Anisotropy of Crumbs and aPKC Drives Myosin Cable Assembly during Tube Formation

Katja Röper

doi:10.1016/j.devcel.2012.09.013

Abstract

SummaryThe formation of tubular structures from epithelial sheets is a key process of organ formation in all animals, but the cytoskeletal rearrangements that cause the cell shape changes that drive tubulogenesis are not well understood. Using live imaging and super-resolution microscopy to analyze the tubulogenesis of the Drosophila salivary glands, I find that an anisotropic plasma membrane distribution of the protein Crumbs, mediated by its large extracellular domain, determines the subcellular localization of a supracellular actomyosin cable in the cells at the placode border, with myosin II accumulating at edges where Crumbs is lowest. Laser ablation shows that the cable is under increased tension, implying an active involvement in the invagination process. Crumbs anisotropy leads to anisotropic distribution of aPKC, which in turn can negatively regulate Rok, thus preventing the formation of a cable where Crumbs and aPKC are localized.

Highlights

Cell shape changes and rearrangements within epithelial tissues provide two of the main mechanisms of organ formation during development
Myosin has the ability to form many different dynamic structures within a cell, but an understanding of myosin II regulation that leads to the selective formation of specific actin-myosin structures in particular processes is lacking in most cases
A Prominent Myosin II Cable Surrounds the Salivary Gland Placode during Tubulogenesis Myosin II in the embryo can be visualized using a GFP-tagged MRLC, termed Spaghetti squash (Sqh) in flies, in a sqh null mutant background (Karess et al, 1991; Royou et al, 2004). Employing this genetic tool, I analyzed the early stages of salivary gland tubulogenesis: the bending of the flat epithelial sheet of the epidermis to form a dimple and an invaginating tube

Summary

Introduction

Cell shape changes and rearrangements within epithelial tissues provide two of the main mechanisms of organ formation during development. Nonmuscle myosin II-actin networks have been found to direct some concerted epithelial rearrangements (for reviews see Kasza and Zallen, 2011; Lecuit and Lenne, 2007): cells within epithelial sheets that undergo convergent extension movements exhibit planar localized myosin II activity during the shrinking of selective cell boundaries to allow neighbor exchanges (Bertet et al, 2004; Simoes Sde et al, 2010); during mesoderm invagination in Drosophila, ventral furrow cells accumulate myosin II in an apical medial web during the constriction of apical surfaces that drives tissue folding (Martin et al, 2009, 2010). Myosin has the ability to form many different dynamic structures within a cell, but an understanding of myosin II regulation that leads to the selective formation of specific actin-myosin structures in particular processes is lacking in most cases

Results

Discussion

Conclusion