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Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila.

Harris TJ, Peifer M - J. Cell Biol. (2004)

Bottom Line: We found apical accumulation of both Drosophila E-Cadherin (DE-Cad) and the apical cue Bazooka (Baz) as cells first form.Some epithelial structures are retained, however.These structures maintain apical Baz, accumulate apical Crumbs, and organize polarized cytoskeletons, but display abnormal cell morphology and fail to segregate the basolateral cue Discs large from the apical domain.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

ABSTRACT
Adherens junctions (AJs) are thought to be key landmarks for establishing epithelial cell polarity, but the origin of epithelial polarity in Drosophila remains unclear. Thus, we examined epithelial polarity establishment during early Drosophila development. We found apical accumulation of both Drosophila E-Cadherin (DE-Cad) and the apical cue Bazooka (Baz) as cells first form. Mutant analyses revealed that apical Baz accumulations can be established in the absence of AJs, whereas assembly of apical DE-Cad complexes requires Baz. Thus, Baz acts upstream of AJs during epithelial polarity establishment. During gastrulation the absence of AJs results in widespread cell dissociation and depolarization. Some epithelial structures are retained, however. These structures maintain apical Baz, accumulate apical Crumbs, and organize polarized cytoskeletons, but display abnormal cell morphology and fail to segregate the basolateral cue Discs large from the apical domain. Thus, although epithelial polarity develops in the absence of AJs, AJs play specific roles in maintaining epithelial architecture and segregating basolateral cues.

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Morphogenesis and cell differentiation in gastrulating armm/z mutants. (A) WT moesin-GFP embryo (ventral side, posterior end). Time (h:min) begins at first gastrulation movement. Note ventral furrow (arrows). (B) WT. Twi (green) shows mesodermal cells in ventral furrow. Dlg (red) outlines cells. (C) armm/z mutant expressing moesin-GFP (ventral view, posterior end). Note disorganized “furrow” along anterior–posterior axis (0:46, arrows) and cell rounding/dissociation (1:07). (D) armm/z. Twi (green) shows ventral mesoderm. (D′) Dorsal section of embryo in D. Dorsal cells are Twi-negative. Dlg (red) shows PMGI and transverse furrows (one outlined). (E) armm/z, ventral view. Mir (green) shows neurectoderm in two bands along anterior–posterior axis. (E′) Dorsal section of embryo in E. Mir-positive dorsal cells are restricted anteriorly and are largely absent from epithelial folds (outlined). Dlg, red. Bars, 50 μm.
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fig4: Morphogenesis and cell differentiation in gastrulating armm/z mutants. (A) WT moesin-GFP embryo (ventral side, posterior end). Time (h:min) begins at first gastrulation movement. Note ventral furrow (arrows). (B) WT. Twi (green) shows mesodermal cells in ventral furrow. Dlg (red) outlines cells. (C) armm/z mutant expressing moesin-GFP (ventral view, posterior end). Note disorganized “furrow” along anterior–posterior axis (0:46, arrows) and cell rounding/dissociation (1:07). (D) armm/z. Twi (green) shows ventral mesoderm. (D′) Dorsal section of embryo in D. Dorsal cells are Twi-negative. Dlg (red) shows PMGI and transverse furrows (one outlined). (E) armm/z, ventral view. Mir (green) shows neurectoderm in two bands along anterior–posterior axis. (E′) Dorsal section of embryo in E. Mir-positive dorsal cells are restricted anteriorly and are largely absent from epithelial folds (outlined). Dlg, red. Bars, 50 μm.

Mentions: At the end of cellularization, armm/z mutant cells form a hexagonal array (Fig. 4 C, 0:00), as in WT (Fig. 4 A, 0:00), and during early gastrulation, a ventral furrow is attempted (Fig. 4 C, 0:46, arrow). Soon afterward, however, much of the ectoderm breaks into rounded, dissociated cells (Fig. 4 C, 1:07), as seen before (Cox et al., 1996; Müller and Wieschaus, 1996). Even so, cells make roughly correct cell fate choices. Using Twist (Twi) as a mesoderm marker, we found a ventral band of mesodermal cells (Fig. 4 D), similar to WT (Fig. 4 B). Arm is needed for Twi expression in some contexts (Farge, 2003), but is apparently not as the body axis is determined. Using Miranda (Mir) as a neuroblast marker, we found two regions of putative neuroblasts where the neurectoderm normally forms on each side of the mesoderm (Fig. 4 E). On the armm/z mutant dorsal side, Twi-positive cells are absent (Fig. 4 D′) and Mir is restricted to anterior regions where the brain develops (Fig. 4 E′). Thus, most dorsal cells are likely dorsal ectoderm although an amnioserosa-like region also develops (unpublished data).


Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila.

