The Frizzled Planar Cell Polarity signaling pathway controls Drosophila wing topography

Abstract

The Drosophila wing is a primary model system for studying the genetic control of epithelial Planar Cell Polarity (PCP). Each wing epithelial cell produces a distally pointing hair under the control of the Frizzled (Fz) PCP signaling pathway. Here, we show that Fz PCP signaling also controls the formation and orientation of ridges on the adult wing membrane. Ridge formation requires hexagonal cell packing, consistent with published data showing that Fz PCP signaling promotes hexagonal packing in developing wing epithelia. In contrast to hair polarity, ridge orientation differs across the wing and is primarily anteroposterior (A-P) in the anterior and proximodistal (P-D) in the posterior. We present evidence that A-P ridge specification is genetically distinct from P-D ridge organization and occurs later in wing development. We propose a two-phase model for PCP specification in the wing. P-D ridges are specified in an Early PCP Phase and both A-P ridges and distally pointing hairs in a Late PCP Phase. Our data suggest that isoforms of the Fz PCP pathway protein Prickle are differentially required for the two PCP Phases, with the Spiny-legs isoform primarily active in the Early PCP Phase and the Prickle isoform in the Late PCP Phase.

Cooperative functions of the two F-BAR proteins Cip4 and Nostrin in regulating E-cadherin in epithelial morphogenesis

“…The hexagonal cell shape, in turn, leads to the formation and distinct orientation of ridges on the adult wing (Doyle et al, 2008). Cuticle refraction microscopy analysis of adult wings reveals that RNAi-mediated knockdown of cip4 and nostrin affects the shape of wing cells, resulting in interrupted ridges (supplementary material Fig.…”

Signal transduction by the Fat cytoplasmic domain

“…In the abdomen, a subtle phenotype was observed for Fat∆F, whereas other transgenes fully rescued abdominal hair polarity ( Fig. 3D-F We also analyzed the organization of intercellular ridges within the wing, the formation of which reflects polarized cellular organization (Doyle et al, 2008). Like wing hairs, ridges are influenced by both Frizzled and Fat-PCP pathways; however, ridge orientation is regulated separately from hair polarity (Hogan et al, 2011).…”

Cell shape and epithelial patterning in the Drosophila embryonic epidermis

“…8,9 Fz PCP signaling is not restricted to wing hair organization, but is also required to control Drosophila bristle orientation, 10 ommatidial polarity, 11 aristal branching, 12 tarsal joint formation 13 and tissue topography. 14 The Fz PCP pathway appears to be conserved in vertebrates and components of the pathway are known to be required for convergent extension movements during embryogenesis, 15 the organization of stereociliary bundles in the inner ear, 1 fur patterning, 16 cardiovascular development, 17 axonal guidance 18 and are permissive for Sonic Hedgehog signaling. 19 The Drosophila larval cuticle is also patterned with regular arrays of polarized structures.…”