Abstract
Through their coordinated alignment and beating, motile cilia generate directional fluid flow and organismal movement. While the mechanisms used by multiciliated epithelial tissues to achieve this coordination have been widely studied, much less is known about regulation of monociliated tissues such as those found in the vertebrate node and swimming planktonic larvae. Here, we show that a calcium sensor protein associated with outer arm dynein, calaxin, is a critical regulator for the coordinated movements of monocilia. Knockdown of calaxin gene in sea urchin embryos results in uncoordinated ciliary beating and defective directional movement of the embryos, but no apparent abnormality in axoneme ultrastructure. Examination of the beating cycle of individual calaxin-deficient cilia revealed a marked effect on the waveform and spatial range of ciliary bending. These findings indicate that calaxin-mediated regulation of ciliary beating is responsible for proper basal body orientation and ciliary alignment in fields of monociliated cells.
Highlights
In vertebrates, two types of cilia are present in terms of the number of cilium per cell: monocilia and multicilia[1, 2]
We analyzed the beating of individual cilia using high speed camera and found that initially (14 hpf) the direction of ciliary beating is random with respect to the embryonic axis but by 24 hpf it becomes oriented in an anterior to posterior direction (Fig. 1C; Supplementary Videos S3 and S4)
To determine if calaxin is involved in the orientation of ciliary basal structures, we examined the distribution of two marker proteins, γ-tubulin and atypical protein kinase C which like BBS1 is localized at the base of cilia and forms a ring-like structure at the transition zone of cilia in the Paracentrotus lividus sea urchin embryo[22]
Summary
Two types of cilia are present in terms of the number of cilium per cell: monocilia and multicilia[1, 2]. The direction of ciliary movement depends on the orientation of the basal body, which is primarily determined by the planar cell polarity (PCP) pathway during differentiation of epithelial tissues[3,4,5]. Coordination of ciliary movement as well as the orientations of basal bodies are highly responsive to the fluid-mediated hydrodynamic interactions between neighboring cilia[6, 7]. Because calaxin is an opisthokont-specific molecule and present in ciliated cells other than sperm[14, 16], we suspected that it may function in the Ca2+-dependent regulation of ciliary movements in epithelial tissues. From a series of experiments, we found that calaxin is essential for establishing the orientation of ciliary basal structures
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