Cilia density and flow velocity affect alignment of motile cilia from brain cells.

Nicola Pellicciotta,Debasish Das,Pietro Cicuta,Jurij Kotar,Eric Lauga,Marion Faucourt,Nathalie Spassky

doi:10.1242/jeb.229310

Abstract

ABSTRACTIn many organs, thousands of microscopic ‘motile cilia’ beat in a coordinated fashion generating fluid flow. Physiologically, these flows are important in both development and homeostasis of ciliated tissues. Combining experiments and simulations, we studied how cilia from brain tissue align their beating direction. We subjected cilia to a broad range of shear stresses, similar to the fluid flow that cilia themselves generate, in a microfluidic setup. In contrast to previous studies, we found that cilia from mouse ependyma respond and align to these physiological shear stress at all maturation stages. Cilia align more easily earlier in maturation, and we correlated this property with the increase in multiciliated cell density during maturation. Our numerical simulations show that cilia in densely packed clusters are hydrodynamically screened from the external flow, in agreement with our experimental observation. Cilia carpets create a hydrodynamic screening that reduces the susceptibility of individual cilia to external flows.

Highlights

The ventricular cavities of the brain are covered by ependymal cells bearing motile cilia (Worthington and Cathcart, 1966), which are whip-like organelles that can propagate bending waves and produce fluid flow over the cell surface
Contrary to past findings (Guirao et al, 2010), our measurements show that cilia can respond and align to physiological shear stress found in the brain even after complete cell maturation
We observed that the shear stress needed to align mature cells significantly is around τ≃0.1 dyne cm−2

Summary

Introduction

The ventricular cavities of the brain are covered by ependymal cells bearing motile cilia (Worthington and Cathcart, 1966), which are whip-like organelles that can propagate bending waves and produce fluid flow over the cell surface. Their ability to generate fluid flow is a fascinating example of collective behaviour (Blake and Sleigh, 1974) in biology. Motile cilia circulate cerebrospinal fluid (CSF) thought to be necessary for brain homoeostasis, toxin washout and orientation of the migration of newborn neurons (Sawamoto et al, 2006). In zebrafish juveniles and adults, ciliadriven flow was shown to be critical for body axis formation in the embryo and spine morphogenesis (Zhang et al, 2018)

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Conclusion