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Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons

Nature Cell Biology volume 6, pages 1109–1113 (2004)Cite this article

Abstract

Cilia have diverse roles in motility and sensory reception and their dysfunction contributes to cilia-related diseases. Assembly and maintenance of cilia depends on the intraflagellar transport (IFT) of axoneme, membrane, matrix and signalling proteins to appropriate destinations within the organelle1,2,3,4. In the current model, these diverse cargo proteins bind to multiple sites on macromolecular IFT particles, which are moved by a single anterograde IFT motor, kinesin-II, from the ciliary base to its distal tip5,6, where cargo-unloading occurs1,2,3,4,7. Here, we describe the observation of fluorescent IFT motors and IFT particles moving along distinct domains within sensory cilia of wild-type and IFT-motor-mutant Caenorhabditis elegans. We show that two anterograde IFT motor holoenzymes, kinesin-II and Osm-3–kinesin8, cooperate in a surprising way to control two pathways of IFT that build distinct parts of cilia. Instead of each motor independently moving its own specific cargo to a distinct destination, the two motors function redundantly to transport IFT particles along doublet microtubules adjacent to the transition zone to form the axoneme middle segment9. Next, Osm-3–kinesin alone transports IFT particles along the distal singlet microtubules to stabilize the distal segment. Thus, the subtle coordinate activity of these IFT motors creates two sequential transport pathways.

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Figure 1: Sensory cilia on neurons of wild-type and mutant C. elegans.
Figure 2: Anterograde IFT along middle and distal segments of sensory cilia.

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Acknowledgements

We thank G. Civelekoglu-Scholey for drawing Fig. 2b, and L. Rose, F. McNally, K. B. Kaplan, D. Starr, W. Snell, J. Pan and many members of the IFT and C. elegans communities for encouragement and discussion. We thank T. Stiernagle, R. Herman and the C. elegans gene-knockout consortium for providing kinesin-II mutants. This work was supported by a grant from the National Institutes of Health.

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  1. Joshua J. Snow and Guangshuo Ou: These authors contributed equally to this work.

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  1. Center for Genetics and Development, Section of Molecular and Cellular Biology, University of California, Davis, 95616, CA, USA

    Joshua J. Snow, Guangshuo Ou, Amy L. Gunnarson, M. Regina S. Walker, H. Mimi Zhou, Ingrid Brust-Mascher & Jonathan M. Scholey

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Snow, J., Ou, G., Gunnarson, A. et al. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nat Cell Biol 6, 1109–1113 (2004). https://doi.org/10.1038/ncb1186

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