Biophysical Journal
Volume 97, Issue 11, 2 December 2009, Pages 2939-2947
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Article
Simulation of Cyclic Dynein-Driven Sliding, Splitting, and Reassociation in an Outer Doublet Pair

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Abstract

A regular cycle of dynein-driven sliding, doublet separation, doublet reassociation, and resumption of sliding was previously observed by Aoyama and Kamiya in outer doublet pairs obtained after partial dissociation of Chlamydomonas flagella. In the work presented here, computer programming based on previous simulations of oscillatory bending of microtubules was extended to simulate the cycle of events observed with doublet pairs. These simulations confirm the straightforward explanation of this oscillation by inactivation of dynein when doublets separate and resumption of dynein activity after reassociation. Reassociation is augmented by a dynein-dependent “adhesive force” between the doublets. The simulations used a simple mathematical model to generate velocity-dependent shear force, and an independent elastic model for adhesive force. Realistic results were obtained with a maximum adhesive force that was 36% of the maximum shear force. Separation between a pair of doublets is the result of a buckling instability that also initiates a period of uniform sliding that enlarges the separation. A similar instability may trigger sliding initiation events in flagellar bending cycles.

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