Massive centriole production can occur in the absence of deuterosomes in multiciliated cells

Mercey, Olivier; Levine, Marshall; LoMastro, Gina M.; Rostaing, Philippe; Brotslaw, Eva; Gomez, Valerie; Kumar, Abhijay; Spassky, Nathalie; Mitchell, Brian J.; Meunier, Anne; Holland, Andrew J.

doi:10.1038/s41556-019-0427-x

Cited by 47 publications

(54 citation statements)

References 48 publications

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“…Mature OSNs had a mean centriole number of 15.7, with as many as 37 observed in a single cell, whereas the rosettes that we observed in the olfactory epithelium and in cultured cells overexpressing Plk4 had no more than eight centrioles, suggesting that this simple model cannot account for the total number. It is possible to form rosettes with more centrioles, similar to what has been observed in multiciliated cells lacking deuterosomes [10]. We did not observe such cases in olfactory epithelium, but we cannot rule out that it occurs.…”

Section: Discussionsupporting

confidence: 51%

Centrioles are amplified in cycling progenitors of olfactory sensory neurons

Ching¹,

Stearns²

2020

PLoS Biol

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Olfaction in most animals is mediated by neurons bearing cilia that are accessible to the environment. Olfactory sensory neurons (OSNs) in chordates usually have multiple cilia, each with a centriole at its base. OSNs differentiate from stem cells in the olfactory epithelium, and how the epithelium generates cells with many centrioles is not yet understood. We show that centrioles are amplified via centriole rosette formation in both embryonic development and turnover of the olfactory epithelium in adult mice, and rosette-bearing cells often have free centrioles in addition. Cells with amplified centrioles can go on to divide, with centrioles clustered at each pole. Additionally, we found that centrioles are amplified in immediate neuronal precursors (INPs) concomitant with elevation of mRNA for polo-like kinase 4 (Plk4) and SCL/Tal1-interrupting locus gene (Stil), key regulators of centriole duplication. These results support a model in which centriole amplification occurs during a transient state characterized by elevated Plk4 and Stil in early INP cells. These cells then go on to divide at least once to become OSNs, demonstrating that cell division with amplified centrioles, known to be tolerated in disease states, can occur as part of a normal developmental program.

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Section: Discussionsupporting

confidence: 51%

Centrioles are amplified in cycling progenitors of olfactory sensory neurons

Ching¹,

Stearns²

2020

PLoS Biol

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“…In D. melanogaster cultured cells, co-depletion of the centriolar protein Ana2 and the PCM component D-Pericentrin–like protein (D-Plp) additively impair centriole biogenesis, indicating that two alternative pathways – a centriolar and a PCM-mediated – may be at play (Ito et al, 2019). Moreover, in mouse ependymal cells without centrioles and specialised electron-dense deuterosomes that can feed centriole assembly, a correct number of centrioles can form de novo within Pericentrin rich areas (Mercey et al, 2019b). To test the role of the PCM in de novo centriole assembly, we started by performing perturbation experiments in Drosophila DMEL cultured cells, since it is easier to knock down several genes in vitro than in the organism.…”

Section: Resultsmentioning

confidence: 99%

“…For instance, MTs likely participate to the localisation of some components at the centrosome through molecular motor based transport. Furthermore, the PCM was shown to be important for canonical centriole biogenesis (Dammermann et al, 2004; Pelletier et al, 2004; Kemp et al, 2004; Delattre et al, 2006; Kleylein-Sohn et al, 2007) and recent studies in multicilliated cells propose that, in the absence of centrioles or specialised deuterosomes, centrioles can form within PCM clouds (Mercey et al, 2019b). De novo centriole biogenesis has been described to occur within Pericentrin and Gamma-tubulin-rich foci in vertebrate somatic cells (Khodjakov et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

“…Centrioles can also form de novo in a variety of cell-types (reviewed in (Nabais et al, 2018)), but the regulation of this process remains largely unknown. De novo centriole assembly occurs naturally in organisms that lack centrosomes and generate centrioles to nucleate motile cilia, such as land plants that produce ciliated sperm (Renzaglia and Garbary, 2001), several unicellular organisms that alternate between non-flagellated and flagellated life-cycle states and in animal multiciliated cells, where many centrioles are produced at once (Dingle and Fulton, 1966; Aldrich, 1967; Fulton and Dingle, 1971; Grimes, 1973a; b; Mir et al, 1984; Al Jord et al, 2014; Meunier and Azimzadeh, 2016; Fritz-Laylin et al, 2016; Mercey et al, 2019a; b; Zhao et al, 2019) Furthermore, centrosomes form de novo in parthenogenetic insects that develop without fertilisation (Riparbelli et al, 1998; Tram and Sullivan, 2000; Riparbelli and Callaini, 2003). In most animals, centrioles are lost during female oogenesis and are provided by the sperm upon fertilisation, as they are needed for embryo development (Rodrigues-martins et al, 2008; Varmark et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

