Absence of Radial Spokes in Mouse Node Cilia Is Required for Rotational Movement but Confers Ultrastructural Instability as a Trade-Off

• Published in: Developmental cell Vol. 35; no. 2; pp. 236 - 246
• Main Authors: Shinohara, Kyosuke, Chen, Duanduan, Nishida, Tomoki, Misaki, Kazuyo, Yonemura, Shigenobu, Hamada, Hiroshi
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 26.10.2015
• Subjects: Animals; Body Patterning - genetics; Cilia - genetics; Cilia - physiology; Cilia - ultrastructure; Embryo, Mammalian; Embryonic Development - drug effects; Embryonic Development - genetics; Mice; Microtubules - drug effects; Microtubules - ultrastructure; Paclitaxel - administration & dosage
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2015.10.001

Determination of left-right asymmetry in mouse embryos is established by a leftward fluid flow that is generated by clockwise rotation of node cilia. How node cilia achieve stable unidirectional rotation has remained unknown, however. Here we show that brief exposure to the microtubule-stabilizing drug paclitaxel (Taxol) induces randomly directed rotation and changes the ultrastructure of node cilia. In vivo observations and a computer simulation revealed that a regular 9+0 arrangement of doublet microtubules is essential for stable unidirectional rotation of node cilia. The 9+2 motile cilia of the airway, which manifest planar beating, are resistant to Taxol treatment. However, the airway cilia of mice lacking the radial spoke head protein Rsph4a undergo rotational movement instead of planar beating, are prone to microtubule rearrangement, and are sensitive to Taxol. Our results suggest that the absence of radial spokes allows node cilia to rotate unidirectionally but, as a trade-off, renders them ultrastructurally fragile. [Display omitted] •Mouse node cilia but not airway cilia are sensitive to microtubule destabilization•Node cilia rotation requires a 9+0 doublet MT structure with no radial spokes•Radial spokes are required to maintain an airway cilia 9+2 structure and beating motion•Lack of radial spokes induces rotational motion but makes the MT ultrastructure fragile How do mammalian cilia sustain a specific pattern of motion? Shinohara et al. show that radial spokes in the ciliary microtubule structure are determinates of ciliary motion. Radial spokes maintain airway cilia beating motion, whereas their absence from node cilia allows for unidirectional rotation but renders them ultrastructurally fragile.