Coordinated Ciliary Beating Requires Odf2-Mediated Polarization of Basal Bodies via Basal Feet

Kunimoto, Koshi; Yamazaki, Y.; Nishida, Tomoki; Shinohara, Kyosuke; Ishikawa, Hiroaki; Hasegawa, Toshiaki; Okanoue, Takeshi; Hamada, Hiroshi; Noda, Tetsuo; Tamura, Atsushi; Tsukita, Shöichiro; Tsukita, Sachiko

doi:10.1016/j.cell.2011.10.052

Cited by 189 publications

(284 citation statements)

References 47 publications

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“…Such strategies are vital not only in microswimmers bearing few flagella but also in ciliary arrays. In mice, defects in structures known as basal feet can cause ciliopathies (21), whereas the striated (kinetodesmal) fibers in Tetrahymena help maintain BB orientation and resist hydrodynamic stresses (22). Insights from primitive flagellates may thus have significant broader implications.…”

Section: Significancementioning

confidence: 99%

Coordinated beating of algal flagella is mediated by basal coupling

Wan

Goldstein

2016

Proc. Natl. Acad. Sci. U.S.A.

163

193

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Cilia and flagella often exhibit synchronized behavior; this includes phase locking, as seen in Chlamydomonas, and metachronal wave formation in the respiratory cilia of higher organisms. Since the observations by Gray and Rothschild of phase synchrony of nearby swimming spermatozoa, it has been a working hypothesis that synchrony arises from hydrodynamic interactions between beating filaments. Recent work on the dynamics of physically separated pairs of flagella isolated from the multicellular alga Volvox has shown that hydrodynamic coupling alone is sufficient to produce synchrony. However, the situation is more complex in unicellular organisms bearing few flagella. We show that flagella of Chlamydomonas mutants deficient in filamentary connections between basal bodies display markedly different synchronization from the wild type. We perform micromanipulation on configurations of flagella and conclude that a mechanism, internal to the cell, must provide an additional flagellar coupling. In naturally occurring species with 4, 8, or even 16 flagella, we find diverse symmetries of basal body positioning and of the flagellar apparatus that are coincident with specific gaits of flagellar actuation, suggesting that it is a competition between intracellular coupling and hydrodynamic interactions that ultimately determines the precise form of flagellar coordination in unicellular algae.

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Section: Significancementioning

confidence: 99%

Coordinated beating of algal flagella is mediated by basal coupling

Wan

Goldstein

2016

Proc. Natl. Acad. Sci. U.S.A.

163

193

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“…ODF2, basal bodies become randomly oriented, resulting in ineffective cilia-driven flow (Kunimoto et al, 2012).…”

Section: Force Generation and Anchoringmentioning

confidence: 99%

Centrosome positioning in vertebrate development

Tang

Marshall

2012

Journal of Cell Science

115

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SummaryThe centrosome, a major organizer of microtubules, has important functions in regulating cell shape, polarity, cilia formation and intracellular transport as well as the position of cellular structures, including the mitotic spindle. By means of these activities, centrosomes have important roles during animal development by regulating polarized cell behaviors, such as cell migration or neurite outgrowth, as well as mitotic spindle orientation. In recent years, the pace of discovery regarding the structure and composition of centrosomes has continuously accelerated. At the same time, functional studies have revealed the importance of centrosomes in controlling both morphogenesis and cell fate decision during tissue and organ development. Here, we review examples of centrosome and centriole positioning with a particular emphasis on vertebrate developmental systems, and discuss the roles of centrosome positioning, the cues that determine positioning and the mechanisms by which centrosomes respond to these cues. The studies reviewed here suggest that centrosome functions extend to the development of tissues and organs in vertebrates.

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“…S6). Thus, the core features of basal bodies appear largely normal in bbof1 morphants, including the basal foot that was previously implicated in planar orientation (Kunimoto et al, 2012). The basal bodies in bbof1 morphants could have defects in more peripheral appendages or the way in which these appendages attach to cytoskeletal elements.…”

Section: Basal Body Structure In Bbof1 Morphantsmentioning

confidence: 83%

“…As is the case with odf2, which has been clearly shown to function both during basal body docking as part of the distal fibers and during cilia orientation as part of the basal foot, bbof1 could also contribute to several distinct parts of the ciliary apparatus (Kunimoto et al, 2012). Bbof1-GFP localizes transiently to the basal body, raising the possibility that bbof1 mediates the maturation of a basal body attachment point around the time cilia orientation is established.…”

Section: Research Articlementioning

confidence: 99%

“…One such attachment point is the basal foot, a subdistal appendage that extends off the cylindrical wall of the basal body in the direction of ciliary flow. Loss of the basal foot, as occurs in Odf2 3469 RESEARCH ARTICLE Maturation of cilia orientation mouse mutants, leads to ciliary disorientation (Kunimoto et al, 2012). The basal foot has long been known to be an attachment point for microtubules, and a more recent study describes a link to a specific population of tyrosinated microtubules that extend in a planar fashion to localized PCP components .…”

Section: Introductionmentioning

confidence: 99%

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Bbof1 is required to maintain cilia orientation

et al. 2013

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SUMMARYMulticiliate cells (MCCs) are highly specialized epithelial cells that employ hundreds of motile cilia to produce a vigorous directed flow in a variety of organ systems. The production of this flow requires the establishment of planar cell polarity (PCP) whereby MCCs align hundreds of beating cilia along a common planar axis. The planar axis of cilia in MCCs is known to be established via the PCP pathway and hydrodynamic cues, but the downstream steps required for cilia orientation remain poorly defined. Here, we describe a new component of cilia orientation, based on the phenotypic analysis of an uncharacterized coiled-coil protein, called bbof1. We show that the expression of bbof1 is induced during the early phases of MCC differentiation by the master regulator foxj1. MCC differentiation and ciliogenesis occurs normally in embryos where bbof1 activity is reduced, but cilia orientation is severely disrupted. We show that cilia in bbof1 mutants can still respond to patterning and hydrodynamic cues, but lack the ability to maintain their precise orientation. Misexpression of bbof1 promotes cilia alignment, even in the absence of flow or in embryos where microtubules and actin filaments are disrupted. Bbof1 appears to mediate cilia alignment by localizing to a polar structure adjacent to the basal body. Together, these results suggest that bbof1 is a basal body component required in MCCs to align and maintain cilia orientation in response to flow.

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Coordinated Ciliary Beating Requires Odf2-Mediated Polarization of Basal Bodies via Basal Feet

Cited by 189 publications

References 47 publications

Coordinated beating of algal flagella is mediated by basal coupling

Coordinated beating of algal flagella is mediated by basal coupling

Centrosome positioning in vertebrate development

Bbof1 is required to maintain cilia orientation

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