RRC ID 65253
Author Xie C, Li L, Li M, Shao W, Zuo Q, Huang X, Chen R, Li W, Brunnbauer M, Ökten Z, Chen L, Ou G.
Title Optimal sidestepping of intraflagellar transport kinesins regulates structure and function of sensory cilia.
Journal EMBO J
Abstract Cytoskeletal-based molecular motors produce force perpendicular to their direction of movement. However, it remains unknown whether and why motor proteins generate sidesteps movement along their filamentous tracks in vivo. Using Hessian structured illumination microscopy, we located green fluorescent protein (GFP)-labeled intraflagellar transport (IFT) particles inside sensory cilia of live Caenorhabditis elegans with 3-6-nanometer accuracy and 3.4-ms resolution. We found that IFT particles took sidesteps along axoneme microtubules, demonstrating that IFT motors generate torque in a living animal. Kinesin-II and OSM-3-kinesin collaboratively drive anterograde IFT. We showed that the deletion of kinesin-II, a torque-generating motor protein, reduced sidesteps, whereas the increase of neck flexibility of OSM-3-kinesin upregulated sidesteps. Either increase or decrease of sidesteps of IFT kinesins allowed ciliogenesis to the regular length, but changed IFT speeds, disrupted axonemal ninefold symmetry, and inhibited sensory cilia-dependent animal behaviors. Thus, an optimum level of IFT kinesin sidestepping is associated with the structural and functional fidelity of cilia.
Volume 39(12)
Pages e103955
Published 2020-6-17
DOI 10.15252/embj.2019103955
PMID 32338401
PMC PMC7298308
MeSH Animals Animals, Genetically Modified / genetics Animals, Genetically Modified / metabolism* Axoneme / genetics Axoneme / metabolism* Caenorhabditis elegans / genetics Caenorhabditis elegans / metabolism* Caenorhabditis elegans Proteins / genetics Caenorhabditis elegans Proteins / metabolism* Cilia / genetics Cilia / metabolism* Kinesins / genetics Kinesins / metabolism*
Resource
C.elegans tm324