Super-resolution Molecular Map of Basal Foot Reveals Novel Cilium in Airway Multiciliated Cells

Nguyen, Quynh P. H.; Liu, Zhen; Nanjundappa, Rashmi; Megherbi, Alexandre; Delgehyr, Nathalie; Ouyang, Hong; Zlock, Lorna; Coyaud, Étienne; Laurent, Estelle; Dell, Sharon; Finkbeiner, Walter E.; Moraes, Theo J.; Raught, Brian; Czymmek, Kirk J.; Munier, Alice; Mahjoub, Moe R.; Mennella, Vito

doi:10.1101/487330

Cited by 4 publications

(5 citation statements)

References 87 publications

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“…They were eventually joined by the procentrioles to form the basal body patch. This was confirmed by fate-tracing centrosomal centrioles using Cen2GFP/Cen-RFP pulse-chase experiments 13 .…”

Section: An Atypical Centrosome Cycle Is Observed During Centriole Ammentioning

confidence: 78%

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

Mercey

Jord

Rostaing

et al. 2018

Preprint

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Centrioles are essential microtubule-based organelles organizing cilia and centrosomes. Their mode of biogenesis is semi-conservative: each pre-existing centriole scaffolds the formation of a new one, a process coordinated with the cell cycle. By contrast, multiciliated progenitors with two centrosomal centrioles massively amplify centrioles to support the nucleation of hundred of motile cilia and transport vital fluids. This occurs through cell type-specific organelles called deuterosomes, composed of centrosome-related elements, and is regulated by the cell cycle machinery. Deuterosome-dependent centriole amplification was proposed for decades to occur de novo, i.e. independently from preexisting centrioles. Challenging this hypothesis, we recently reported an accumulation of procentriole and deuterosome precursors at the centrosomal daughter centriole during centriole amplification in brain multiciliated cells. Here we further investigate the relationship between the centrosome and the dynamic of centriole amplification by (i) characterizing the centrosome behavior during the centriole amplification dynamics and (ii) assessing the dynamics of amplification in centrosome-depleted cells. Surprisingly, although our data strengthen the centrosomal origin of amplified centrioles, we show limited consequences in deuterosome/centriole number when we deplete centrosomal centrioles.

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“…They were eventually joined by the procentrioles to form the basal body patch. This was confirmed by fate-tracing centrosomal centrioles using Cen2GFP/Cen-RFP pulse-chase experiments 13 .…”

Section: An Atypical Centrosome Cycle Is Observed During Centriole Ammentioning

confidence: 78%

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

Mercey

Jord

Rostaing

et al. 2018

Preprint

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“…Additionally, it will be important to understand how the same molecules organize such different basal feet in multiple cell types. Of note, recent studies using super-resolution microscopy showed slightly different relative positions of basal feet components in primary versus motile mammalian cilia (Figure 2) [53].…”

Section: Cilia: Variations Of a Basic Structure To Fulfill Myriad mentioning

confidence: 99%

“…The most proximal region (I) contains proteins that are common to the primary cilia basal feet (i.e. Centrosomal protein of 128 kDa (CEP128) and ODF2) that are most likely responsible for the scaffolding (based on proteomics and super-resolution microscopy data in [53]).…”

Section: Figurementioning

confidence: 99%

Cilia Distal Domain: Diversity in Evolutionarily Conserved Structures

Soares

Carmona

Nolasco

et al. 2019

Cells

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Eukaryotic cilia are microtubule-based organelles that protrude from the cell surface to fulfill sensory and motility functions. Their basic structure consists of an axoneme templated by a centriole/basal body. Striking differences in ciliary ultra-structures can be found at the ciliary base, the axoneme and the tip, not only throughout the eukaryotic tree of life, but within a single organism. Defects in cilia biogenesis and function are at the origin of human ciliopathies. This structural/functional diversity and its relationship with the etiology of these diseases is poorly understood. Some of the important events in cilia function occur at their distal domain, including cilia assembly/disassembly, IFT (intraflagellar transport) complexes’ remodeling, and signal detection/transduction. How axonemal microtubules end at this domain varies with distinct cilia types, originating different tip architectures. Additionally, they show a high degree of dynamic behavior and are able to respond to different stimuli. The existence of microtubule-capping structures (caps) in certain types of cilia contributes to this diversity. It has been proposed that caps play a role in axoneme length control and stabilization, but their roles are still poorly understood. Here, we review the current knowledge on cilia structure diversity with a focus on the cilia distal domain and caps and discuss how they affect cilia structure and function.

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“…2b). A previous study divided the BF assembly of motile cilia into two regions, I and II 20,26 . For immature cells, we observed CNTRL in close proximity to ODF2 in the future BF region I.…”

Section: Resultsmentioning

confidence: 99%

“…For example, while outer dense fiber 2 (ODF2), which is an essential scaffold for initiating the assembly of basal feet/SDAs, appears near the centriolar wall along the transverse axis of both BF types, centriolin (CNTRL) appears near ODF2 in primary cilia but not in motile cilia. In motile cilia, CNTRL appears further away in the region where the BF tapers 20,25,26 . FGFR1 oncogene partner (FOP) is also localized to the basal feet/SDAs of primary cilia 27 , whereas its precise localization in the BB of motile cilia is unknown.…”

mentioning

confidence: 98%

The molecular dynamics of subdistal appendages in multi-ciliated cells

et al. 2021

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The motile cilia of ependymal cells coordinate their beats to facilitate a forceful and directed flow of cerebrospinal fluid (CSF). Each cilium originates from a basal body with a basal foot protruding from one side. A uniform alignment of these basal feet is crucial for the coordination of ciliary beating. The process by which the basal foot originates from subdistal appendages of the basal body, however, is unresolved. Here, we show FGFR1 Oncogene Partner (FOP) is a useful marker for delineating the transformation of a circular, unpolarized subdistal appendage into a polarized structure with a basal foot. Ankyrin repeat and SAM domain-containing protein 1A (ANKS1A) interacts with FOP to assemble region I of the basal foot. Importantly, disruption of ANKS1A reduces the size of region I. This produces an unstable basal foot, which disrupts rotational polarity and the coordinated beating of cilia in young adult mice. ANKS1A deficiency also leads to severe degeneration of the basal foot in aged mice and the detachment of cilia from their basal bodies. This role of ANKS1A in the polarization of the basal foot is evolutionarily conserved in vertebrates. Thus, ANKS1A regulates FOP to build and maintain the polarity of subdistal appendages.

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Super-resolution Molecular Map of Basal Foot Reveals Novel Cilium in Airway Multiciliated Cells

Cited by 4 publications

References 87 publications

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

Cilia Distal Domain: Diversity in Evolutionarily Conserved Structures

The molecular dynamics of subdistal appendages in multi-ciliated cells

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