Abstract
Ciliary and flagellar motility is caused by the ensemble action of inner and outer dynein arm motors acting on axonemal doublet microtubules. The switch point or switching hypothesis, for which much experimental and computational evidence exists, requires that dyneins on only one side of the axoneme are actively working during bending, and that this active motor region propagate along the axonemal length. Generation of a reverse bend results from switching active sliding to the opposite side of the axoneme. However, the mechanochemical states of individual dynein arms within both straight and curved regions and how these change during beating has until now eluded experimental observation. Recently, Lin and Nicastro used high‐resolution cryo‐electron tomography to determine the power stroke state of dyneins along flagella of sea urchin sperm that were rapidly frozen while actively beating. The results reveal that axonemal dyneins are generally in a pre‐power stroke conformation that is thought to yield a force‐balanced state in straight regions; inhibition of this conformational state and microtubule release on specific doublets may then lead to a force imbalance across the axoneme allowing for microtubule sliding and consequently the initiation and formation of a ciliary bend. Propagation of this inhibitory signal from base‐to‐tip and switching the microtubule doublet subsets that are inhibited is proposed to result in oscillatory motion.
Highlights
The rhythmic beating of cilia and flagella is driven by the coordinated action of multiple dynein ATPase motors generating inter-doublet microtubule sliding (Satir, 1968; Summers & Gibbons, 1971)
For microtubule sliding to be converted into a ciliary bend, dynein activity must be tightly controlled so that motors on only one side of the axoneme are active; this region of active motors must propagate along the ciliary structure
Numerous experimental and computational results support this “switch point” hypothesis which predicts that within a ciliary bend, dyneins on one side of the axoneme will be in a different functional state to those on the opposite side (Shingyoji et al, 1977; Wais-Steider & Satir, 1979; Brokaw, 1991, 2009; Bayly & Dutcher, 2016; Sartori et al, 2016; King & Sale, 2018; Shingyogi, 2018); this switching must occur at a rate consistent with the ciliary beat frequency which in some organisms can approach 100 Hz
Summary
The rhythmic beating of cilia and flagella (here the term cilia is mainly used throughout) is driven by the coordinated action of multiple dynein ATPase motors generating inter-doublet microtubule sliding (Satir, 1968; Summers & Gibbons, 1971). Outer arm dynein HCs in both EHNA-treated sperm and demembranated axonemes were all found in the post-power stroke (inactive) state tightly bound to the B-tubule.
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