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

Shinohara, Kyosuke; Chen, Duanduan; Nishida, Tomoki; Misaki, Kazuyo; Yonemura, Shigenobu; Hamada, Hiroshi

doi:10.1016/j.devcel.2015.10.001

Cited by 56 publications

(61 citation statements)

References 63 publications

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“…But such movement may not be appropriate for a select few. The lowfrequency helical beat of 9þ0 nodal cilia may be just right for establishing a gradient of morphogens that direct the development of leftright asymmetry (Nonaka et al 2002;Shinohara et al 2015). By the same token, 3D-bihelical movement is what Trypanosome adopt to navigate in the viscous bloodstream.…”

Section: Generation Of Planar Waveformmentioning

confidence: 99%

Radial Spokes—A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella

Zhu

Liu

Yang

2016

Cold Spring Harb Perspect Biol

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Section: Generation Of Planar Waveformmentioning

confidence: 99%

Radial Spokes—A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella

Zhu

Liu

Yang

2016

Cold Spring Harb Perspect Biol

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“…The ultrastructure of the cilia, especially the morphology of doublet MTs, plays a crucial role in controlling the movement of the cilium [32]. The main ultrastructure of wild-type nodal cilia contains a ring of nine outer doublet MTs, which are approximately evenly distributed around the center.…”

Section: O R P H O L O G I C a L Analysismentioning

confidence: 99%

“…Dissected embryos were cultured at 37°C in phenol red-free DMEM supplemented with 75% rat serum (Invitrogen). The experimental data obtained in our previous study [32] were analyzed in the previous and the present studies, which focused on the Taxol-treated nodal cilia and inv mutant cilium, respectively.…”

Section: Imaging Data Acquisitionmentioning

confidence: 99%

The Motion of An Inv Nodal Cilium: a Realistic Model Revealing Dynein-Driven Ciliary Motion with Microtubule Mislocalization

Shinohara

et al. 2018

Cell Physiol Biochem

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Background/Aims: Nodal cilia that rotate in the ventral node play an important role in establishing left-right asymmetry during embryogenesis; however, inv mutant cilia present abnormal movement and induce laterality defects. The mechanism of their motility, which is regulated by dynein activation and microtubule arrangement, has not been fully understood. This study analyzed the dynein-triggered ciliary motion in the abnormal ultrastructure of the inv mutant, aiming to quantitatively evaluate the influence of microtubule mislocalization on the movement of the cilium. Methods: We established a realistic 3-D model of an inv mutant cilium with an ultrastructure based on tomographic datasets generated by ultra-high voltage electron microscopy. The time-variant activation of the axonemal dynein force was simulated by pairs of point loads and embedded at dynein-mounted positions between adjacent microtubule doublets in this mathematical model. Utilizing the finite element method and deformable grid, the motility of the mutant cilium that is induced by various dynein activation hypotheses was investigated and compared to experimental observation. Results: The results indicate that for the inv mutant, simulations of the ciliary movement with the engagement of dyneins based on the distance-controlled pattern in the partially activation scenario are broadly consistent with the observation; the shortening of the microtubules induces smaller movement amplitudes, while the angles of the mislocalized microtubules affect the pattern of the ciliary movement, and during the ciliary movement, the microtubules swing and twist in the mutant ciliary body. Conclusion: More generally, this study implies that dynein engagement is sensitive to subtle geometric changes in the axoneme, and thus, this geometry greatly influences the integrity of a well-formed ciliary rotation.

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“…The nodal ciliary axoneme consists of 9+0 doublets, with each doublet linked to nearby doublets by elastic nexin linkages (Shinohara et al, 2015). The microtubule doublet is composed of a circular A-tubule, which has a complete set of 13 protofilaments, and an adjacent B-tubule (Ueno et al, 2012).…”

Section: Ciliary Axoneme Modelmentioning

confidence: 99%

“…Left-right asymmetry of the vertebrate body plan is achieved in the early embryo (Hirokawa et al, 2009;Shinohara et al, 2015). In the mouse embryo, an embryonic cavity structure is found at the ventral midline surface 7-8 days after fertilization (Hirokawa et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Elastohydrodynamic phase-lock in two rotating cilia

Omori

Ishikawa

2018

JBSE

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Determination of left-right asymmetry of the body plan is achieved in the early embryo. At the 4-6 somite stage, a cavity structure, called a node, is observed in the ventral midline surface, in which hundreds of cilia rotate. Nodal cilia are typically tilted toward the posterior and rotate in the clockwise direction, resulting in the generation of leftward flow in the node. Such leftward flow acts as a trigger of left-specific gene expression, and fluid mechanics plays a role in left-right symmetry breaking. To understand the cilia-driven nodal flow, it is necessary to determine the hydrodynamic interactions among rotating cilia, as ciliary motions interact with each other through fluid motion. In this study, we numerically investigated the elastohydrodynamic synchronization of two rotating cilia, as well as the flow field. The ciliary motion was determined by the balance of cytoskeletal elastic force, motor protein-induced active force, and fluid viscous force. According to the geometric clutch hypothesis, the frequency of rotating cilia is controlled by the bending curvature. Owing to hydrodynamic interactions, bending deformations of two cilia become time-dependent, and the rotation is finally locked in anti-phase regardless of the relative position and initial phase difference. By locking in the reverse phase, the average propulsion flow rate becomes 2-3 times larger than in-phase beating. The results of this study form a basis for understanding cilium-driven nodal flow.

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

Cited by 56 publications

References 63 publications

Radial Spokes—A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella

Radial Spokes—A Snapshot of the Motility Regulation, Assembly, and Evolution of Cilia and Flagella

The Motion of An Inv Nodal Cilium: a Realistic Model Revealing Dynein-Driven Ciliary Motion with Microtubule Mislocalization

Elastohydrodynamic phase-lock in two rotating cilia

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