The geometric clutch at 20: stripping gears or gaining traction?

Abstract

It has been 20 years since the geometric clutch (GC) hypothesis was first proposed. The core principle of the GC mechanism is fairly simple. When the axoneme of a eukaryotic flagellum is bent, mechanical stress generates forces transverse to the outer doublets (t-forces). These t-forces can push doublets closer together or pry them apart. The GC hypothesis asserts that changes in the inter-doublet spacing caused by t-forces are responsible for the activation and deactivation of the dynein motors, that creates the beat cycle. A series of computer models utilizing the clutch mechanism has shown that it can simulate ciliary and flagellar beating. The objective of the present review is to assess where things stand with the GC hypothesis in the clarifying light of new information. There is considerable new evidence to support the hypothesis. However, it is also clear that it is necessary to modify some of the original conceptions of the hypothesis so that it can be consistent with the results of recent experimental and ultrastructural studies. In particular, dynein deactivation by t-forces must be able to occur with dyneins that remain attached to the B-subtubule of the adjacent doublet.Reproduction (2015) 150 R45-R53

Direction of flagellum beat propagation is controlled by proximal/distal outer dynein arm asymmetry

“…The leading model is arguably the geometric clutch hypothesis, which states that mechanical distortion of the axoneme as it bends regulates force generation by regulating dynein arm engagement (25,58,59). The simplest interpretation of our results in the context of this hypothesis is that the distal docking complex positions the distal ODAs so they are more likely than the proximal ODAs to spontaneously engage and start a flagellar waveform (although more complex interpretations, like involvement of the IDAs, are also possible).…”

Radial Spokes—A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella

“…The selection appears determined by the CP with asymmetric projections (see Loreng and Smith 2016). The geometric clutch model (Lindemann and Lesich 2015) offers an explicit explanation of mechanical feedback. It posits that the CP and RSs, which contact intermittently during each beat cycle (Warner and Satir 1974), transmit transverse forces developed from flagellar bend, which in turn differentially alter the distances among doublets confined by the base, tip, and N-DRC links.…”

Effects of external strain on the regulation of microtubule sliding induced by outer arm dynein of sea urchin sperm flagella

“…The direction of the external strain (the red arrow) relative to the direction of the active sliding (the black arrow) is the same as that of the elastic strain in the interbend region of an axoneme (A). Lindemann and Lesich, 2015), and signals related to calcium ion (Brokaw, 1979). The present result suggests that isolated outer arm dyneins have the ability to respond to mechanical signals of strain, which might reflect an important aspect of the communication within a beating axoneme and a basic requirement for the overall flagellar oscillation.…”

“…Stoppage of sliding in the present study suggests that this is also the case even at a high, physiological concentration (1 mmol l −1 ) of ATP. Furthermore, in addition to transverse strain (t-force; Lindemann and Lesich, 2015), the present study indicates that backward, parallel strain may also be important in inducing stoppage of sliding.…”