Reciprocal and dynamic polarization of planar cell polarity core components and myosin.

Erin Newman-Smith,Wendy Reeves,Michael Veeman,Matthew J Kourakis,William C Smith

doi:10.7554/elife.05361

Erin Newman-Smith, Wendy Reeves + Show 3 more

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https://doi.org/10.7554/elife.05361

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Abstract

The Ciona notochord displays planar cell polarity (PCP), with anterior localization of Prickle (Pk) and Strabismus (Stbm). We report that a myosin is polarized anteriorly in these cells and strongly colocalizes with Stbm. Disruption of the actin/myosin machinery with cytochalasin or blebbistatin disrupts polarization of Pk and Stbm, but not of myosin complexes, suggesting a PCP-independent aspect of myosin localization. Wash out of cytochalasin restored Pk polarization, but not if done in the presence of blebbistatin, suggesting an active role for myosin in core PCP protein localization. On the other hand, in the pk mutant line, aimless, myosin polarization is disrupted in approximately one third of the cells, indicating a reciprocal action of core PCP signaling on myosin localization. Our results indicate a complex relationship between the actomyosin cytoskeleton and core PCP components in which myosin is not simply a downstream target of PCP signaling, but also required for PCP protein localization.

Highlights

Despite the importance of the planar cell polarity (PCP) pathway in ensuring the proper orientation of cells in a range of embryonic and adult tissues, the molecular mechanisms of this pathway are not fully understood
The results presented here demonstrate a dynamic interaction between PCP components and the actin/myosin cytoskeleton in establishing and maintaining notochord cell AP polarity
PCP-directed polarization of actin is seen in the Drosophila wing, where the actin-rich prehair is targeted to the distal side, opposite where pk and stbm are enriched (Wong and Adler, 1993)

Summary

Introduction

Despite the importance of the planar cell polarity (PCP) pathway in ensuring the proper orientation of cells in a range of embryonic and adult tissues, the molecular mechanisms of this pathway are not fully understood. The function of the PCP pathway can be seen in the coordinated polarization of subcellular components such as cilia and multi-celled structures such as bristles in epithelial sheets and organs like the Drosophila wing, vertebrate inner ear, and kidney, as well as in dynamic processes, such as cell migration, convergence and extension of mesoderm, neural tube closure, and axonal guidance (Ybot-Gonzalez et al, 2007; Wallingford, 2012; Tissir and Goffinet, 2013; Papakrivopoulou et al, 2014). The key components of the core pathway include the transmembrane proteins Strabismus/Van Gogh and Frizzled, and the cytoplasmic proteins Prickle and Dishevelled. Some components of this pathway are shared with the wnt/β-catenin signaling pathway, unlike the Wnt/β-catenin pathway the core PCP pathway is thought to act primarily by directing cytoskeletal organization, rather than by regulating transcription

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