Cytoskeleton polarity is essential in determining orientational order in basal bodies of multi-ciliated cells

In multi-ciliated cells, directed and synchronous ciliary beating in the apical membrane occurs through appropriate configuration of basal bodies (BBs, roots of cilia). Although it has been experimentally shown that the position and orientation of BBs are coordinated by apical cytoskeletons (CSKs), such as microtubules (MTs), and planar cell polarity (PCP), the underlying mechanism for achieving the patterning of BBs is not yet understood. In this study, we propose that polarity in bundles of apical MTs play a crucial role in the patterning of BBs. First, the necessity of the polarity was discussed by theoretical consideration on the symmetry of the system. The existence of the polarity was investigated by measuring relative angles between the MTs and BBs using published experimental data. Next, a mathematical model for BB patterning was derived by combining the polarity and self-organizational ability of CSKs. In the model, BBs were treated as finite-size particles in the medium of CSKs and excluded volume effects between BBs and CSKs were taken into account. The model reproduces the various experimental observations, including normal and drug-treated phenotypes. Our model with polarity provides a coherent and testable mechanism for apical BB pattern formation. We have also discussed the implication of our study on cell chirality.Author summary: Synchronous and directed ciliary beating in trachea allows transport and ejection of virus and dust from the body. This ciliary function depends on the coordinated configuration of basal bodies (root of cilia) in apical cell membrane. However, the mechanism for their formation remains unknown. In this study, we show that the polarity in apical microtubule bundles plays a significant role in the organization of basal bodies. A mathematical model incorporating polarity has been formulated which provides a coherent explanation and is able to reproduce experimental observations. We have clarified both necessity (‘why polarity is required for pattern formation’) and sufficiency (‘how polarity works for pattern formation’) of cytoskeleton polarity for correct pattering of basal bodies with verification by experimental data. This model further leads us to a possible mechanism for cellular chirality.