Strikingly fast microtubule sliding in bundles formed by Chlamydomonas axonemal dynein

Abstract

Chlamydomonas axonemal extracts containing outer-arm dynein bundle microtubules when added in the absence of ATP. The bundles dissociate after addition of ATP (Haimo et al., Proc Natl Acad Sci USA 76:5759-5768, 1979). In the present study, we investigated the ATP-induced bundle dissociation process using caged ATP. Application of approximately 0.5 mM ATP induced microtubule sliding at approximately 30 microm.s(-1), which was 1.5 times faster than the microtubule sliding observed in protease-treated axonemes and five times faster than microtubule gliding on glass surfaces coated with outer-arm dynein. Bundles formed by mutant dynein molecules that lack one of the three heavy chains (HCs) displayed similar high-speed intermicrotubule sliding. These results suggest that Chlamydomonas outer-arm dynein molecules, when aligned, can translocate microtubules at high speed and that the high-speed sliding under load-free conditions does not require the complete set of the three HCs. It is likely that each of the three HCs has the ability to produce high-speed sliding, which should be an important property for their cooperation.