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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 distribution during oogenesis. (A–E) Wild-type ovariole costained for βH (top) and α-spectrin (bottom). The middle panels are merged false color images with βH in green and α-spectrin in red. Representative chambers for stages 1–10 are shown. Specific stages are indicated by the boxed numbers. (A) βH is uniformly distributed along the germ cell membranes and is apically polarized in the follicle cell monolayer. βH is also strongly expressed in stalks (arrow) and exhibits a patchy distribution on the border cell track during stage 9 (arrowhead). Scale bar, 50 μm. (B) High magnification view of a wild-type germarium indicating the location of zones 1–3. βH is strongly expressed in the terminal filament and cap cells (TF/CC) but is absent from fusomes marked by α-spectrin (arrow). Scale bar, 10 μm. (C) Nurse cell cluster of a stage 11 egg chamber. βH is seen faintly in filamentous structures within the dumping nurse cells. βH reappears at the apical domain of the border cells (arrowhead; see also E). Scale bar, 50 μm in C–E. (D and E) Anterior ends of stages 12, 13, and 14 egg chambers, respectively. βH is strongly expressed at the apical surface of follicle cells that are actively secreting chorion (arrow in D indicates the cells forming the dorsal appendages; arrowheads in C and E point to the border cells that secrete the micropyle). The nurse cells between the emerging dorsal appendages in D are undergoing programmed cell death. (F) High magnification view of a ring canal showing a slight enrichment of βH (left) on the outer rim of this actin rich structure (right). (G) En face high magnification view of the apical domain of follicle cells showing βH at the terminal web (left) and DE-cadherin (right) at the ZA. The central panels in F and G are merged false color images with the left and right panels of each in green and red, respectively. Bars: (F and G) 10 μm.
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Figure 1: βH distribution during oogenesis. (A–E) Wild-type ovariole costained for βH (top) and α-spectrin (bottom). The middle panels are merged false color images with βH in green and α-spectrin in red. Representative chambers for stages 1–10 are shown. Specific stages are indicated by the boxed numbers. (A) βH is uniformly distributed along the germ cell membranes and is apically polarized in the follicle cell monolayer. βH is also strongly expressed in stalks (arrow) and exhibits a patchy distribution on the border cell track during stage 9 (arrowhead). Scale bar, 50 μm. (B) High magnification view of a wild-type germarium indicating the location of zones 1–3. βH is strongly expressed in the terminal filament and cap cells (TF/CC) but is absent from fusomes marked by α-spectrin (arrow). Scale bar, 10 μm. (C) Nurse cell cluster of a stage 11 egg chamber. βH is seen faintly in filamentous structures within the dumping nurse cells. βH reappears at the apical domain of the border cells (arrowhead; see also E). Scale bar, 50 μm in C–E. (D and E) Anterior ends of stages 12, 13, and 14 egg chambers, respectively. βH is strongly expressed at the apical surface of follicle cells that are actively secreting chorion (arrow in D indicates the cells forming the dorsal appendages; arrowheads in C and E point to the border cells that secrete the micropyle). The nurse cells between the emerging dorsal appendages in D are undergoing programmed cell death. (F) High magnification view of a ring canal showing a slight enrichment of βH (left) on the outer rim of this actin rich structure (right). (G) En face high magnification view of the apical domain of follicle cells showing βH at the terminal web (left) and DE-cadherin (right) at the ZA. The central panels in F and G are merged false color images with the left and right panels of each in green and red, respectively. Bars: (F and G) 10 μm.

Mentions: Oogenesis in flies takes place in ovaries formed of 12–16 ovarioles, each of which consists of an anterior structure called the germarium and several egg chambers sequentially ordered with regard to their developmental stage (for review, see Spradling 1993; see Fig. 1 A for example). The germarium is comprised of three zones (Fig. 1 B). In zone 1, two germline stem cells divide asymmetrically to give rise to a cystoblast and a stem cell. The cystoblast then divides synchronously four times to produce 16 cell cysts interconnected by ring canals as a result of incomplete cytokinetic events. In zone 2, 16 cell cysts become surrounded by a pool of follicle cells produced by asymmetric division of two to three somatic stem cells. By this stage, 1 of the 16 germ cells has adopted an oocyte fate and becomes located at the posterior of the cyst. The remaining 15 nurse cells undergo polytenization. In zone 3, fully formed stage 1 egg chambers begin to emerge from the germarium, bounded by a well polarized follicular epithelium (Fig. 1 A). Egg chambers will continue to grow and increase in size up to stage 9, while the follicle cell monolayer accommodates this growth by a series of cell divisions.


