Functional plasticity of polarity proteins controls epithelial tissue architecture

The Drosophila polarity protein Crumbs is essential for the establishment and growth of the apical domain in epithelial cells. Dynamic regulation of apical domain size is crucial for forming and maintaining complex epithelial structures such as tubes or acini. The protein Yurt limits the ability of Crumbs to promote apical membrane growth, thereby defining proper apical/basal membrane ratio that is essential for the functional architecture of epithelial cells. Here, we show that Yurt is not a general inhibitor of Crumbs, but rather hijacks Crumbs activity toward specific functions. In particular, Crumbs recruits Yurt to the apical domain to increase Myosin-dependent cortical tension while decreasing relative tissue viscosity. Yurt overexpression thus induces apical constriction in epithelial cells. The kinase aPKC phosphorylates Yurt, thereby dislodging the latter from the apical domain and releasing apical tension. In contrast, the kinase Pak1 promotes Yurt dephosphorylation through activation of the phosphatase PP2A. The Pak1-PP2A module thus opposes aPKC function and supports Yurt-induced apical constriction. Hence, the complex interplay between Yurt, aPKC, Pak1 and PP2A contributes to the functional plasticity of Crumbs. Overall, our data increase our understanding of how proteins sustaining epithelial cell polarization and Myosin-dependent cell contractility interact with one another to control epithelial tissue architecture.