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Plk4 triggers autonomous de novo centriole biogenesis and maturation

Nabais

Pessoa

de-Carvalho

et al. 2020

Preprint

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23Centrioles form centrosomes and cilia. In most proliferating cells, centrioles assemble 24 through canonical duplication, which is spatially, temporally and numerically regulated 25 by the cell cycle and the presence of mature centrioles. However, in certain cell-types, 26 centrioles assemble de novo, yet by poorly understood mechanisms. Here, we 27 established a controlled system to investigate de novo centriole biogenesis, using 28Drosophila melanogaster egg explants overexpressing Polo-like kinase 4 (Plk4), a 29 trigger for centriole biogenesis. At high Plk4 concentration, centrioles form de novo, 30 mature and duplicate, independently of cell cycle progression and of the presence of 31 other centrioles. We show that Plk4 concentration determines the kinetics of centriole 32 assembly. Moreover, our results suggest Plk4 operates in a switch-like manner to control 33

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“…This suggests that a process of de novo assembly like that observed in parthenogenetic eggs could operate in Mastotermes spermatids. However, it has recently been shown show that deuterosomes are dispensable for centriole amplification during multiciliogenesis of some mouse and Xenopus cell types where a high number of procentrioles is formed in the vicinity of the parent centrioles [135]. Since orthogonally oriented centrioles are also found in Mastotermes spermatids it is possible that a such mechanism of rapid duplication could operate in this system to enable the assembly of many centrioles without the presence of deuterosomes.…”

Section: Centriole Overduplication In Insects: Breaking the Rulesmentioning

confidence: 99%

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

Riparbelli

Persico

Dallai

et al. 2020

Cells

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Centrioles are-widely conserved barrel-shaped organelles present in most organisms. They are indirectly involved in the organization of the cytoplasmic microtubules both in interphase and during the cell division by recruiting the molecules needed for microtubule nucleation. Moreover, the centrioles are required to assemble cilia and flagella by the direct elongation of their microtubule wall. Due to the importance of the cytoplasmic microtubules in several aspects of the cell life, any defect in centriole structure can lead to cell abnormalities that in humans may result in significant diseases. Many aspects of the centriole dynamics and function have been clarified in the last years, but little attention has been paid to the exceptions in centriole structure that occasionally appeared within the animal kingdom. Here, we focused our attention on non-canonical aspects of centriole architecture within the Hexapoda. The Hexapoda is one of the major animal groups and represents a good laboratory in which to examine the evolution and the organization of the centrioles. Although these findings represent obvious exceptions to the established rules of centriole organization, they may contribute to advance our understanding of the formation and the function of these organelles.Thus, the increase of g-tubulin leads to an increase in the nucleation of both astral and spindle microtubules, which drive the assembly of a functional spindle.At the heart of the centrosome there is a pair of centrioles, two microtubule-based barrel-shaped organelles of defined length and diameter [29], that warrants the integrity and the supramolecular organization of the centrosome itself. The coiled-coil proteins, pericentrin-like protein (PLP) and Cep152/Asterless form the scaffold for the matrix proteins Cep192/Spd-2, Cep215/Cnn and g-tubulin.It was observed PLP's C termini are located close to the centriole wall [26].In addition, to be the reference point for the organization of the centrosomal material, the centrioles may also act as templates for the axoneme assembly in cilia and flagella, that are involved in signalling and motility [30]. Therefore, the proper organization and dynamics of the centrioles are mandatory to ensure healthy cell life. Structural anomalies of the centrioles are found in several human cancers [31][32][33][34][35][36] and can be the cause of a spectrum of pathologies spanning from infertility to ciliopathies [37,38].Since, the centrioles impact upon several aspects of cell development and physiology, their structure and function have been studied over the years. However, this analysis was mainly addressed to examine centrioles in a few model organisms, such as Chlamydomonas reinhardtii, Caenorhabditis elegans, Drosophila melanogaster, and some vertebrate cell lines. From these studies emerge a highly conserved organization of the centrioles. However, investigations in different animal groups revealed distinct and sometimes important differences in the architecture of the centrioles [39,40]. Therefore, the analysi...

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Massive centriole production can occur in the absence of deuterosomes in multiciliated cells

Cited by 47 publications

References 48 publications

Centrioles are amplified in cycling progenitors of olfactory sensory neurons

Centrioles are amplified in cycling progenitors of olfactory sensory neurons

Plk4 triggers autonomous de novo centriole biogenesis and maturation

Centrioles and Ciliary Structures during Male Gametogenesis in Hexapoda: Discovery of New Models

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