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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 during wild-type oogenesis. (A and B) A germarium, double-stained for  DE-cadherin (A) and F-actin  (B). DE-cadherin expression  is seen throughout the germarium (g), in germline cells and  somatic cells except for the  terminal filament. A previously unidentified group of  6–7 somatic cells close to the  base of the terminal filament  is strongly stained (arrow).  Low levels of DE-cadherin  are detected in the anterior  region of the germarium  where germline stem cells  and early cystoblasts are located. Posterior to this region  strong DE-cadherin expression is seen in the germline  cells and all somatic cells. The  DE-cadherin expression in  the germarium was described  in more detail elsewhere  (Godt and Tepass, 1998). (C)  Throughout oogenesis DE-cadherin is expressed in the  follicular epithelium and the  germline cells of follicles. Anterior and posterior polar  cells (arrows) show a higher  level of expression than the  remaining follicle cells during stages 4–7. (D) The highest amounts of DE-cadherin  are seen in two migrating follicle cell populations, the border cells (arrow) and the centripetal cells (arrowheads).  (E) shows a top view of the  DE-cadherin expression pattern in the follicular epithelium at stage 14. (F) shows  DE-cadherin distribution in  the dorsal appendages (arrow) and in the part of the follicular epithelium that covers the anterior side of the oocyte including the micropyle (arrowhead). This part of the follicular epithelium is composed of the border cells and the centripetal cells. Anterior is to the left in  all panels. s, stage; TF, terminal filament; IS, interfollicular stalk. Bars: (A and B) 50 μm; (C, D, and F) 50 μm; (E) 15 μm.
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Figure 1: Expression of DE-cadherin during wild-type oogenesis. (A and B) A germarium, double-stained for DE-cadherin (A) and F-actin (B). DE-cadherin expression is seen throughout the germarium (g), in germline cells and somatic cells except for the terminal filament. A previously unidentified group of 6–7 somatic cells close to the base of the terminal filament is strongly stained (arrow). Low levels of DE-cadherin are detected in the anterior region of the germarium where germline stem cells and early cystoblasts are located. Posterior to this region strong DE-cadherin expression is seen in the germline cells and all somatic cells. The DE-cadherin expression in the germarium was described in more detail elsewhere (Godt and Tepass, 1998). (C) Throughout oogenesis DE-cadherin is expressed in the follicular epithelium and the germline cells of follicles. Anterior and posterior polar cells (arrows) show a higher level of expression than the remaining follicle cells during stages 4–7. (D) The highest amounts of DE-cadherin are seen in two migrating follicle cell populations, the border cells (arrow) and the centripetal cells (arrowheads). (E) shows a top view of the DE-cadherin expression pattern in the follicular epithelium at stage 14. (F) shows DE-cadherin distribution in the dorsal appendages (arrow) and in the part of the follicular epithelium that covers the anterior side of the oocyte including the micropyle (arrowhead). This part of the follicular epithelium is composed of the border cells and the centripetal cells. Anterior is to the left in all panels. s, stage; TF, terminal filament; IS, interfollicular stalk. Bars: (A and B) 50 μm; (C, D, and F) 50 μm; (E) 15 μm.

Mentions: DE-cadherin shows a dynamic expression pattern during follicular morphogenesis. DE-cadherin is expressed in the germline throughout oogenesis, with the possible exception of the germline stem cells and early cystoblasts in the germarium. Furthermore, DE-cadherin is expressed in all somatic cells in the germarium and the follicles, except for the terminal filaments in which DE-cadherin was not detected (Fig. 1, A–D). High levels of DE-cadherin are found in a honeycomb pattern in the follicular epithelium that corresponds to the zonulae adherentes (Fig. 1 E). Lower levels of DE-cadherin are seen along the lateral surfaces of follicle cells and on the surfaces of the germ-line cells (Fig. 1, C and D). Expression of DE-cadherin is upregulated in various cell populations during oogenesis. In the germarium increased concentrations of DE-cadherin are seen in the oocyte and the anterior and posterior follicle cells. This differential expression of DE-cadherin promotes a cell sorting process that is responsible for posterior oocyte localization (Godt and Tepass, 1998). From stage 4/5 of oogenesis onwards increased levels of DE-cadherin are seen in a pair of follicle cells at the anterior and posterior pole, respectively, called the polar cells (Fig. 1 C). The anterior polar cells become part of the border cell cluster that forms during stage 8. The border cells and the centripetal cells express high levels of DE-cadherin during their migration as described in more detail below (Fig. 1 D). The distribution of the shg transcript as assayed by tissue in situ hybridization and a lacZ reporter (shgP34-1; Tepass et al., 1996; Godt and Tepass, 1998) is similar to the protein distribution. An exception are the dorsal appendages in which only the level of the mRNA but not the level of the protein is increased (Fig. 1 F; data not shown). Taken together, the shg/DE-cadherin expression profile during oogenesis suggests a possible role for DE-cadherin in maintaining the integrity of the follicular epithelium and, in particular, in the dynamic movements of border cells and centripetal cells.