Harris TJ, Peifer M - J. Cell Biol. (2004)

Morphogenesis and cell differentiation in gastrulating armm/z mutants. (A) WT moesin-GFP embryo (ventral side, posterior end). Time (h:min) begins at first gastrulation movement. Note ventral furrow (arrows). (B) WT. Twi (green) shows mesodermal cells in ventral furrow. Dlg (red) outlines cells. (C) armm/z mutant expressing moesin-GFP (ventral view, posterior end). Note disorganized “furrow” along anterior–posterior axis (0:46, arrows) and cell rounding/dissociation (1:07). (D) armm/z. Twi (green) shows ventral mesoderm. (D′) Dorsal section of embryo in D. Dorsal cells are Twi-negative. Dlg (red) shows PMGI and transverse furrows (one outlined). (E) armm/z, ventral view. Mir (green) shows neurectoderm in two bands along anterior–posterior axis. (E′) Dorsal section of embryo in E. Mir-positive dorsal cells are restricted anteriorly and are largely absent from epithelial folds (outlined). Dlg, red. Bars, 50 μm.
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Related In: Results  -  Collection

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fig4: Morphogenesis and cell differentiation in gastrulating armm/z mutants. (A) WT moesin-GFP embryo (ventral side, posterior end). Time (h:min) begins at first gastrulation movement. Note ventral furrow (arrows). (B) WT. Twi (green) shows mesodermal cells in ventral furrow. Dlg (red) outlines cells. (C) armm/z mutant expressing moesin-GFP (ventral view, posterior end). Note disorganized “furrow” along anterior–posterior axis (0:46, arrows) and cell rounding/dissociation (1:07). (D) armm/z. Twi (green) shows ventral mesoderm. (D′) Dorsal section of embryo in D. Dorsal cells are Twi-negative. Dlg (red) shows PMGI and transverse furrows (one outlined). (E) armm/z, ventral view. Mir (green) shows neurectoderm in two bands along anterior–posterior axis. (E′) Dorsal section of embryo in E. Mir-positive dorsal cells are restricted anteriorly and are largely absent from epithelial folds (outlined). Dlg, red. Bars, 50 μm.
Mentions: At the end of cellularization, armm/z mutant cells form a hexagonal array (Fig. 4 C, 0:00), as in WT (Fig. 4 A, 0:00), and during early gastrulation, a ventral furrow is attempted (Fig. 4 C, 0:46, arrow). Soon afterward, however, much of the ectoderm breaks into rounded, dissociated cells (Fig. 4 C, 1:07), as seen before (Cox et al., 1996; Müller and Wieschaus, 1996). Even so, cells make roughly correct cell fate choices. Using Twist (Twi) as a mesoderm marker, we found a ventral band of mesodermal cells (Fig. 4 D), similar to WT (Fig. 4 B). Arm is needed for Twi expression in some contexts (Farge, 2003), but is apparently not as the body axis is determined. Using Miranda (Mir) as a neuroblast marker, we found two regions of putative neuroblasts where the neurectoderm normally forms on each side of the mesoderm (Fig. 4 E). On the armm/z mutant dorsal side, Twi-positive cells are absent (Fig. 4 D′) and Mir is restricted to anterior regions where the brain develops (Fig. 4 E′). Thus, most dorsal cells are likely dorsal ectoderm although an amnioserosa-like region also develops (unpublished data).

Bottom Line: We found apical accumulation of both Drosophila E-Cadherin (DE-Cad) and the apical cue Bazooka (Baz) as cells first form.Some epithelial structures are retained, however.These structures maintain apical Baz, accumulate apical Crumbs, and organize polarized cytoskeletons, but display abnormal cell morphology and fail to segregate the basolateral cue Discs large from the apical domain.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA.

ABSTRACT
Adherens junctions (AJs) are thought to be key landmarks for establishing epithelial cell polarity, but the origin of epithelial polarity in Drosophila remains unclear. Thus, we examined epithelial polarity establishment during early Drosophila development. We found apical accumulation of both Drosophila E-Cadherin (DE-Cad) and the apical cue Bazooka (Baz) as cells first form. Mutant analyses revealed that apical Baz accumulations can be established in the absence of AJs, whereas assembly of apical DE-Cad complexes requires Baz. Thus, Baz acts upstream of AJs during epithelial polarity establishment. During gastrulation the absence of AJs results in widespread cell dissociation and depolarization. Some epithelial structures are retained, however. These structures maintain apical Baz, accumulate apical Crumbs, and organize polarized cytoskeletons, but display abnormal cell morphology and fail to segregate the basolateral cue Discs large from the apical domain. Thus, although epithelial polarity develops in the absence of AJs, AJs play specific roles in maintaining epithelial architecture and segregating basolateral cues.

Show MeSH
Related in: MedlinePlus