Planar Polarity Specification through Asymmetric Subcellular Localization of Fat and Dachsous

Abstract

SummaryTwo pathways regulate planar polarity: the core proteins and the Fat-Dachsous-Four-jointed (Ft-Ds-Fj) system. Morphogens specify complementary expression patterns of Ds and Fj that potentially act as polarizing cues. It has been suggested that Ft-Ds-Fj-mediated cues are weak and that the core proteins amplify them [1, 2]. Another view is that the two pathways act independently to generate and propagate polarity [3, 4]: if correct, this raises the question of how gradients of Ft and Ds expression or activity might be interpreted to provide strong cellular polarizing cues and how such cues are propagated from cell to cell. Here, we demonstrate that the complementary expression of Ds and Fj results in biased Ft and Ds protein distribution across cells, with Ft and Ds accumulating on opposite edges. Furthermore, boundaries of Ft and Ds expression result in subcellular asymmetries in protein distribution that are transmitted to neighboring cells, and asymmetric Ds localization results in a corresponding asymmetric distribution of the myosin Dachs. We show that the generation of subcellular asymmetries of Ft and Ds and the core proteins is largely independent in the wing disc and additionally that ommatidial polarity in the eye can be determined without input from the Ft-Ds-Fj system, consistent with the two pathways acting in parallel.

A global pattern of mechanical stress polarizes cell divisions and cell shape in the growing Drosophila wing disc

“…More observations will be needed to dissect the mechanism by which Dachs polarizes growth radially in the wing pouch. Brittle et al observed a cellular-level polarity of Dachs near the hinge region at very late stages of larval development (Brittle et al, 2012). Although we find that Dachs is not polarized at earlier stages and that it is not required for cell stretching (Fig.…”

An intracellular partitioning-based framework for tissue cell polarity in plants and animals

“…Cells in the eye become polarised through preferential distribution of the cadherin Ds (A*) to one cell end and its binding partner the cadherin Ft (B*) to the opposite cell end (Ambegaonkar et al, 2012;Brittle et al, 2012). Planar polarity patterns are specified by opposite gradients in expression of Ds and the Golgi-associated protein Four-jointed (Fj) (Simon, 2004).…”

Regulation of long-range planar cell polarity by Fat-Dachsous signaling

“…Data from cell culture studies and from overexpression and mutant clones suggest that Ft and Ds form trans-heterodimers (Ma et al, 2003;Matakatsu and Blair, 2004;Strutt and Strutt, 2002). Ft and Ds can also localize on opposite sides of a cell, along the polarity axis ( Figure 3E) (Ambegaonkar et al, 2012;Brittle et al, 2012). Unlike classical cadherins, there is no evidence of homodimers of either Ft or Ds forming across cells (Brasch et al, 2012;Matakatsu and Blair, 2004).…”

“…PCP is also evident in dynamic processes, such as oriented cell division in Drosophila imaginal discs (Baena-Lopez et al, 2005) and cell intercalation during zebrafish neurulation (Ciruna et al, 2006). Ft and Ds cadherins act together with Fj, D, and the transcriptional co-repressor Atrophin (Atro) to regulate PCP (Thomas and Strutt, 2012). Vertebrate orthologs of Drosophila ft and ds, such as fat1, fat4, and dachsous1 also regulate PCP (Mao et al, 2011a;Saburi et al, 2008;Saburi et al, 2012).…”

“…Many tissues display directionally organized cell structures or behaviors, which are called PCP (Bayly and Axelrod, 2011;Thomas and Strutt, 2012). Ft-Ds signaling and Frizzled/PCP (Fz/PCP) signaling are the main PCP pathways (Figure 2), regulating PCP in contexts as disparate as ommatidial orientation in the Drosophila eye and orientation of stereocilia in the mouse cochlea (Saburi et al, 2008;Yang et al, 2002).…”