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Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila.

Zarnescu DC, Thomas GH - J. Cell Biol. (1999)

Bottom Line: We report that apical beta(Heavy)-spectrin (beta(H)), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis.Elimination of beta(H) prevents the stable recruitment of alpha-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity.These results demonstrate a direct role for apical (alphabeta(H))(2)-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.

ABSTRACT
Changes in cell shape and position drive morphogenesis in epithelia and depend on the polarized nature of its constituent cells. The spectrin-based membrane skeleton is thought to be a key player in the establishment and/or maintenance of cell shape and polarity. We report that apical beta(Heavy)-spectrin (beta(H)), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis. Elimination of beta(H) by the karst mutation prevents apical constriction of the follicle cells during mid-oogenesis, and is accompanied by a gross breakup of the zonula adherens. We also report that the integrity of the migratory border cell cluster, a group of anterior follicle cells that delaminates from the follicle epithelium, is disrupted. Elimination of beta(H) prevents the stable recruitment of alpha-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity. These results demonstrate a direct role for apical (alphabeta(H))(2)-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.

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karst follicle cells fail to constrict their apices over the oocyte. (A) Plot of 578 wild-type apical cell areas from 17 egg chambers (black line) and 603 karst mutant apical cell areas from 19 egg chambers (gray line) versus each cell's position on the anterior–posterior axis. The origin of the x axis corresponds to the boundary between the nurse cell cluster and the oocyte. Each line is a rolling average (window size = 10 pixels). (B) Histograms representing the distribution of apical surface areas from those follicle cells residing on the oocyte. Data was grouped as follows: bin 1 = 0–50 pixels, bin 2 = 51–100 pixels, bin 3 = 101–150 pixels, etc., up to bin 19 = 901–950 pixels.
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Figure 4: karst follicle cells fail to constrict their apices over the oocyte. (A) Plot of 578 wild-type apical cell areas from 17 egg chambers (black line) and 603 karst mutant apical cell areas from 19 egg chambers (gray line) versus each cell's position on the anterior–posterior axis. The origin of the x axis corresponds to the boundary between the nurse cell cluster and the oocyte. Each line is a rolling average (window size = 10 pixels). (B) Histograms representing the distribution of apical surface areas from those follicle cells residing on the oocyte. Data was grouped as follows: bin 1 = 0–50 pixels, bin 2 = 51–100 pixels, bin 3 = 101–150 pixels, etc., up to bin 19 = 901–950 pixels.

Mentions: The failure of karst follicle cells to complete their migration onto the oocyte by the onset of stage 10B implies that the total apical surface area of the epithelium is greater than that of the oocyte membrane. Moreover, karst mutant follicle cells often appear to have a more cuboidal shape than in the wild-type (see Fig. 5G and Fig. H). Since there is no over-proliferation in the mutant monolayer (data not shown), this cannot arise due to an increase in cell number. However, an inability of karst follicle cells to properly change their cell shape or constrain their apical surface area at the appropriate size would explain this observation. We therefore compared the apical surface area of wild-type and mutant follicle cells during monolayer migration. This analysis reveals a sharp decrease in the apical surface area of the wild-type follicle cells as they approach and migrate onto the oocyte (Fig. 4 A). In contrast, the majority of karst mutant follicle cells fail to apically constrict (Fig. 4 A). The mean apical surface area of the mutant follicle cells is almost twice that of the wild-type (Fig. 4 B). Moreover, comparison of the apical surface areas of mutant follicle cells in chambers during migration with those where migration has been completed reveals a slight increase (Table ; P < 0.001). This suggests that, in addition to the constriction defect, the monolayer cannot withstand the forces exerted by the growing oocyte.


Apical spectrin is essential for epithelial morphogenesis but not apicobasal polarity in Drosophila.