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

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

Expression of DE-cadherin during wild-type oogenesis. (A and B) A germarium, double-stained for  DE-cadherin (A) and F-actin  (B). DE-cadherin expression  is seen throughout the germarium (g), in germline cells and  somatic cells except for the  terminal filament. A previously unidentified group of  6–7 somatic cells close to the  base of the terminal filament  is strongly stained (arrow).  Low levels of DE-cadherin  are detected in the anterior  region of the germarium  where germline stem cells  and early cystoblasts are located. Posterior to this region  strong DE-cadherin expression is seen in the germline  cells and all somatic cells. The  DE-cadherin expression in  the germarium was described  in more detail elsewhere  (Godt and Tepass, 1998). (C)  Throughout oogenesis DE-cadherin is expressed in the  follicular epithelium and the  germline cells of follicles. Anterior and posterior polar  cells (arrows) show a higher  level of expression than the  remaining follicle cells during stages 4–7. (D) The highest amounts of DE-cadherin  are seen in two migrating follicle cell populations, the border cells (arrow) and the centripetal cells (arrowheads).  (E) shows a top view of the  DE-cadherin expression pattern in the follicular epithelium at stage 14. (F) shows  DE-cadherin distribution in  the dorsal appendages (arrow) and in the part of the follicular epithelium that covers the anterior side of the oocyte including the micropyle (arrowhead). This part of the follicular epithelium is composed of the border cells and the centripetal cells. Anterior is to the left in  all panels. s, stage; TF, terminal filament; IS, interfollicular stalk. Bars: (A and B) 50 μm; (C, D, and F) 50 μm; (E) 15 μm.
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Figure 1: Expression of DE-cadherin during wild-type oogenesis. (A and B) A germarium, double-stained for DE-cadherin (A) and F-actin (B). DE-cadherin expression is seen throughout the germarium (g), in germline cells and somatic cells except for the terminal filament. A previously unidentified group of 6–7 somatic cells close to the base of the terminal filament is strongly stained (arrow). Low levels of DE-cadherin are detected in the anterior region of the germarium where germline stem cells and early cystoblasts are located. Posterior to this region strong DE-cadherin expression is seen in the germline cells and all somatic cells. The DE-cadherin expression in the germarium was described in more detail elsewhere (Godt and Tepass, 1998). (C) Throughout oogenesis DE-cadherin is expressed in the follicular epithelium and the germline cells of follicles. Anterior and posterior polar cells (arrows) show a higher level of expression than the remaining follicle cells during stages 4–7. (D) The highest amounts of DE-cadherin are seen in two migrating follicle cell populations, the border cells (arrow) and the centripetal cells (arrowheads). (E) shows a top view of the DE-cadherin expression pattern in the follicular epithelium at stage 14. (F) shows DE-cadherin distribution in the dorsal appendages (arrow) and in the part of the follicular epithelium that covers the anterior side of the oocyte including the micropyle (arrowhead). This part of the follicular epithelium is composed of the border cells and the centripetal cells. Anterior is to the left in all panels. s, stage; TF, terminal filament; IS, interfollicular stalk. Bars: (A and B) 50 μm; (C, D, and F) 50 μm; (E) 15 μm.
Mentions: DE-cadherin shows a dynamic expression pattern during follicular morphogenesis. DE-cadherin is expressed in the germline throughout oogenesis, with the possible exception of the germline stem cells and early cystoblasts in the germarium. Furthermore, DE-cadherin is expressed in all somatic cells in the germarium and the follicles, except for the terminal filaments in which DE-cadherin was not detected (Fig. 1, A–D). High levels of DE-cadherin are found in a honeycomb pattern in the follicular epithelium that corresponds to the zonulae adherentes (Fig. 1 E). Lower levels of DE-cadherin are seen along the lateral surfaces of follicle cells and on the surfaces of the germ-line cells (Fig. 1, C and D). Expression of DE-cadherin is upregulated in various cell populations during oogenesis. In the germarium increased concentrations of DE-cadherin are seen in the oocyte and the anterior and posterior follicle cells. This differential expression of DE-cadherin promotes a cell sorting process that is responsible for posterior oocyte localization (Godt and Tepass, 1998). From stage 4/5 of oogenesis onwards increased levels of DE-cadherin are seen in a pair of follicle cells at the anterior and posterior pole, respectively, called the polar cells (Fig. 1 C). The anterior polar cells become part of the border cell cluster that forms during stage 8. The border cells and the centripetal cells express high levels of DE-cadherin during their migration as described in more detail below (Fig. 1 D). The distribution of the shg transcript as assayed by tissue in situ hybridization and a lacZ reporter (shgP34-1; Tepass et al., 1996; Godt and Tepass, 1998) is similar to the protein distribution. An exception are the dorsal appendages in which only the level of the mRNA but not the level of the protein is increased (Fig. 1 F; data not shown). Taken together, the shg/DE-cadherin expression profile during oogenesis suggests a possible role for DE-cadherin in maintaining the integrity of the follicular epithelium and, in particular, in the dynamic movements of border cells and centripetal cells.

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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Related in: MedlinePlus