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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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βH is required for a stable spectrin membrane skeleton in the apical domain. Part of three follicle cell monolayers costained for α-spectrin (A, C, and E) and β-spectrin (B, D, and F) are shown. (A and B) Wild-type follicle cell monolayer. Arrowhead indicates an example of α-spectrin in the apical domain. Both α- and β-spectrins stain the lateral membranes. (C–F) two examples of karst mutant follicle cell monolayers (kst01318 in C and D, kst2/Df(3L)1226 in E and F). α-Spectrin is no longer present at the apical membrane domain (C and E, arrowheads), and there is no change in the distribution of β-spectrin in any allelic combination (D and F). Scale bar represents 10 μm. The strong staining on the basal side of the epithelia corresponds to the surrounding muscle sheath.
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Figure 7: βH is required for a stable spectrin membrane skeleton in the apical domain. Part of three follicle cell monolayers costained for α-spectrin (A, C, and E) and β-spectrin (B, D, and F) are shown. (A and B) Wild-type follicle cell monolayer. Arrowhead indicates an example of α-spectrin in the apical domain. Both α- and β-spectrins stain the lateral membranes. (C–F) two examples of karst mutant follicle cell monolayers (kst01318 in C and D, kst2/Df(3L)1226 in E and F). α-Spectrin is no longer present at the apical membrane domain (C and E, arrowheads), and there is no change in the distribution of β-spectrin in any allelic combination (D and F). Scale bar represents 10 μm. The strong staining on the basal side of the epithelia corresponds to the surrounding muscle sheath.

Mentions: βH is no longer detectable at the apical domain of the follicle cells in any allelic combination of karst alleles that we have examined (data not shown). The localization of βH to the apical domain has been previously shown to be dependent on α-spectrin (Lee et al. 1997). To see if α-spectrin is dependent on βH for its localization to the apical domain, and to confirm that no apical spectrin function remains in karst mutants, we examined the distribution of α-spectrin in karst follicle cells. While the lateral α-spectrin distribution is unaffected by this mutation, apical α-spectrin is no longer detectable by immunofluorescence (Fig. 7C and Fig. E). This indicates that the stable recruitment of α-spectrin to the apical domain is dependent on βH, and that there is thus a mutual interdependence between α-spectrin and βH. This further suggests that αβH-spectrin is recruited to the apical domain as a heterodimer or tetramer, or that following separate recruitment only the dimers or tetramers remain stably associated with the apical domain.


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

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

βH is required for a stable spectrin membrane skeleton in the apical domain. Part of three follicle cell monolayers costained for α-spectrin (A, C, and E) and β-spectrin (B, D, and F) are shown. (A and B) Wild-type follicle cell monolayer. Arrowhead indicates an example of α-spectrin in the apical domain. Both α- and β-spectrins stain the lateral membranes. (C–F) two examples of karst mutant follicle cell monolayers (kst01318 in C and D, kst2/Df(3L)1226 in E and F). α-Spectrin is no longer present at the apical membrane domain (C and E, arrowheads), and there is no change in the distribution of β-spectrin in any allelic combination (D and F). Scale bar represents 10 μm. The strong staining on the basal side of the epithelia corresponds to the surrounding muscle sheath.
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Related In: Results  -  Collection

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Figure 7: βH is required for a stable spectrin membrane skeleton in the apical domain. Part of three follicle cell monolayers costained for α-spectrin (A, C, and E) and β-spectrin (B, D, and F) are shown. (A and B) Wild-type follicle cell monolayer. Arrowhead indicates an example of α-spectrin in the apical domain. Both α- and β-spectrins stain the lateral membranes. (C–F) two examples of karst mutant follicle cell monolayers (kst01318 in C and D, kst2/Df(3L)1226 in E and F). α-Spectrin is no longer present at the apical membrane domain (C and E, arrowheads), and there is no change in the distribution of β-spectrin in any allelic combination (D and F). Scale bar represents 10 μm. The strong staining on the basal side of the epithelia corresponds to the surrounding muscle sheath.
Mentions: βH is no longer detectable at the apical domain of the follicle cells in any allelic combination of karst alleles that we have examined (data not shown). The localization of βH to the apical domain has been previously shown to be dependent on α-spectrin (Lee et al. 1997). To see if α-spectrin is dependent on βH for its localization to the apical domain, and to confirm that no apical spectrin function remains in karst mutants, we examined the distribution of α-spectrin in karst follicle cells. While the lateral α-spectrin distribution is unaffected by this mutation, apical α-spectrin is no longer detectable by immunofluorescence (Fig. 7C and Fig. E). This indicates that the stable recruitment of α-spectrin to the apical domain is dependent on βH, and that there is thus a mutual interdependence between α-spectrin and βH. This further suggests that αβH-spectrin is recruited to the apical domain as a heterodimer or tetramer, or that following separate recruitment only the dimers or tetramers remain stably associated with the apical domain.

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