Zarnescu DC, Thomas GH - J. Cell Biol. (1999)

karst follicle cells fail to constrict their apices over the oocyte. (A) Plot of 578 wild-type apical cell areas from 17 egg chambers (black line) and 603 karst mutant apical cell areas from 19 egg chambers (gray line) versus each cell's position on the anterior–posterior axis. The origin of the x axis corresponds to the boundary between the nurse cell cluster and the oocyte. Each line is a rolling average (window size = 10 pixels). (B) Histograms representing the distribution of apical surface areas from those follicle cells residing on the oocyte. Data was grouped as follows: bin 1 = 0–50 pixels, bin 2 = 51–100 pixels, bin 3 = 101–150 pixels, etc., up to bin 19 = 901–950 pixels.
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Related In: Results  -  Collection

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Figure 4: karst follicle cells fail to constrict their apices over the oocyte. (A) Plot of 578 wild-type apical cell areas from 17 egg chambers (black line) and 603 karst mutant apical cell areas from 19 egg chambers (gray line) versus each cell's position on the anterior–posterior axis. The origin of the x axis corresponds to the boundary between the nurse cell cluster and the oocyte. Each line is a rolling average (window size = 10 pixels). (B) Histograms representing the distribution of apical surface areas from those follicle cells residing on the oocyte. Data was grouped as follows: bin 1 = 0–50 pixels, bin 2 = 51–100 pixels, bin 3 = 101–150 pixels, etc., up to bin 19 = 901–950 pixels.
Mentions: The failure of karst follicle cells to complete their migration onto the oocyte by the onset of stage 10B implies that the total apical surface area of the epithelium is greater than that of the oocyte membrane. Moreover, karst mutant follicle cells often appear to have a more cuboidal shape than in the wild-type (see Fig. 5G and Fig. H). Since there is no over-proliferation in the mutant monolayer (data not shown), this cannot arise due to an increase in cell number. However, an inability of karst follicle cells to properly change their cell shape or constrain their apical surface area at the appropriate size would explain this observation. We therefore compared the apical surface area of wild-type and mutant follicle cells during monolayer migration. This analysis reveals a sharp decrease in the apical surface area of the wild-type follicle cells as they approach and migrate onto the oocyte (Fig. 4 A). In contrast, the majority of karst mutant follicle cells fail to apically constrict (Fig. 4 A). The mean apical surface area of the mutant follicle cells is almost twice that of the wild-type (Fig. 4 B). Moreover, comparison of the apical surface areas of mutant follicle cells in chambers during migration with those where migration has been completed reveals a slight increase (Table ; P < 0.001). This suggests that, in addition to the constriction defect, the monolayer cannot withstand the forces exerted by the growing oocyte.

Bottom Line: We report that apical beta(Heavy)-spectrin (beta(H)), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis.Elimination of beta(H) prevents the stable recruitment of alpha-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity.These results demonstrate a direct role for apical (alphabeta(H))(2)-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, USA.

ABSTRACT
Changes in cell shape and position drive morphogenesis in epithelia and depend on the polarized nature of its constituent cells. The spectrin-based membrane skeleton is thought to be a key player in the establishment and/or maintenance of cell shape and polarity. We report that apical beta(Heavy)-spectrin (beta(H)), a terminal web protein that is also associated with the zonula adherens, is essential for normal epithelial morphogenesis of the Drosophila follicle cell epithelium during oogenesis. Elimination of beta(H) by the karst mutation prevents apical constriction of the follicle cells during mid-oogenesis, and is accompanied by a gross breakup of the zonula adherens. We also report that the integrity of the migratory border cell cluster, a group of anterior follicle cells that delaminates from the follicle epithelium, is disrupted. Elimination of beta(H) prevents the stable recruitment of alpha-spectrin to the apical domain, but does not result in a loss of apicobasal polarity, as would be predicted from current models describing the role of spectrin in the establishment of cell polarity. These results demonstrate a direct role for apical (alphabeta(H))(2)-spectrin in epithelial morphogenesis driven by apical contraction, and suggest that apical and basolateral spectrin do not play identical roles in the generation of apicobasal polarity.

Show MeSH
Related in: MedlinePlus