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Published 25 September 2006. doi:10.1083/jcb.200606003
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 174, Number 7, 1035-1045
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Article

Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors



Xiaoyu Pan1, Guangshuo Ou1, Gul Civelekoglu-Scholey1, Oliver E. Blacque2, Nicholas F. Endres3,4, Li Tao1, Alex Mogilner1, Michel R. Leroux2, Ronald D. Vale3,4, and Jonathan M. Scholey1

1 Section of Molecular and Cellular Biology, Center for Genetics and Development, University of California, Davis, Davis, CA 95616
2 Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada
3 Howard Hughes Medical Institute and 4 Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94107

Correspondence to Jonathan M. Scholey: jmscholey{at}ucdavis.edu

The assembly and function of cilia on Caenorhabditis elegans neurons depends on the action of two kinesin-2 motors, heterotrimeric kinesin-II and homodimeric OSM-3–kinesin, which cooperate to move the same intraflagellar transport (IFT) particles along microtubule (MT) doublets. Using competitive in vitro MT gliding assays, we show that purified kinesin-II and OSM-3 cooperate to generate movement similar to that seen along the cilium in the absence of any additional regulatory factors. Quantitative modeling suggests that this could reflect an alternating action mechanism, in which the motors take turns to move along MTs, or a mechanical competition, in which the motors function in a concerted fashion to move along MTs with the slow motor exerting drag on the fast motor and vice versa. In vivo transport assays performed in Bardet-Biedl syndrome (BBS) protein and IFT motor mutants favor a mechanical competition model for motor coordination in which the IFT motors exert a BBS protein–dependent tension on IFT particles, which controls the IFT pathway that builds the cilium foundation.

X. Pan and G. Ou contributed equally to this paper.

Abbreviations used in this paper: BBS, Bardet-Biedl syndrome; IFT, intraflagellar transport; MT, microtubule.


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