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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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Time-lapse imaging of gastrulating armm/z mutants. (A) WT moesin-GFP embryo (lateral side, posterior end). Time (h:min) begins at first gastrulation movement. Note PMGI (0:18, arrow); early germband extension (0:32, arrow). (B) armm/z mutant expressing moesin-GFP (lateral side, posterior end). Note normal cell shape after cellularization (0:00); early PMGI (0:27, arrow); partial germband extension (0:40, arrow); transverse furrows (0:40, arrowheads); ectoderm cell dissociation (1:00); pole cells on embryo surface (1:00, blue arrowhead); cell rosettes at embryo surface (1:52, outlined). (C) As cells undergo rounding/dissociation (pink), some intervening cells (blue) undergo apical constriction and internalization as rosettes. Bars: (gray) 50 μm; (white) 5 μm.
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fig5: Time-lapse imaging of gastrulating armm/z mutants. (A) WT moesin-GFP embryo (lateral side, posterior end). Time (h:min) begins at first gastrulation movement. Note PMGI (0:18, arrow); early germband extension (0:32, arrow). (B) armm/z mutant expressing moesin-GFP (lateral side, posterior end). Note normal cell shape after cellularization (0:00); early PMGI (0:27, arrow); partial germband extension (0:40, arrow); transverse furrows (0:40, arrowheads); ectoderm cell dissociation (1:00); pole cells on embryo surface (1:00, blue arrowhead); cell rosettes at embryo surface (1:52, outlined). (C) As cells undergo rounding/dissociation (pink), some intervening cells (blue) undergo apical constriction and internalization as rosettes. Bars: (gray) 50 μm; (white) 5 μm.

Mentions: Subsets of dorsal cells retain epithelial character in gastrulating armm/z mutants. Dlg staining revealed large folds resembling the posterior midgut invagination (PMGI) and dorsal transverse furrows (Fig. 4, D′ and E′, furrow outlined; see Fig. 6, B and J). Live imaging of armm/z mutants revealed an attempted PMGI (Fig. 5 B, 0:27 arrow), and early germband extension (Fig. 5 B, 0:40, arrow), similar to WT (Fig. 5 A, 0:18 and 0:32 arrows). Transverse furrows are also evident in armm/z mutants (Fig. 5 B, 0:40 arrowheads). However, much of the dorsal surface then breaks apart into dissociated, rounded cells (Fig. 5 B, 1:00). Even so, some groups of cells remain associated, show coordinated constriction of their apical ends and are internalized as small cell “rosettes” (Fig. 5 B, 1:52 outlined; Fig. 5 C). Thus, although proper epithelial structure is lost over the surface of gastrulating armm/z mutants, some cells retain residual epithelial character and undergo limited morphogenesis, making infoldings and rosettes.


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

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

Time-lapse imaging of gastrulating armm/z mutants. (A) WT moesin-GFP embryo (lateral side, posterior end). Time (h:min) begins at first gastrulation movement. Note PMGI (0:18, arrow); early germband extension (0:32, arrow). (B) armm/z mutant expressing moesin-GFP (lateral side, posterior end). Note normal cell shape after cellularization (0:00); early PMGI (0:27, arrow); partial germband extension (0:40, arrow); transverse furrows (0:40, arrowheads); ectoderm cell dissociation (1:00); pole cells on embryo surface (1:00, blue arrowhead); cell rosettes at embryo surface (1:52, outlined). (C) As cells undergo rounding/dissociation (pink), some intervening cells (blue) undergo apical constriction and internalization as rosettes. Bars: (gray) 50 μm; (white) 5 μm.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2172516&req=5

fig5: Time-lapse imaging of gastrulating armm/z mutants. (A) WT moesin-GFP embryo (lateral side, posterior end). Time (h:min) begins at first gastrulation movement. Note PMGI (0:18, arrow); early germband extension (0:32, arrow). (B) armm/z mutant expressing moesin-GFP (lateral side, posterior end). Note normal cell shape after cellularization (0:00); early PMGI (0:27, arrow); partial germband extension (0:40, arrow); transverse furrows (0:40, arrowheads); ectoderm cell dissociation (1:00); pole cells on embryo surface (1:00, blue arrowhead); cell rosettes at embryo surface (1:52, outlined). (C) As cells undergo rounding/dissociation (pink), some intervening cells (blue) undergo apical constriction and internalization as rosettes. Bars: (gray) 50 μm; (white) 5 μm.
Mentions: Subsets of dorsal cells retain epithelial character in gastrulating armm/z mutants. Dlg staining revealed large folds resembling the posterior midgut invagination (PMGI) and dorsal transverse furrows (Fig. 4, D′ and E′, furrow outlined; see Fig. 6, B and J). Live imaging of armm/z mutants revealed an attempted PMGI (Fig. 5 B, 0:27 arrow), and early germband extension (Fig. 5 B, 0:40, arrow), similar to WT (Fig. 5 A, 0:18 and 0:32 arrows). Transverse furrows are also evident in armm/z mutants (Fig. 5 B, 0:40 arrowheads). However, much of the dorsal surface then breaks apart into dissociated, rounded cells (Fig. 5 B, 1:00). Even so, some groups of cells remain associated, show coordinated constriction of their apical ends and are internalized as small cell “rosettes” (Fig. 5 B, 1:52 outlined; Fig. 5 C). Thus, although proper epithelial structure is lost over the surface of gastrulating armm/z mutants, some cells retain residual epithelial character and undergo limited morphogenesis, making infoldings and rosettes.

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