Ion channels and calcium signaling in motile cilia

Abstract

The beating of motile cilia generates fluid flow over epithelia in brain ventricles, airways, and Fallopian tubes. Here, we patch clamp single motile cilia of mammalian ependymal cells and examine their potential function as a calcium signaling compartment. Resting motile cilia calcium concentration ([Ca ²⁺] ~170 nM) is only slightly elevated over cytoplasmic [Ca ²⁺] (~100 nM) at steady state. Ca ²⁺ changes that arise in the cytoplasm rapidly equilibrate in motile cilia. We measured Ca _V1 voltage-gated calcium channels in ependymal cells, but these channels are not specifically enriched in motile cilia. Membrane depolarization increases ciliary [Ca ²⁺], but only marginally alters cilia beating and cilia-driven fluid velocity within short (~1 min) time frames. We conclude that beating of ependymal motile cilia is not tightly regulated by voltage-gated calcium channels, unlike that of well-studied motile cilia and flagella in protists, such as Paramecia and Chlamydomonas.

DOI: http://dx.doi.org/10.7554/eLife.11066.001

eLife digest

Certain specialized cells in the brain, airways and Fallopian tubes have large numbers of hair-like structures called motile cilia on their surface. By beating in a synchronized manner, these cilia help to move fluids across the surface of the cells: for example, cilia on lung cells beat to clear mucus away, while those in the brain help the cerebrospinal fluid to circulate.

Motile cilia in mammals are structurally similar to the flagella that propel sperm cells and certain single-celled organisms around their environments. These flagella have specialized pore-forming proteins called ion channels in their membrane through which calcium ions can move. This flow of calcium ions controls the beating of the flagella. However, it is unclear whether a similar movement of calcium ions across the cilia membrane regulates motile cilia beating in mammals.

Doerner et al. have now used a method called patch clamping to study the movement of calcium ions across the membrane of the motile cilia found on a particular type of mouse brain cell. This revealed that unlike flagella, these motile cilia have very few voltage-gated calcium channels; instead, the vast majority of these ion channels reside in the main body of the cell. Furthermore, the level of calcium ions in the motile cilia follows changes in calcium ion levels that originate in the cell body.

Overall, Doerner et al. demonstrate that the activity of voltage-gated calcium channels does not control the beating rhythm of the motile cilia in the mouse brain or how quickly the fluid above the cell surface moves. Future work should investigate whether this is also the case for the cells that line the trachea and Fallopian tubes.

DOI: http://dx.doi.org/10.7554/eLife.11066.002