  DE-cadherin is seen at the contact surfaces between rosette cells and polar cells and between rosette cells. Lower amounts of DE-cadherin are seen at the interface of rosette cells and nurse cells in a punctate pattern (arrow). (I) Stage 10a. Border cells have established  contact to the surface of the oocyte (white line). The polar cells are centrally located and their constricted apical surface contacts the oocyte (see also Peifer et al., 1993). (J–L′) show distribution of DE-cadherin (red) and F-actin (green) in border cells at stage 9. F-actin is  concentrated in the periphery of the border cell cluster. (J) Border cells at the onset of migration and (K) during mid migration. Note  the round centrally located polar cells with constricted apical cell surfaces that are rich in DE-cadherin and F-actin. (L) and (L′) show  two confocal sections of the same cluster. The arrows in L′ point to the constricted apical surfaces of the polar cells. Anterior is to the  left in all panels. Bars: (A–C) 50 μm; (D–G, J–L′) 10 μm; (H and I) 10 μm.
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Related In: Results  -  Collection

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Figure 2: Expression of DE-cadherin in border cells of wild-type ovaries. (A–C) Arrows point to border cells. (A) At early stage 9 border cells have accumulated high levels of DE-cadherin before migration is initiated. (B) Border cells expressing elevated levels of DE-cadherin migrate on a straight path through the center of the follicle towards the oocyte during stage 9. (C) After border cells have reached the oocyte that fills the posterior half of a follicle at stage 10a, they maintain high levels of DE-cadherin expression for some time and move slightly dorsally. (D–I) show high resolution images of DE-cadherin (red) expression in border cells. (F–H) show follicles that are counterstained for Fasciclin III (green) that serves as a marker for the two polar cells. Fasciclin III accumulates at the contact surface between polar cells. (D) Stage 6. Anterior polar cells contain more DE-cadherin than neighboring follicle cells. Polar cells are constricted apically (arrow) and have a rounded shape. DE-cadherin is concentrated at the zonula adherens. (E) Stage 8. Follicle cells adjacent to polar cells have upregulated DE-cadherin expression (arrows). (F) Early stage 9. Same follicle as in A. DE-cadherin distribution in follicle cells adjacent to polar cells (the rosette cells) has depolarized. (G) Early stage 9. Migration is initiated by a rosette cell penetrating between nurse cells (arrow). (H) Late stage 9. Same follicle as in B. During migration polar cells have a central position and are surrounded by rosette cells. Highest concentration of DE-cadherin is seen at the contact surfaces between rosette cells and polar cells and between rosette cells. Lower amounts of DE-cadherin are seen at the interface of rosette cells and nurse cells in a punctate pattern (arrow). (I) Stage 10a. Border cells have established contact to the surface of the oocyte (white line). The polar cells are centrally located and their constricted apical surface contacts the oocyte (see also Peifer et al., 1993). (J–L′) show distribution of DE-cadherin (red) and F-actin (green) in border cells at stage 9. F-actin is concentrated in the periphery of the border cell cluster. (J) Border cells at the onset of migration and (K) during mid migration. Note the round centrally located polar cells with constricted apical cell surfaces that are rich in DE-cadherin and F-actin. (L) and (L′) show two confocal sections of the same cluster. The arrows in L′ point to the constricted apical surfaces of the polar cells. Anterior is to the left in all panels. Bars: (A–C) 50 μm; (D–G, J–L′) 10 μm; (H and I) 10 μm.
Mentions: The border cells consist of the two anterior polar cells and an average of 6 additional follicle cells. DE-cadherin expression increases in these cells shortly before they segregate from the follicular epithelium (Fig. 2). Closer examination of migrating border cells revealed that the polar cells behave very differently from the other cells in the cluster. The polar cells upregulate DE-cadherin expression, constrict their apical surfaces, and assume a round shape at stage 4/5, long before the border cell cluster forms (Fig. 2 D). At stage 8, follicle cells next to the polar cells upregulate DE-cadherin expression (Fig. 2 E). At late stage 8, the border cells segregate from the follicular epithelium and DE-cadherin becomes distributed rather uniformly over the surface of the border cells (Fig. 2 F). At early stage 9, border cell migration is initiated by a single border cell that extends a process between nurse cells. This border cell is never a polar cell (Fig. 2, G and J). In fact, here and during the entire migration process the polar cells occupy a central position in the border cell cluster (see also Edwards et al., 1997), and maintain their constricted apical surface and round shapes (Fig. 2, H and J–L′). The polar cells can be specifically addressed with anti–Fasciclin III antibodies (Brower et al., 1980; Patel et al., 1987) that label most prominently the contact surface of the two polar cells (Fig. 2, F and H). The other border cells in the cluster form a single layered rosette that surrounds the polar cells (we will refer to these cells as rosette cells; Fig. 2, H, K, and L). In the migrating border cell cluster the highest concentration of DE-cadherin is found at the contact sites between rosette cells and polar cells and between adjacent rosette cells (Fig. 2 H). At the interface between rosette cells and nurse cells substantially lower amounts of DE-cadherin are seen. Here, DE-cadherin is distributed in a punctate pattern that might represent surface clusters or intracellular vesicles (Fig. 2 H), and might be a consequence of a high turn-over rate of DE-cadherin at the interface between rosette cells and nurse cells. In contrast to DE-cadherin, the highest concentration of F-actin in rosette cells is found in the region of the cytocortex that contacts the nurse cells whereas lower levels of F-actin are seen at contact sites between border cells (Fig. 2, J–L). The high concentration of F-actin in the periphery of the border cell cluster is consistent with a role of actin polymerization in border cell migration (see also Murphy and Montell, 1996; Oda et al., 1997). Our results show that the border cell cluster has a two-dimensional organization and suggest that the polar cells maintain aspects of epithelial polarity during 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