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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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DE-Cad localization depends on Baz. (A–D) Cross sections. (A) bazm/z. DE-Cad (green) is at basal junctions at mid cellularization (arrow), as in WT (B, arrow). Dlg (red) shows furrows. (C) bazm/z. DE-Cad (green) is all along the furrow at late cellularization (bracket). Some apical (arrowhead) and basal (blue arrowheads) accumulations are seen. (D) WT. DE-cad is at apical junctions (arrowhead). (E and F) Embryo surface views. (E) bazm/z. Note relatively smooth DE-Cad distribution (green). (F) WT. DE-cad in spot junctions (red arrowhead). Bars, 5 μm.
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fig3: DE-Cad localization depends on Baz. (A–D) Cross sections. (A) bazm/z. DE-Cad (green) is at basal junctions at mid cellularization (arrow), as in WT (B, arrow). Dlg (red) shows furrows. (C) bazm/z. DE-Cad (green) is all along the furrow at late cellularization (bracket). Some apical (arrowhead) and basal (blue arrowheads) accumulations are seen. (D) WT. DE-cad is at apical junctions (arrowhead). (E and F) Embryo surface views. (E) bazm/z. Note relatively smooth DE-Cad distribution (green). (F) WT. DE-cad in spot junctions (red arrowhead). Bars, 5 μm.

Mentions: Because Baz colocalizes with apical DE-Cad during WT cellularization, we hypothesized that Baz may direct apical DE-Cad recruitment. Müller and Wieschaus (1996) observed a loss of apical AJs in gastrulating bazm/z mutants. We tested whether this mislocalization begins during cellularization by examining m/z mutants for bazXi106 (Müller and Wieschaus, 1996). During mid cellularization, DE-Cad accumulates basally in the bazm/z mutants (Fig. 3 A, arrow), similar to WT (Fig. 3 B, arrow). However, at the end of cellularization, DE-Cad displays a punctate distribution along the full length of the furrows (Fig. 3 C, brackets) with slight enrichment at both the apical and basal ends (Fig. 3 C, white and blue arrowheads), in contrast to WT (Fig. 3 D). From the surface, the apical DE-Cad is more evenly distributed in bazm/z mutants (Fig. 3 E) than in WT (Fig. 3 F, red arrowhead), indicating a failure to assemble DE-Cad into spot junctions. During later development, total DE-Cad levels were indistinguishable between bazm/z mutants and their zygotically rescued siblings by immunofluorescence (unpublished data), suggesting that Baz does not affect DE-Cad accumulation. Instead, Baz is required for the effective apical redistribution of DE-Cad and its assembly into spot junctions. Importantly, these data indicate that Baz acts upstream of AJs as epithelial polarity is established during cellularization.


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

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

DE-Cad localization depends on Baz. (A–D) Cross sections. (A) bazm/z. DE-Cad (green) is at basal junctions at mid cellularization (arrow), as in WT (B, arrow). Dlg (red) shows furrows. (C) bazm/z. DE-Cad (green) is all along the furrow at late cellularization (bracket). Some apical (arrowhead) and basal (blue arrowheads) accumulations are seen. (D) WT. DE-cad is at apical junctions (arrowhead). (E and F) Embryo surface views. (E) bazm/z. Note relatively smooth DE-Cad distribution (green). (F) WT. DE-cad in spot junctions (red arrowhead). Bars, 5 μm.
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fig3: DE-Cad localization depends on Baz. (A–D) Cross sections. (A) bazm/z. DE-Cad (green) is at basal junctions at mid cellularization (arrow), as in WT (B, arrow). Dlg (red) shows furrows. (C) bazm/z. DE-Cad (green) is all along the furrow at late cellularization (bracket). Some apical (arrowhead) and basal (blue arrowheads) accumulations are seen. (D) WT. DE-cad is at apical junctions (arrowhead). (E and F) Embryo surface views. (E) bazm/z. Note relatively smooth DE-Cad distribution (green). (F) WT. DE-cad in spot junctions (red arrowhead). Bars, 5 μm.
Mentions: Because Baz colocalizes with apical DE-Cad during WT cellularization, we hypothesized that Baz may direct apical DE-Cad recruitment. Müller and Wieschaus (1996) observed a loss of apical AJs in gastrulating bazm/z mutants. We tested whether this mislocalization begins during cellularization by examining m/z mutants for bazXi106 (Müller and Wieschaus, 1996). During mid cellularization, DE-Cad accumulates basally in the bazm/z mutants (Fig. 3 A, arrow), similar to WT (Fig. 3 B, arrow). However, at the end of cellularization, DE-Cad displays a punctate distribution along the full length of the furrows (Fig. 3 C, brackets) with slight enrichment at both the apical and basal ends (Fig. 3 C, white and blue arrowheads), in contrast to WT (Fig. 3 D). From the surface, the apical DE-Cad is more evenly distributed in bazm/z mutants (Fig. 3 E) than in WT (Fig. 3 F, red arrowhead), indicating a failure to assemble DE-Cad into spot junctions. During later development, total DE-Cad levels were indistinguishable between bazm/z mutants and their zygotically rescued siblings by immunofluorescence (unpublished data), suggesting that Baz does not affect DE-Cad accumulation. Instead, Baz is required for the effective apical redistribution of DE-Cad and its assembly into spot junctions. Importantly, these data indicate that Baz acts upstream of AJs as epithelial polarity is established during cellularization.

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