Calibrated mitotic oscillator drives motile ciliogenesis

Jord, Adel Al; Shihavuddin, Asm; d’Aout, Raphaël Servignat; Faucourt, Marion; Genovesio, Auguste; Karaı̈skou, Anthi; Sobczak-Thépot, Joëlle; Spassky, Nathalie; Meunier, Anne

doi:10.1126/science.aan8311

Cited by 85 publications

(110 citation statements)

References 43 publications

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“…This is interesting because in cycling cells the daughter centriole needs to go through mitosis to mature into the mother centriole, which possesses appendages and can serve as a basal body . Possibly, this unexpected centriole maturation is rendered by the recently reported mitosis‐like program in the differentiating mEPCs . In addition, the bottom region of these cilia was usually Centrin‐positive (Fig C) .…”

Section: Resultsmentioning

confidence: 76%

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

et al. 2019

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Mammalian epithelial cells use a pair of parental centrioles and numerous deuterosomes as platforms for efficient basal body production during multiciliogenesis. How deuterosomes form and function, however, remain controversial. They are proposed to arise either spontaneously for massive de novo centriole biogenesis or in a daughter centriole‐dependent manner as shuttles to carry away procentrioles assembled at the centriole. Here, we show that both parental centrioles are dispensable for deuterosome formation. In both mouse tracheal epithelial and ependymal cells (mTECs and mEPCs), discrete deuterosomes in the cytoplasm are initially procentriole‐free. They emerge at widely dispersed positions in the cytoplasm and then enlarge, concomitant with their increased ability to form procentrioles. More importantly, deuterosomes still form efficiently in mEPCs whose daughter centriole or even both parental centrioles are eliminated through shRNA‐mediated depletion or drug inhibition of Plk4, a kinase essential to centriole biogenesis in both cycling cells and multiciliated cells. Therefore, deuterosomes can be assembled autonomously to mediate de novo centriole amplification in multiciliated cells.

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Section: Resultsmentioning

confidence: 76%

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

et al. 2019

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“…Concurrent maturation of the young centrosomal centriole and the procentrioles is also seen in cycling cells and was shown to be Plk1 dependent 24 . Since Plk1 regulates the A-to G-transition in brain MCC progenitors 5 , it is tempting to speculate that it also drives the concurrent maturation of the two generations of centrioles in these differentiating cells. Interestingly, such maturation of the daughter centriole is also observed in MCC induced from primary fibroblasts 11 .…”

Section: Discussionmentioning

confidence: 99%

“…This amplification occurs through the formation of intermediate organelles, the deuterosomes, which are composed of centrosome-related elements 2,3 . Deuterosomes support massive centriole production within a molecular cascade that is shared with the cell cycle centrosome duplication program [3][4][5] . Because two centrosomal centrioles seemed insufficient to scaffold the formation of tens of centrioles, massive centriole production through deuterosome structures was proposed to arise independently from the centrosome in MCC 6 .…”

Section: Introductionmentioning

confidence: 99%

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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“…Having discovered a link between APC/C activity and centrosome stability, we investigated which APC/C substrate could account for the centrosome transport failure. Our prime candidate was Polo kinase (Plk1 in human): it is required for PCM recruitment to the centrioles (Prosser et al, 2012), is a known target of the APC/C in other organisms (Lindon and Pines, 2004), and in mammals is involved in the uncoupling of the centrosome cycle from the cell cycle during ciliogenesis (Al Jord et al, 2017). Furthermore, it was recently shown that Polo activity is crucial for centrosome stability in the Drosophila egg chamber (Pimenta-Marques et al, 2016).…”

Section: Polo Kinase Regulates Centrosome Stability and Transport Dowmentioning

confidence: 99%

APC/C-Vihar regulates centrosome activity and stability in theDrosophilagermline

Meghini

Villa-Fombuena

et al. 2017

Preprint

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Abstract:In metazoans, the centrioles/centrosomes of the female germline are eliminated prior to the end of oogenesis. Although this phenomenon is important for reproduction, the function of the centrosomes during oogenesis and the mechanism controlling their stability is still unclear. Here we demonstrate that the multi-subunit ubiquitin ligase, the Anaphase Promoting Complex/Cyclosome (APC/C), ensures normal germline development by regulating the activity and stability of centrosomes during early Drosophila oogenesis. We show that perturbing APC/C activity by altering the activity of its co-factor Vihar/Ube2c causes ectopic microtubule-nucleation activity of the centrosomes, resulting in a failure of oocyte specification and decreased female fertility.Altering APC/C regulation induces precocious destruction of the key centrosome regulator, Polo Kinase, which leads to destabilization of the centrosomes and blocks their migration into the oocyte. Our study highlights the critical importance of the spatiotemporal regulation of centrosomes by the proteolytic mechanism during metazoan oocyte development.

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Calibrated mitotic oscillator drives motile ciliogenesis

Cited by 85 publications

References 43 publications

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

Parental centrioles are dispensable for deuterosome formation and function during basal body amplification

Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

APC/C-Vihar regulates centrosome activity and stability in theDrosophilagermline

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