Round and round gets you somewhere: collective cell migration and planar polarity in elongating Drosophila egg chambers

Abstract

Planar polarity is a developmental mechanism wherein individual cell behaviors are coordinated across a two-dimensional plane. A great deal of attention has been paid to the roles that the Frizzled/Strabismus and Fat/Dachsous signaling pathways play in this process; however, it is becoming increasingly clear that planar polarity can also be generated through alternate mechanisms. This review focuses on an unconventional form of planar polarity found within the follicular epithelium of the Drosophila egg chamber that helps to create the elongated shape of the egg. We highlight recent studies showing that the planar polarity in this system arises through collective migration of the follicle cells and the resulting rotational motion of the egg chamber.

Figure 1

Introduction to egg chamber rotation. (a) Image of a developmental array of egg chambers indicating the developmental window and two phases in which rotation occurs. (b) Overview of egg chamber structure. (c) A schematic of a transverse section through an egg chamber showing that rotation occurs within the surrounding BM. (d) Illustrations showing the planar polarization of actin bundles and leading edge protrusions at the basal surface of the follicular epithelium during rotation. (e) At the time rotation begins the egg chamber is connected to the germarium at its anterior pole and to stalk cells at its posterior pole (white arrow heads). For all images, anterior is to the left.

Figure 2

Planar polarity within the follicular epithelium. (a) The tissue-level alignment of the basal actin bundles occurs in three steps. Representative images of the basal actin bundles (rhodamine phalloidin) and BM (Collagen IV-GFP) are shown for each step. (b) The front-rear axes of the migrating follicle cells are also aligned across the tissue. Leading edge protrusions (white jagged lines) mark the front of each migrating follicle cell and the localization of the Fat2 and Misshapen proteins (yellow chevrons) define the rear. (c) Local order can exist in the follicular epithelium in the absence of global polarity. In a mosaic epithelium that is comprised of both wild-type cells and cells that lack the β-integrin subunit Myospheroid, the basal actin bundles can show a swirling pattern. Wild-type cells are marked in green in the first two panels. The orientation of the actin bundle array within each cell is indicated by the yellow lines. For all images, anterior is to the left.