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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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Oocyte distortion and centripetal cell migration defects in karst mutant egg chambers. (A) Midregion of a sagittal section through a stage 10A-B karst mutant egg chamber costained for actin and DE-cadherin. Note the distorted interface between nurse cells and oocyte (between arrowheads). (B) Midregion of a stage 10B karst mutant egg chamber costained for α-spectrin and propidium iodide. In this severe case, the centripetal cells of the incompletely migrated follicle cell layer have disrupted the nurse cell cluster and incorporated a nurse cell nucleus (arrow) into the oocyte. Both channels were flattened into a grayscale image in each panel. Anterior is to the left in both panels. Scale bars, 50 μm.
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Figure 3: Oocyte distortion and centripetal cell migration defects in karst mutant egg chambers. (A) Midregion of a sagittal section through a stage 10A-B karst mutant egg chamber costained for actin and DE-cadherin. Note the distorted interface between nurse cells and oocyte (between arrowheads). (B) Midregion of a stage 10B karst mutant egg chamber costained for α-spectrin and propidium iodide. In this severe case, the centripetal cells of the incompletely migrated follicle cell layer have disrupted the nurse cell cluster and incorporated a nurse cell nucleus (arrow) into the oocyte. Both channels were flattened into a grayscale image in each panel. Anterior is to the left in both panels. Scale bars, 50 μm.

Mentions: Consistent with the hypothesis that the primary morphogenetic defect lies in follicle cell migration, some follicle cells in karst mutant egg chambers often remain in contact with the nurse cell membranes at stage 10A. These follicle cells still attempt to make the appropriate adhesive contacts with the oocyte membrane (Goode et al. 1996), pulling the oocyte membrane towards them and grossly distorting the nurse cells/oocyte interface (Fig. 3 A). In most cases, the subsequent inward migration of the follicle cell layer at stage 10B proceeds along the nurse cell/oocyte interface in a relatively normal fashion. However, in rare, extreme cases, the centripetally migrating cells penetrate between nearby nurse cell membranes and cause one or more nurse cells to become included within the egg along with the oocyte (Fig. 3 B).


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

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

Oocyte distortion and centripetal cell migration defects in karst mutant egg chambers. (A) Midregion of a sagittal section through a stage 10A-B karst mutant egg chamber costained for actin and DE-cadherin. Note the distorted interface between nurse cells and oocyte (between arrowheads). (B) Midregion of a stage 10B karst mutant egg chamber costained for α-spectrin and propidium iodide. In this severe case, the centripetal cells of the incompletely migrated follicle cell layer have disrupted the nurse cell cluster and incorporated a nurse cell nucleus (arrow) into the oocyte. Both channels were flattened into a grayscale image in each panel. Anterior is to the left in both panels. Scale bars, 50 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2169487&req=5

Figure 3: Oocyte distortion and centripetal cell migration defects in karst mutant egg chambers. (A) Midregion of a sagittal section through a stage 10A-B karst mutant egg chamber costained for actin and DE-cadherin. Note the distorted interface between nurse cells and oocyte (between arrowheads). (B) Midregion of a stage 10B karst mutant egg chamber costained for α-spectrin and propidium iodide. In this severe case, the centripetal cells of the incompletely migrated follicle cell layer have disrupted the nurse cell cluster and incorporated a nurse cell nucleus (arrow) into the oocyte. Both channels were flattened into a grayscale image in each panel. Anterior is to the left in both panels. Scale bars, 50 μm.
Mentions: Consistent with the hypothesis that the primary morphogenetic defect lies in follicle cell migration, some follicle cells in karst mutant egg chambers often remain in contact with the nurse cell membranes at stage 10A. These follicle cells still attempt to make the appropriate adhesive contacts with the oocyte membrane (Goode et al. 1996), pulling the oocyte membrane towards them and grossly distorting the nurse cells/oocyte interface (Fig. 3 A). In most cases, the subsequent inward migration of the follicle cell layer at stage 10B proceeds along the nurse cell/oocyte interface in a relatively normal fashion. However, in rare, extreme cases, the centripetally migrating cells penetrate between nearby nurse cell membranes and cause one or more nurse cells to become included within the egg along with the oocyte (Fig. 3 B).

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