Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans

James E. Evans, Joshua J. Snow, Amy L. Gunnarson, Guangshuo Ou, Henning Stahlberg, Kent L. McDonald, Jonathan M. Scholey

Research output: Contribution to journalArticle

88 Citations (Scopus)

Abstract

The diversity of sensory cilia on Caenorhabditis elegans neurons allows the animal to detect a variety of sensory stimuli. Sensory cilia are assembled by intraflagellar transport (IFT) kinesins, which transport ciliary precursors, bound to IFT particles, along the ciliary axoneme for incorporation into ciliary structures. Using fluorescence microscopy of living animals and serial section electron microscopy of high pressure-frozen, freeze-substituted IFT motor mutants, we found that two IFT kinesins, homodimeric OSM-3 kinesin and heterotrimeric kinesin II, function in a partially redundant manner to build full-length amphid channel cilia but are completely redundant for building full-length amphid wing (AWC) cilia. This difference reflects cilia-specific differences in OSM-3 activity, which serves to extend distal singlets in channel cilia but not in AWC cilia, which lack such singlets. Moreover, AWC-specific chemotaxis assays reveal novel sensory functions for kinesin II in these wing cilia. We propose that kinesin II is a "canonical" IFT motor, whereas OSM-3 is an "accessory" IFT motor, and that subtle changes in the deployment or actions of these IFT kinesins can contribute to differences in cilia morphology, cilia function, and sensory perception.

Original languageEnglish (US)
Pages (from-to)663-669
Number of pages7
JournalJournal of Cell Biology
Volume172
Issue number5
DOIs
StatePublished - Feb 27 2006

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Kinesin
Cilia
Caenorhabditis elegans
Neurons
Axoneme
Chemotaxis
Fluorescence Microscopy
Electron Microscopy
Pressure

ASJC Scopus subject areas

  • Cell Biology

Cite this

Evans, J. E., Snow, J. J., Gunnarson, A. L., Ou, G., Stahlberg, H., McDonald, K. L., & Scholey, J. M. (2006). Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. Journal of Cell Biology, 172(5), 663-669. https://doi.org/10.1083/jcb.200509115

Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. / Evans, James E.; Snow, Joshua J.; Gunnarson, Amy L.; Ou, Guangshuo; Stahlberg, Henning; McDonald, Kent L.; Scholey, Jonathan M.

In: Journal of Cell Biology, Vol. 172, No. 5, 27.02.2006, p. 663-669.

Research output: Contribution to journalArticle

Evans, JE, Snow, JJ, Gunnarson, AL, Ou, G, Stahlberg, H, McDonald, KL & Scholey, JM 2006, 'Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans', Journal of Cell Biology, vol. 172, no. 5, pp. 663-669. https://doi.org/10.1083/jcb.200509115
Evans, James E. ; Snow, Joshua J. ; Gunnarson, Amy L. ; Ou, Guangshuo ; Stahlberg, Henning ; McDonald, Kent L. ; Scholey, Jonathan M. / Functional modulation of IFT kinesins extends the sensory repertoire of ciliated neurons in Caenorhabditis elegans. In: Journal of Cell Biology. 2006 ; Vol. 172, No. 5. pp. 663-669.
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