The Rise of the Cartwheel: Seeding the Centriole Organelle

Guichard, Paul; Hamel, Virginie; Gönczy, Pierre

doi:10.1002/bies.201700241

Cited by 55 publications

(55 citation statements)

References 66 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Despite considerable variation across species and tissues, within any given tissue their size is essentially constant [1,2]. While the diameter of the centriole cylinder is set by the dimensions of the inner scaffolding structure of the cartwheel [3], how centriole length is set so precisely and stably maintained over many cell divisions is not well understood. Cep97 and CP110 are conserved proteins that localize to the distal end of centrioles and have been reported to limit centriole elongation in vertebrates [4,5].…”

mentioning

confidence: 99%

Cep97 Is Required For Centriole Structural Integrity And Cilia Formation In Drosophila

Dobbelaere

Černohorská

Huranová

et al. 2019

Preprint

View full text Add to dashboard Cite

Centrioles are highly elaborate microtubule-based structures responsible for the formation of centrosomes and cilia. Despite considerable variation across species and tissues, within any given tissue their size is essentially constant [1,2]. While the diameter of the centriole cylinder is set by the dimensions of the inner scaffolding structure of the cartwheel [3], how centriole length is set so precisely and stably maintained over many cell divisions is not well understood. Cep97 and CP110 are conserved proteins that localize to the distal end of centrioles and have been reported to limit centriole elongation in vertebrates [4,5]. Here, we examine Cep97 function in Drosophila melanogaster. We show that Cep97 is essential for formation of full-length centrioles in multiple tissues of the fly. We further identify the microtubule deacetylase Sirt2 as a Cep97 proximity interactor. Deletion of Sirt2 likewise affects centriole size. Interestingly, so does deletion of the acetylase Atat1, indicating that loss of stabilizing acetyl marks impairs centriole integrity. Cep97 and CP110 were originally identified as inhibitors of cilia formation in vertebrate cultured cells [6] and loss of CP110 is a widely used marker of basal body maturation. In contrast, in Drosophila Cep97 is only transiently removed from basal bodies and loss of Cep97 strongly impairs ciliogenesis.Collectively, our results support a model whereby Cep97 functions as part of a protective cap that acts together with the microtubule acetylation machinery to maintain centriole stability, essential for proper function in cilium biogenesis. Dobbelaere et al., page 3 RESULTS AND DISCUSSIONCentrioles generally assemble adjacent to pre-existing parental centrioles in a series of steps which have been extensively studied in a range of experimental models. First, PLK4/Sak/ZYG-1 is recruited to the vicinity of the mother centriole where it concentrates into a single focus that marks the site of daughter centriole assembly. PLK4 then recruits and phosphorylates STIL/Ana2/SAS-5 as well as SAS-6, which oligomerizes to form the huband-spoke structure of the cartwheel. Finally, CPAP/SAS-4 along with g-tubulin directs the assembly of the microtubule-based centriole wall, aided in some species by CEP135/Bld10[7]. Overexpression of CPAP as well as its interacting proteins CEP120 and SPICE1 is known to result in over-elongation of centrioles [4,5,[8][9][10] and recent studies have demonstrated that CPAP plays a key role in imparting slow, processive growth on centriolar microtubules [11,12]. The distal (plus) ends of centriolar microtubules are bound by a complex of Cep97 and CP110 [6,13,14]. In vertebrates, this complex is thought to counteract CPAP activity, as loss of either component results in over-elongated centrioles, while overexpression of CP110 can suppress the effect of excess CPAP [4,5]. Cep97 and CP110 have been shown to interact with the depolymerizing kinesin KIF24, which specifically acts on centriolar, but not cytoplasmic microtubules to limit centriole...

show abstract

mentioning

confidence: 99%

Cep97 Is Required For Centriole Structural Integrity And Cilia Formation In Drosophila

Dobbelaere

Černohorská

Huranová

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…Now, breakthroughs in understanding the nature and dynamism of the core protein components of both centrosomes and centrioles (Jana et al, 2014), and the realization that their assembly is tightly regulated and orchestrated provide the tools to address inheritance. With considerable simplification, centrioles assemble upon a SAS-6 cartwheel (Guichard et al, 2018), upon which the other components of the 9-triplet structures assemble and onto which centrosomal PCM later concentrates (Kollman et al, 2015). In consequence, the question as to whether centrosomes and centrioles are inherited, strictly speaking, may need to be examined more stringently.…”

Section: Discussionmentioning

confidence: 99%

Separation and Loss of Centrioles From Primordidal Germ Cells to Mature Oocytes in the Mouse

Schatten

Simerly

Manil-Ségalen

et al. 2018

Preprint

View full text Add to dashboard Cite

Abstract.Oocytes, including those from mammals, lack centrioles, but neither the mechanism by which mature eggs lose their centrioles nor the exact stage at which centrioles are destroyed during oogenesis is known. To answer questions raised by centriole disappearance during oogenesis, using a transgenic mouse expressing GFP-centrin-2 (GFP CETN2), we traced their presence from e11.5 primordial germ cells (PGCs) through oogenesis and their ultimate dissolution in mature oocytes. We show tightly coupled CETN2 doublets in PGCs, oogonia, and pre-pubertal oocytes. Beginning with follicular recruitment of incompetent germinal vesicle (GV) oocytes, through full oocyte maturation, the CETN2 doublets separate within the pericentriolar material (PCM); concomitantly, a rise in single CETN2 pairs is identified. CETN2 dissolution accelerates following meiosis resumption. Remarkably, a single CETN2 pair is retained in the PCM of most meiotic metaphase-I and -II spindle poles. Partial dissolution of the CETN2 foci occurs even as other centriole markers, like Cep135, a protein necessary for centriole duplication, are maintained at the PCM. Furthermore, live imaging demonstrates that the link between the two centrioles breaks as meiosis resumes and that centriole association with the PCM is progressively lost.Microtubule inhibition shows that centriole dissolution is uncoupled from microtubule dynamics. Thus, centriole doublets, present in early G2-arrested meiotic prophase oocytes, begin partial reduction during follicular recruitment and meiotic resumption, much later than previously thought.All rights reserved. No reuse allowed without permission.was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

show abstract

“…The coiled-coil region determines the dimerization of Sas6 monomers into homodimers that form the radial spokes, whereas the head domain mediates the interaction between Sas6 homodimers forming the central hub. This arrangement leads to the assembly of Sas6 into a nine-fold symmetric cartwheel [103][104][105][106][107][108]. Ultrastructural analysis of the male gametogenesis in Sciara, that also displays a giant axoneme consisting of a spiral of about 70 doublet microtubules, reveals the presence in primary and secondary spermatocytes of extraordinarily large centrioles consisting up to 70 doublet microtubules [101].…”

Section: Centrioles In Hexapoda: Common and Uncommon Modelsmentioning

confidence: 99%

Section: Centrioles In Hexapoda: Common and Uncommon Modelsmentioning

confidence: 99%

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

Riparbelli

Persico

Dallai

et al. 2020

Cells

View full text Add to dashboard Cite

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...

show abstract

The Rise of the Cartwheel: Seeding the Centriole Organelle

Cited by 55 publications

References 66 publications

Cep97 Is Required For Centriole Structural Integrity And Cilia Formation In Drosophila

Cep97 Is Required For Centriole Structural Integrity And Cilia Formation In Drosophila

Separation and Loss of Centrioles From Primordidal Germ Cells to Mature Oocytes in the Mouse

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

Contact Info

Product

Resources

About