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The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila.

Harris TJ, Peifer M - J. Cell Biol. (2005)

Bottom Line: Adherens junctions (AJs) often direct this polarity, but we previously found that Bazooka (Baz) acts upstream of AJs as epithelial polarity is first established in Drosophila.Surprisingly, we found that Baz localizes to an apical domain below its typical binding partners atypical protein kinase C (aPKC) and partitioning defective (PAR)-6 as the Drosophila epithelium first forms.These results reveal key steps in the assembly of the apical domain in Drosophila.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. tonyh@email.unc.edu

ABSTRACT
Cell polarity is critical for epithelial structure and function. Adherens junctions (AJs) often direct this polarity, but we previously found that Bazooka (Baz) acts upstream of AJs as epithelial polarity is first established in Drosophila. This prompted us to ask how Baz is positioned and how downstream polarity is elaborated. Surprisingly, we found that Baz localizes to an apical domain below its typical binding partners atypical protein kinase C (aPKC) and partitioning defective (PAR)-6 as the Drosophila epithelium first forms. In fact, Baz positioning is independent of aPKC and PAR-6 relying instead on cytoskeletal cues, including an apical scaffold and dynein-mediated basal-to-apical transport. AJ assembly is closely coupled to Baz positioning, whereas aPKC and PAR-6 are positioned separately. This forms a stratified apical domain with Baz and AJs localizing basal to aPKC and PAR-6, and we identify specific mechanisms that keep these proteins apart. These results reveal key steps in the assembly of the apical domain in Drosophila.

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A model of apical domain assembly during cellularization and gastrulation. See Discussion for details.
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fig9: A model of apical domain assembly during cellularization and gastrulation. See Discussion for details.

Mentions: Our results frame a model of apical domain assembly during epithelial polarity establishment in Drosophila (Fig. 9). During cellularization, Baz acts as a primary polarity landmark that positions AJs and aPKC. Baz, itself, is positioned by two cues (an apical scaffold and dynein-mediated transport). Baz recruits and colocalizes with AJ proteins in a subapical region while helping direct aPKC to the extreme apical region (Fig. 9). During gastrulation, a third cue becomes important for Baz and AJ positioning. At this stage, aPKC becomes required for maintaining Baz and AJs. PAR-6 is also recruited to the extreme apical region and maintains Baz and AJs (Hutterer et al., 2004). Although Baz can interact with aPKC and PAR-6 at this stage, Crb blocks these interactions (Fig. 9). We propose that this interaction network establishes a robust, stratified apical domain from the earliest stages of epithelial development.


The positioning and segregation of apical cues during epithelial polarity establishment in Drosophila.

Harris TJ, Peifer M - J. Cell Biol. (2005)

A model of apical domain assembly during cellularization and gastrulation. See Discussion for details.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2171335&req=5

fig9: A model of apical domain assembly during cellularization and gastrulation. See Discussion for details.
Mentions: Our results frame a model of apical domain assembly during epithelial polarity establishment in Drosophila (Fig. 9). During cellularization, Baz acts as a primary polarity landmark that positions AJs and aPKC. Baz, itself, is positioned by two cues (an apical scaffold and dynein-mediated transport). Baz recruits and colocalizes with AJ proteins in a subapical region while helping direct aPKC to the extreme apical region (Fig. 9). During gastrulation, a third cue becomes important for Baz and AJ positioning. At this stage, aPKC becomes required for maintaining Baz and AJs. PAR-6 is also recruited to the extreme apical region and maintains Baz and AJs (Hutterer et al., 2004). Although Baz can interact with aPKC and PAR-6 at this stage, Crb blocks these interactions (Fig. 9). We propose that this interaction network establishes a robust, stratified apical domain from the earliest stages of epithelial development.

Bottom Line: Adherens junctions (AJs) often direct this polarity, but we previously found that Bazooka (Baz) acts upstream of AJs as epithelial polarity is first established in Drosophila.Surprisingly, we found that Baz localizes to an apical domain below its typical binding partners atypical protein kinase C (aPKC) and partitioning defective (PAR)-6 as the Drosophila epithelium first forms.These results reveal key steps in the assembly of the apical domain in Drosophila.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA. tonyh@email.unc.edu

ABSTRACT
Cell polarity is critical for epithelial structure and function. Adherens junctions (AJs) often direct this polarity, but we previously found that Bazooka (Baz) acts upstream of AJs as epithelial polarity is first established in Drosophila. This prompted us to ask how Baz is positioned and how downstream polarity is elaborated. Surprisingly, we found that Baz localizes to an apical domain below its typical binding partners atypical protein kinase C (aPKC) and partitioning defective (PAR)-6 as the Drosophila epithelium first forms. In fact, Baz positioning is independent of aPKC and PAR-6 relying instead on cytoskeletal cues, including an apical scaffold and dynein-mediated basal-to-apical transport. AJ assembly is closely coupled to Baz positioning, whereas aPKC and PAR-6 are positioned separately. This forms a stratified apical domain with Baz and AJs localizing basal to aPKC and PAR-6, and we identify specific mechanisms that keep these proteins apart. These results reveal key steps in the assembly of the apical domain in Drosophila.

Show MeSH