Modelling planar polarity of epithelia: the role of signal relay in collective cell polarization

Abstract

Collective cell polarization is an important characteristic of tissues. Epithelia commonly display cellular structures that are polarized within the plane of the tissue. Establishment of this planar cell polarity requires mechanisms that locally align polarized structures between neighbouring cells, as well as cues that provide global information about alignment relative to an axis of a tissue. In the Drosophila ovary, the cadherin Fat2 is required to orient actin filaments located at the basal side of follicle cells perpendicular to the long axis of the egg chamber. The mechanisms directing this orientation of actin filaments, however, remain unknown. Here we show, using genetic mosaic analysis, that fat2 is not essential for the local alignment of actin filaments between neighbouring cells. Moreover, we provide evidence that Fat2 is involved in the propagation of a cue specifying the orientation of actin filaments relative to the tissue axis. Monte Carlo simulations of actin filament orientation resemble the results of the genetic mosaic analysis, if it is assumed that a polarity signal can propagate from a signal source only through a connected chain of wild-type cells. Our results suggest that Fat2 is required for propagating global polarity information within the follicle epithelium through direct cell -cell contact. Our computational model might be more generally applicable to study collective cell polarization in tissues.

Symmetry Breaking in an Edgeless Epithelium by Fat2-Regulated Microtubule Polarity

“…The atypical cadherin Fat2 is required to initiate rotation (Cetera et al, 2014) and for egg elongation and cytoskeletal PCP, but its role in the latter has been largely inferred from phenotypes seen ~16 hours after rotation has initiated (Viktorinova et al, 2009; 2011). We identified RNAi lines that knockdown fat2 either strongly or mildly; the strong knockdown line phenocopies the fat2 null phenotype with 100% penetrance ( Supplemental Fig.…”

Fat3 and Ena/VASP proteins influence the emergence of asymmetric cell morphology in the developing retina

“…Our data confirm an autonomous requirement for Fat3, but do not rule out additional non-autonomous functions. Indeed, in Drosophila, the effect of Fat-like on actin organization in follicle cells is strictly non-cell autonomous (Viktorinova et al, 2009(Viktorinova et al, , 2011. The presence of Fat3 in retinal ganglion cells underscores the potential for non-autonomous functions, which could explain why migration is more severely affected in Fat3 null mutants than amacrine cell-specific knockouts (Deans et al, 2011).…”

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

“…The first evidence that the planar polarization of the basal actin bundles is a direct consequence of the epithelial rotation came through careful studies of fat2 mosaic egg chambers [14,43]. When fat2 mutant cells comprise less than 60% of the epithelium, the actin bundles are still perfectly aligned across the tissue.…”