Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II

Hirota, Yuki; Meunier, Anne; Huang, Shihhui; Togo, Shinji; Yamada, Osamu; Kida, Yasuyuki S.; Inoue, Masashi; Ito, Tsugutaka; Kato, Hiroko; Sakaguchi, Masanori; Sunabori, Takehiko; Nakaya, Muneo; Nonaka, Shigenori; Ogura, Toshihiko; Higuchi, Hideo; Okano, Hideyuki; Spassky, Nathalie; Sawamoto, Kazunobu

doi:10.1242/dev.050120

Cited by 100 publications

(123 citation statements)

References 42 publications

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“…The mean induced-flow direction is perpendicular to the main axis of the cilium. Such a beating pattern has been observed in embryonic nervous epithelium in mice (Sanderson and Sleigh, 1981;Hirota et al, 2010) and possibly in tissues of other species, such as in the LR organizer (Schweickert et al, 2007) or the larval skin (Mitchell et al, 2009) in Xenopus. Interestingly, the beating frequency of cilia is rather similar between species and organs, and usually varies between 10 and 30 Hz (Supatto and Vermot, 2011).…”

Section: Directional Cilia-driven Flows: Theory and Modelingmentioning

confidence: 72%

Fluid flows and forces in development: functions, features and biophysical principles

et al. 2012

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Throughout morphogenesis, cells experience intracellular tensile and contractile forces on microscopic scales. Cells also experience extracellular forces, such as static forces mediated by the extracellular matrix and forces resulting from microscopic fluid flow. Although the biological ramifications of static forces have received much attention, little is known about the roles of fluid flows and forces during embryogenesis. Here, we focus on the microfluidic forces generated by cilia-driven fluid flow and heart-driven hemodynamics, as well as on the signaling pathways involved in flow sensing. We discuss recent studies that describe the functions and the biomechanical features of these fluid flows. These insights suggest that biological flow determines many aspects of cell behavior and identity through a specific set of physical stimuli and signaling pathways.

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Section: Directional Cilia-driven Flows: Theory and Modelingmentioning

confidence: 72%

Fluid flows and forces in development: functions, features and biophysical principles

et al. 2012

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“…We showed that non-muscle myosin II and the Wnt/PCP pathway distinctly regulate the processes responsible for generating translational and rotational polarity, respectively. 47,48 These results suggest that the distribution and orientation of basal bodies are regulated by distinct mechanisms, and that both contribute to the control of CSF flow.…”

Section: Fig 2 Regulation Of Svz Neurogenesis By Wnt Signalingmentioning

confidence: 86%

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

Sawada

Sawamoto

2013

Keio J. Med.

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Even in the adult brain, new neurons are continuously generated from endogenous neural stem cells that reside in two restricted regions: the subventricular zone (SVZ) of the lateral ventricle and the dentate gyrus of the hippocampus. These new neurons are integrated into the mature neuronal circuitry and become involved in various functions, thereby contributing to structural and functional plasticity in the adult brain. In this review, we summarize our recent findings on the regulatory mechanisms of SVZ neurogenesis under physiological and pathological conditions in various animal models. Some of these findings were presented in the Kitazato Prize Lecture at Keio University School of Medicine in

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“…This alignment of the polarity of ciliated cells is an example of planar cell polarity (PCP), which is the polarity of epithelial cells in a plane perpendicular to their apical-basal axis. Recent studies have revealed that PCP genes regulate ciliary polarity in frog epidermis (Mitchell et al, 2009;Park et al, 2008), the mouse brain ventricle (Guirao et al, 2010;Hirota et al, 2010;Tissir et al, 2010), the mouse embryonic node (Antic et al, 2010;Hashimoto et al, 2010;Song et al, 2010), the zebrafish Kupffer's vesicle (Borovina et al, 2010;May-Simera et al, 2010) and the mouse trachea (Vladar et al, 2012). However, as yet, the roles of PCP genes in the oviduct epithelium have not been studied.…”

Section: Introductionmentioning

confidence: 99%

Celsr1 is required for the generation of polarity at multiple levels of the mouse oviduct

et al. 2014

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The oviduct is an important organ in reproduction where fertilization occurs, and through which the fertilized eggs are carried to the uterus in mammals. This organ is highly polarized, where the epithelium forms longitudinal folds along the ovary-uterus axis, and the epithelial multicilia beat towards the uterus to transport the ovulated ova. Here, we analyzed the postnatal development of mouse oviduct and report that multilevel polarities of the oviduct are regulated by a planar cell polarity (PCP) gene, Celsr1. In the epithelium, Celsr1 is concentrated in the specific cellular boundaries perpendicular to the ovary-uterus axis from postnatal day 2. We found a new feature of cellular polarity in the oviduct -the apical surface of epithelial cells is elongated along the ovary-uterus axis. In Celsr1-deficient mice, the ciliary motion is not orchestrated along the ovary-uterus axis and the transport ability of beating cilia is impaired. Epithelial cells show less elongation and randomized orientation, and epithelial folds show randomized directionality and ectopic branches in the mutant. Our mosaic analysis suggests that the geometry of epithelial cells is primarily regulated by Celsr1 and as a consequence the epithelial folds are aligned. Taken together, we reveal the characteristics of the multilevel polarity formation processes in the mouse oviduct epithelium and suggest a novel function of the PCP pathway for proper tissue morphogenesis.

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Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II

Cited by 100 publications

References 42 publications

Fluid flows and forces in development: functions, features and biophysical principles

Fluid flows and forces in development: functions, features and biophysical principles

Mechanisms of Neurogenesis in the Normal and Injured Adult Brain

Celsr1 is required for the generation of polarity at multiple levels of the mouse oviduct

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