Hexagonal Packing of Drosophila Wing Epithelial Cells by the Planar Cell Polarity Pathway

Abstract

The mechanisms that order cellular packing geometry are critical for the functioning of many tissues, but they are poorly understood. Here, we investigate this problem in the developing wing of Drosophila. The surface of the wing is decorated by hexagonally packed hairs that are uniformly oriented by the planar cell polarity pathway. They are constructed by a hexagonal array of wing epithelial cells. Wing epithelial cells are irregularly arranged throughout most of development, but they become hexagonally packed shortly before hair formation. During the process, individual cell boundaries grow and shrink, resulting in local neighbor exchanges, and Cadherin is actively endocytosed and recycled through Rab11 endosomes. Hexagonal packing depends on the activity of the planar cell polarity proteins. We propose that these proteins polarize trafficking of Cadherin-containing exocyst vesicles during junction remodeling. This may be a common mechanism for the action of planar cell polarity proteins in diverse systems.

Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis

“…The current study of MDCK cyst morphogenesis served to link lumen formation to Rab11 and RE function, and both of these aspects to E-cadherin targeting. Thus, this study provided new evidence in a mammalian system for the roles of the RE in E-cadherin trafficking and epithelial morphogenesis that were previously shown in Drosophila (8,19,39).…”

Isoform‐specific interaction of Flamingo/Starry Night with excess Bazooka affects planar cell polarity in the Drosophila wing

“…By this time, all cells have adopted a hexagonal shape and are more tightly packed ( Fig. 5A; Classen et al, 2005). In contrast, cells residing within zones of Bazooka overexpression driven by enGal4 (1) fail to concentrate Fmi/Stan at their distal and proximal edges, exhibiting instead a patchy accumulation of Fmi/ Stan on all apical membranes; and (2) remain irregularly packed (Fig.…”

“…In addition, PCP proteins act at an earlier stage, during the development of the hexagonal shape of the cells. Here, they have been suggested to be involved in remodeling adherens junctions by recruiting Sec5, a component of the exocyst, to the sites of Fmi/Stan accumulation (Classen et al, 2005).…”

Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures

“…Conversely, basal and lateral adhesion receptors favor the increase of contact surfaces (Käfer et al, 2007;Lecuit and Lenne, 2007;Manning et al, 2010). These ideas have been successfully used to quantitatively describe the geometrical configuration of ommatidia (Hilgenfeldt et al, 2008) and the growth of wings (Classen et al, 2005;Hufnagel et al, 2007;Lecuit and Lenne, 2007;Farhadifar et al, 2007) in Drosophila melanogaster and external surface, contacting the ECM, and the apical surface, facing the lumen. The correct architecture and the formation and maintenance of the lumen are crucial for normal cyst morphology and are altered in several common human diseases such as polycystic kidney disease (Boletta and Germino, 2003), hypertension (Iruela-Arispe and Davis, 2009), and many epithelial cancers, such as prostate carcinomas or preinvasive epithelial lesions (Debnath and Brugge, 2005).…”