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Vol. 18, Issue 5, 1554-1569, May 2007

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Sensory Ciliogenesis in Caenorhabditis elegans: Assignment of IFT Components into Distinct Modules Based on Transport and Phenotypic Profiles

Guangshuo Ou^*, Makato Koga^,, Oliver E. Blacque^,,||, Takashi Murayama, Yasumi Ohshima, Jenny C. Schafer^¶, Chunmei Li, Bradley K. Yoder^¶, Michel R. Leroux, and Jonathan M. Scholey^*

*Center for Genetics and Development, Section of Molecular and Cellular Biology, University of California, Davis, CA 95616; Department of Biology, Faculty of Sciences, Kyushu University Graduate School, 6-10-1, Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan; Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, BC V5A 1S6, Canada; ^||School of Biomolecular and Biomedical Science, University College Dublin Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland; and ^¶Department of Cell Biology, University of Alabama at Birmingham Medical Center, Birmingham, AL 35294

Submitted September 11, 2006; Revised February 2, 2007; Accepted February 7, 2007
Monitoring Editor: Erika Holzbaur

Sensory cilium biogenesis within Caenorhabditis elegans neurons depends on the kinesin-2–dependent intraflagellar transport (IFT) of ciliary precursors associated with IFT particles to the axoneme tip. Here we analyzed the molecular organization of the IFT machinery by comparing the in vivo transport and phenotypic profiles of multiple proteins involved in IFT and ciliogenesis. Based on their motility in wild-type and bbs (Bardet-Biedl syndrome) mutants, IFT proteins were classified into groups with similar transport profiles that we refer to as "modules." We also analyzed the distribution and transport of fluorescent IFT particles in multiple known ciliary mutants and 49 new ciliary mutants. Most of the latter mutants were snip-SNP mapped and one, namely dyf-14(ks69), was cloned and found to encode a conserved protein essential for ciliogenesis. The products of these ciliogenesis genes could also be assigned to the aforementioned set of modules or to specific aspects of ciliogenesis, based on IFT particle dynamics and ciliary mutant phenotypes. Although binding assays would be required to confirm direct physical interactions, the results are consistent with the hypothesis that the C. elegans IFT machinery has a modular design, consisting of modules IFT-subcomplex A, IFT-subcomplex B, and a BBS protein complex, in addition to motor and cargo modules, with each module contributing to distinct functional aspects of IFT or ciliogenesis.

The online version of this article contains supplemental material at MBC Online (http://www.molbiolcell.org).

These authors contributed equally to this work.

Address correspondence to: Michel R. Leroux (leroux{at}sfu.ca) or Jonathan M. Scholey (jmscholey{at}ucdavis.edu)

Abbreviations used: IFT, intraflagellar transport; BBS, Bardet-Biedl syndrome.

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