CDC20B is required for deuterosome-mediated centriole production in multiciliated cells

Revinski, Diego R.; Zaragosi, Laure‐Emmanuelle; Boutin, Camille; Ruiz-Garcia, Sandra; Deprez, Marie; Thomé, Virginie; Rosnet, Olivier; Gay, Anne-Sophie; Mercey, Olivier; Paquet, Agnès; Pons, Nicolas; Ponzio, Gilles; Marcet, Brice; Kodjabachian, Laurent; Barbry, Pascal

doi:10.1038/s41467-018-06768-z

Cited by 65 publications

(57 citation statements)

References 57 publications

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“…Its formation requires cytoplasmic E2f4 . Fully assembled centrioles are eventually released from their “cradles” by APC/C‐activated proteolysis and mature into basal bodies .…”

Section: Introductionmentioning

confidence: 99%

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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“…Its formation requires cytoplasmic E2f4 . Fully assembled centrioles are eventually released from their “cradles” by APC/C‐activated proteolysis and mature into basal bodies .…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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“…In addition to this, a dedicated pathway exists in the MCCs for basal body generation. The vast majority of basal bodies are produced by this alternative mechanismthe deuterosome-dependent (DD) pathwayin which DEUP1, CCNO, CCDC78 and CDC20B are believed to be dedicated components (Funk et al, 2015;Klos Dehring et al, 2013;Revinski et al, 2018;Spassky and Meunier, 2017;Zhao et al, 2013). Here, electron-dense structures called deuterosomes are first generated by the oligomerization of the CEP63 paralog DEUP1.…”

Section: In Vitro Culture Of MCI Mutant Airway Cells Revealed a Stronmentioning

confidence: 99%

Mcidas mutant mice reveal a two-step process for the specification and differentiation of multiciliated cells in mammals

Anujan

Zhou

et al. 2019

Development

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Motile cilia on multiciliated cells (MCCs) function in fluid clearance over epithelia. Studies with Xenopus embryos and individuals with the congenital respiratory disorder reduced generation of multiple motile cilia (RGMC), have implicated the nuclear protein MCIDAS (MCI), in the transcriptional regulation of MCC specification and differentiation. Recently, a paralogous protein, geminin coiled-coil domain containing (GMNC), was also shown to be required for MCC formation. Surprisingly, in contrast to the presently held view, we find that Mci mutant mice can specify MCC precursors. However, these precursors cannot produce multiple basal bodies, and mature into single ciliated cells. We identify an essential role for MCI in inducing deuterosome pathway components for the production of multiple basal bodies. Moreover, GMNC and MCI associate differentially with the cell-cycle regulators E2F4 and E2F5, which enables them to activate distinct sets of target genes (ciliary transcription factor genes versus basal body amplification genes). Our data establish a previously unrecognized two-step model for MCC development: GMNC functions in the initial step for MCC precursor specification. GMNC induces Mci expression that drives the second step of basal body production for multiciliation.

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“…For example, Deup1 was recently identified as a deuterosome-specific protein that is essential for the formation of deuterosomes and, subsequently, centriole amplification (Zhao et al, 2013). Similarly, a number of deuterosome-enriched factors have since been shown to play key roles in deuterosome biogenesis and function (Klos Dehring et al, 2013; Mori et al, 2017; Revinski et al, 2018). These data support the theory that the PC-dependent and deuterosome-dependent centriole amplification pathways act in parallel, but use unique molecular components to produce all of the centrioles in a cell.…”

Section: Introductionmentioning

confidence: 99%

Regulation of cilia abundance in multiciliated cells

Nanjundappa

Kong

Shim

et al. 2019

eLife

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Multiciliated cells (MCC) contain hundreds of motile cilia used to propel fluid over their surface. To template these cilia, each MCC produces between 100-600 centrioles by a process termed centriole amplification. Yet, how MCC regulate the precise number of centrioles and cilia remains unknown. Airway progenitor cells contain two parental centrioles (PC) and form structures called deuterosomes that nucleate centrioles during amplification. Using an ex vivo airway culture model, we show that ablation of PC does not perturb deuterosome formation and centriole amplification. In contrast, loss of PC caused an increase in deuterosome and centriole abundance, highlighting the presence of a compensatory mechanism. Quantification of centriole abundance in vitro and in vivo identified a linear relationship between surface area and centriole number. By manipulating cell size, we discovered that centriole number scales with surface area. Our results demonstrate that a cell-intrinsic surface area-dependent mechanism controls centriole and cilia abundance in multiciliated cells.

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CDC20B is required for deuterosome-mediated centriole production in multiciliated cells

Cited by 65 publications

References 57 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

Mcidas mutant mice reveal a two-step process for the specification and differentiation of multiciliated cells in mammals

Regulation of cilia abundance in multiciliated cells

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