Abstract
PCP proteins maintain planar polarity in many epithelial tissues and have been implicated in cilia development in vertebrate embryos. In this study we examine Prickle3 (Pk3), a vertebrate homologue of Drosophila Prickle, in Xenopus gastrocoel roof plate (GRP). GRP is a tissue equivalent to the mouse node, in which cilia-generated flow promotes left-right patterning. We show that Pk3 is enriched at the basal body of GRP cells but is recruited by Vangl2 to anterior cell borders. Interference with Pk3 function disrupted the anterior polarization of endogenous Vangl2 and the posterior localization of cilia in GRP cells, demonstrating its role in PCP. Strikingly, in cells with reduced Pk3 activity, cilia growth was inhibited and γ-tubulin and Nedd1 no longer associated with the basal body, suggesting that Pk3 has a novel function in basal body organization. Mechanistically, this function of Pk3 may involve Wilms tumor protein 1-interacting protein (Wtip), which physically associates with and cooperates with Pk3 to regulate ciliogenesis. We propose that, in addition to cell polarity, PCP components control basal body organization and function.
Highlights
planar cell polarity (PCP) proteins maintain planar polarity in many epithelial tissues and have been implicated in cilia development in vertebrate embryos
In the presence of Vangl[2], Pk3 was recruited to the anterior cell boundary in mosaically-expressing gastrocoel roof plate (GRP) cells (Fig. 1D–D’’), consistent with the anterior distribution of endogenous Vangl[2]
Besides the involvement of Pk3 in PCP, loss-of-function experiments revealed its novel role in basal body organization and function
Summary
PCP proteins maintain planar polarity in many epithelial tissues and have been implicated in cilia development in vertebrate embryos. Loss-of-function studies established a requirement of vertebrate PCP components in diverse cell behaviors including mediolateral and radial cell intercalations, apical constriction and cell migration[8,11,12,13,14,15,16] This evidence demonstrates the expanded roles of vertebrate PCP proteins in multiple developmental processes. The existence of four vertebrate prickle gene homologues suggests that they may have diverged from each other and acquired unique functions, as reported for celsr/flamingo genes[34] Consistent with this possibility, the vertebrate Prickle family has been implicated in a number of developmental processes, including convergent extension movements, apicobasal and planar cell polarity[35,36,37,38,39].
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