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

Xiaoyu Pan, Guangshuo Ou, Gul Civelekoglu-Scholey, Oliver E. Blacque, Nicholas F. Endres, Li Tao, Alex Mogilner, Michel R. Leroux, Ronald D. Vale, Jonathan M. Scholey

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Pages (from-to)1035-1045
Number of pages11
JournalJournal of Cell Biology
Volume174
Issue number7
DOIs
StatePublished - Sep 25 2006

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Cilia
Bardet-Biedl Syndrome
Kinesin
Microtubules
Caenorhabditis elegans
Protein Transport
Neurons
kinesin-II
Proteins

ASJC Scopus subject areas

  • Cell Biology

Cite this

Pan, X., Ou, G., Civelekoglu-Scholey, G., Blacque, O. E., Endres, N. F., Tao, L., ... Scholey, J. M. (2006). Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. Journal of Cell Biology, 174(7), 1035-1045. https://doi.org/10.1083/jcb.200606003

Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. / Pan, Xiaoyu; Ou, Guangshuo; Civelekoglu-Scholey, Gul; Blacque, Oliver E.; Endres, Nicholas F.; Tao, Li; Mogilner, Alex; Leroux, Michel R.; Vale, Ronald D.; Scholey, Jonathan M.

In: Journal of Cell Biology, Vol. 174, No. 7, 25.09.2006, p. 1035-1045.

Research output: Contribution to journalArticle

Pan, X, Ou, G, Civelekoglu-Scholey, G, Blacque, OE, Endres, NF, Tao, L, Mogilner, A, Leroux, MR, Vale, RD & Scholey, JM 2006, 'Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors', Journal of Cell Biology, vol. 174, no. 7, pp. 1035-1045. https://doi.org/10.1083/jcb.200606003
Pan, Xiaoyu ; Ou, Guangshuo ; Civelekoglu-Scholey, Gul ; Blacque, Oliver E. ; Endres, Nicholas F. ; Tao, Li ; Mogilner, Alex ; Leroux, Michel R. ; Vale, Ronald D. ; Scholey, Jonathan M. / Mechanism of transport of IFT particles in C. elegans cilia by the concerted action of kinesin-II and OSM-3 motors. In: Journal of Cell Biology. 2006 ; Vol. 174, No. 7. pp. 1035-1045.
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