Abstract
The coordinated orientation of cells across the tissue plane, known as planar cell polarity (PCP), is manifested by the segregation of core PCP proteins to different sides of the cell. Secreted Wnt ligands are involved in many PCP-dependent processes, yet whether they act as polarity cues has been controversial. We show that in Xenopus early ectoderm, the Prickle3/Vangl2 complex was polarized to anterior cell edges and this polarity was disrupted by several Wnt antagonists. In midgastrula embryos, Wnt5a, Wnt11, and Wnt11b, but not Wnt3a, acted across many cell diameters to orient Prickle3/Vangl2 complexes away from their sources regardless of their positions relative to the body axis. The planar polarity of endogenous Vangl2 in the neuroectoderm was similarly redirected by an ectopic Wnt source and disrupted after depletion of Wnt11b in the presumptive posterior region of the embryo. These observations provide evidence for the instructive role of Wnt ligands in vertebrate PCP.
Highlights
Studies in Drosophila revealed the segregation of core planar cell polarity (PCP) proteins to opposite sides of epithelial cells (Goodrich and Strutt, 2011; Peng and Axelrod, 2012)
We demonstrate that ectodermal PCP visualized by exogenous Prickle3 (Pk3)/Vangl2 complex in the epidermis and endogenous Vangl2 in the neuroectoderm can be instructed by Wnt ligands during gastrulation
To establish early PCP markers, we examined the subcellular localization of GFP-tagged Pk3, one of the core PCP proteins predominantly expressed in the epidermal ectoderm (Ossipova et al, 2015a)
Summary
Studies in Drosophila revealed the segregation of core PCP proteins to opposite sides of epithelial cells (Goodrich and Strutt, 2011; Peng and Axelrod, 2012) This mutually exclusive localization has been preserved in vertebrate tissues and is thought to be essential for multiple morphogenetic processes, including gastrulation and neurulation (Gray et al, 2011; Sokol, 2015; Tada and Heisenberg, 2012; Wallingford, 2012). The Xenopus larval epidermis contains multiciliated cells (MCCs) that are coordinately aligned to generate a unidirectional fluid flow (Konig and Hausen, 1993; Werner and Mitchell, 2012) This alignment is controlled by PCP proteins during gastrulation and neurulation (Butler and Wallingford, 2015; Mitchell et al, 2009; Yasunaga et al, 2011). We demonstrate that ectodermal PCP visualized by exogenous Prickle (Pk3)/Vangl complex in the epidermis and endogenous Vangl in the neuroectoderm can be instructed by Wnt ligands during gastrulation
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