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

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

Research output: Contribution to journalArticle

259 Citations (Scopus)

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 organelle. 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 tip, where cargo-unloading occurs. 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-kinesin, 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 segment. 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.

Original languageEnglish (US)
Pages (from-to)1109-1113
Number of pages5
JournalNature Cell Biology
Volume6
Issue number11
DOIs
StatePublished - Nov 2004

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Cilia
Neurons
Axoneme
Kinesin
Microtubules
Holoenzymes
Caenorhabditis elegans
Organelles
Proteins
Maintenance
Observation
Membranes
kinesin-II

ASJC Scopus subject areas

  • Cell Biology

Cite this

Snow, J. J., Ou, G., Gunnarson, A. L., Walker, M. R. S., Zhou, H. M., Brust-Mascher, I., & Scholey, J. M. (2004). Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nature Cell Biology, 6(11), 1109-1113. https://doi.org/10.1038/ncb1186

Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. / Snow, Joshua J.; Ou, Guangshuo; Gunnarson, Amy L.; Walker, M. Regina S; Zhou, H. Mimi; Brust-Mascher, Ingrid; Scholey, Jonathan M.

In: Nature Cell Biology, Vol. 6, No. 11, 11.2004, p. 1109-1113.

Research output: Contribution to journalArticle

Snow, JJ, Ou, G, Gunnarson, AL, Walker, MRS, Zhou, HM, Brust-Mascher, I & Scholey, JM 2004, 'Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons', Nature Cell Biology, vol. 6, no. 11, pp. 1109-1113. https://doi.org/10.1038/ncb1186
Snow JJ, Ou G, Gunnarson AL, Walker MRS, Zhou HM, Brust-Mascher I et al. Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. Nature Cell Biology. 2004 Nov;6(11):1109-1113. https://doi.org/10.1038/ncb1186
Snow, Joshua J. ; Ou, Guangshuo ; Gunnarson, Amy L. ; Walker, M. Regina S ; Zhou, H. Mimi ; Brust-Mascher, Ingrid ; Scholey, Jonathan M. / Two anterograde intraflagellar transport motors cooperate to build sensory cilia on C. elegans neurons. In: Nature Cell Biology. 2004 ; Vol. 6, No. 11. pp. 1109-1113.
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