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The structure of the axoneme in motile cilia and flagella is emerging with increasing detail from high-resolution imaging, but the mechanism by which the axoneme creates oscillatory, propulsive motion remains mysterious. It has recently been proposed that this motion may be caused by a dynamic ‘flutter’ instability that can occur under steady dynein loading, and not by switching or modulation of dynein motor activity (as commonly assumed). In the current work, we have built an improved multi-filament mathematical model of the axoneme and implemented it as a system of discrete equations using the finite-element method. The eigenvalues and eigenvectors of this model predict the emergence of oscillatory, wave-like solutions in the absence of dynein regulation and specify the associated frequencies and waveforms of beating. Time-domain simulations with this model illustrate the behaviour predicted by the system's eigenvalues. This model and analysis allow us to efficiently explore the potential effects of difficult to measure biophysical parameters, such as elasticity of radial spokes and inter-doublet links, on the ciliary waveform. These results support the idea that dynamic instability without dynamic dynein regulation is a plausible and robust mechanism for generating ciliary beating.
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Finite element models of flagella with sliding radial spokes and interdoublet links exhibit propagating waves under steady dynein loading
Abstract It remains unclear how flagella generate propulsive, oscillatory waveforms. While it is well known that dynein motors, in combination with passive cytoskeletal elements, drive the bending of the axoneme by applying shearing forces and bending moments to microtubule doublets, the origin of rhythmicity is still mysterious. Most conceptual models of flagellar oscillation involve dynein regulation or switching, so that dynein activity first on one side of the axoneme, then the other, drives bending. In contrast, a “viscoelastic flutter” mechanism has recently been proposed, based on a dynamic structural instability. Simple mathematical models of coupled elastic beams in viscous fluid, subjected to steady, axially distributed, dynein forces of sufficient magnitude, can exhibit oscillatory motion without any switching or dynamic regulation. Here we introduce more realistic finite element (FE) models of 6‐doublet and 9‐doublet flagella, with radial spokes and interdoublet links that slide along the central pair or corresponding doublet. These models demonstrate the viscoelastic flutter mechanism. Above a critical force threshold, these models exhibit an abrupt onset of propulsive, wavelike oscillations typical of flutter instability. Changes in the magnitude and spatial distribution of steady dynein force, or to viscous resistance, lead to behavior qualitatively consistent with experimental observations. This study demonstrates the ability of FE models to simulate nonlinear interactions between axonemal components during flagellar beating, and supports the plausibility of viscoelastic flutter as a mechanism of flagellar oscillation.
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- Award ID(s):
- 1633971
- PAR ID:
- 10049805
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Cytoskeleton
- Volume:
- 75
- Issue:
- 5
- ISSN:
- 1949-3584
- Format(s):
- Medium: X Size: p. 185-200
- Size(s):
- p. 185-200
- Sponsoring Org:
- National Science Foundation
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