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

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

βH distribution during oogenesis. (A–E) Wild-type ovariole costained for βH (top) and α-spectrin (bottom). The middle panels are merged false color images with βH in green and α-spectrin in red. Representative chambers for stages 1–10 are shown. Specific stages are indicated by the boxed numbers. (A) βH is uniformly distributed along the germ cell membranes and is apically polarized in the follicle cell monolayer. βH is also strongly expressed in stalks (arrow) and exhibits a patchy distribution on the border cell track during stage 9 (arrowhead). Scale bar, 50 μm. (B) High magnification view of a wild-type germarium indicating the location of zones 1–3. βH is strongly expressed in the terminal filament and cap cells (TF/CC) but is absent from fusomes marked by α-spectrin (arrow). Scale bar, 10 μm. (C) Nurse cell cluster of a stage 11 egg chamber. βH is seen faintly in filamentous structures within the dumping nurse cells. βH reappears at the apical domain of the border cells (arrowhead; see also E). Scale bar, 50 μm in C–E. (D and E) Anterior ends of stages 12, 13, and 14 egg chambers, respectively. βH is strongly expressed at the apical surface of follicle cells that are actively secreting chorion (arrow in D indicates the cells forming the dorsal appendages; arrowheads in C and E point to the border cells that secrete the micropyle). The nurse cells between the emerging dorsal appendages in D are undergoing programmed cell death. (F) High magnification view of a ring canal showing a slight enrichment of βH (left) on the outer rim of this actin rich structure (right). (G) En face high magnification view of the apical domain of follicle cells showing βH at the terminal web (left) and DE-cadherin (right) at the ZA. The central panels in F and G are merged false color images with the left and right panels of each in green and red, respectively. Bars: (F and G) 10 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2169487&req=5

Figure 1: βH distribution during oogenesis. (A–E) Wild-type ovariole costained for βH (top) and α-spectrin (bottom). The middle panels are merged false color images with βH in green and α-spectrin in red. Representative chambers for stages 1–10 are shown. Specific stages are indicated by the boxed numbers. (A) βH is uniformly distributed along the germ cell membranes and is apically polarized in the follicle cell monolayer. βH is also strongly expressed in stalks (arrow) and exhibits a patchy distribution on the border cell track during stage 9 (arrowhead). Scale bar, 50 μm. (B) High magnification view of a wild-type germarium indicating the location of zones 1–3. βH is strongly expressed in the terminal filament and cap cells (TF/CC) but is absent from fusomes marked by α-spectrin (arrow). Scale bar, 10 μm. (C) Nurse cell cluster of a stage 11 egg chamber. βH is seen faintly in filamentous structures within the dumping nurse cells. βH reappears at the apical domain of the border cells (arrowhead; see also E). Scale bar, 50 μm in C–E. (D and E) Anterior ends of stages 12, 13, and 14 egg chambers, respectively. βH is strongly expressed at the apical surface of follicle cells that are actively secreting chorion (arrow in D indicates the cells forming the dorsal appendages; arrowheads in C and E point to the border cells that secrete the micropyle). The nurse cells between the emerging dorsal appendages in D are undergoing programmed cell death. (F) High magnification view of a ring canal showing a slight enrichment of βH (left) on the outer rim of this actin rich structure (right). (G) En face high magnification view of the apical domain of follicle cells showing βH at the terminal web (left) and DE-cadherin (right) at the ZA. The central panels in F and G are merged false color images with the left and right panels of each in green and red, respectively. Bars: (F and G) 10 μm.
Mentions: Oogenesis in flies takes place in ovaries formed of 12–16 ovarioles, each of which consists of an anterior structure called the germarium and several egg chambers sequentially ordered with regard to their developmental stage (for review, see Spradling 1993; see Fig. 1 A for example). The germarium is comprised of three zones (Fig. 1 B). In zone 1, two germline stem cells divide asymmetrically to give rise to a cystoblast and a stem cell. The cystoblast then divides synchronously four times to produce 16 cell cysts interconnected by ring canals as a result of incomplete cytokinetic events. In zone 2, 16 cell cysts become surrounded by a pool of follicle cells produced by asymmetric division of two to three somatic stem cells. By this stage, 1 of the 16 germ cells has adopted an oocyte fate and becomes located at the posterior of the cyst. The remaining 15 nurse cells undergo polytenization. In zone 3, fully formed stage 1 egg chambers begin to emerge from the germarium, bounded by a well polarized follicular epithelium (Fig. 1 A). Egg chambers will continue to grow and increase in size up to stage 9, while the follicle cell monolayer accommodates this growth by a series of cell divisions.

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