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

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.

DOI: http://dx.doi.org/10.7554/eLife.05361.001

eLife digest

Animal cells that form flat layers of a tissue, such as the skin or the lining of internal cavities, are often orientated in the same direction. The same is true for structures such as hairs or feathers, which are attached to the skin. This phenomenon is known as ‘planar cell polarity’ (or ‘PCP’ for short).

Many different organisms use similar mechanisms to establish this kind of tissue pattern. The best-studied mechanism involves the so-called ‘core PCP pathway’. Signaling proteins in this pathway coordinate the polarity of neighboring cells. Other ‘global signaling pathways’ are thought to first ensure that tissues are correctly orientated within the embryo as a whole, and to do this, the global pathways are thought to align a network of filament-like structures within the cells in a particular direction. Once correctly orientated, these filaments—known as microtubules—have been proposed to help position the components of the core PCP pathway such that they can correctly orientate the rest of the cell.

Now Newman-Smith, Kourakis et al. have identified another network of filaments within cells that interacts with components of the core PCP pathway in a sea squirt called Ciona savignyi. This organism begins life as a tadpole-like larva that has a flexible rod-shaped structure, called a ‘notochord’, running along the length of its body. The cells of the notochord become polarized as they develop. When microtubules are disrupted, their planar polarity remains unaffected. However, when another network of filaments—called the actomyosin network––is chemically disrupted, the polarity of certain core PCP components is lost.

The findings of Newman-Smith, Kourakis et al. reveal that the core PCP components and the actomyosin network in this sea squirt reinforce each other's polarity. This represents an alternative to the previously described models of planar polarity in which the core PCP components are thought to drive the polarization of the actomyosin network. Whether this model extends to planar cell polarity mechanisms in other organisms, such humans and other animals with backbones, remains a question for future work.

DOI: http://dx.doi.org/10.7554/eLife.05361.002