Abstract
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.
Highlights
Synchronous and coordinated ciliary beating underlies various biological functions in organisms ranging from ciliates to mammals [1]
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
The patterning of basal bodies (BBs) arrays follows the formation of the CSK matrix, the MT bundles forming on the cytosolic apical membrane [3,11]
Summary
Synchronous and coordinated ciliary beating underlies various biological functions in organisms ranging from ciliates to mammals [1]. Hundreds of cilia covering the apical membrane of a cell beat synchronously in the same direction. This organized directionality in ciliary beating is achieved by basal bodies (BBs), which are roots of the cilia. These BBs point in the same orientation (Fig 1A), which is defined by the relative position of the basal foot (BF), a major appendage associated with BBs. In addition, previous studies have revealed that BBs are regularly aligned in the apical membrane of the mature epithelial cells in mouse trachea [3].
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