scholarly journals Re-examining the role of Drosophila Sas-4 in centrosome assembly using two-colour-3D-SIM FRAP

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Paul T Conduit ◽  
Alan Wainman ◽  
Zsofia A Novak ◽  
Timothy T Weil ◽  
Jordan W Raff
Keyword(s):  
Mother And Daughter ◽  
Mother Centriole ◽  
Pericentriolar Material ◽  
Daughter Centriole

Centrosomes have many important functions and comprise a ‘mother’ and ‘daughter’ centriole surrounded by pericentriolar material (PCM). The mother centriole recruits and organises the PCM and templates the formation of the daughter centriole. It has been reported that several important Drosophila PCM-organising proteins are recruited to centrioles from the cytosol as part of large cytoplasmic ‘S-CAP’ complexes that contain the centriole protein Sas-4. In a previous paper (<xref ref-type="bibr" rid="bib5">Conduit et al., 2014b</xref>) we showed that one of these proteins, Cnn, and another key PCM-organising protein, Spd-2, are recruited around the mother centriole before spreading outwards to form a scaffold that supports mitotic PCM assembly; the recruitment of Cnn and Spd-2 is dependent on another S-CAP protein, Asl. We show here, however, that Cnn, Spd-2 and Asl are not recruited to the mother centriole as part of a complex with Sas-4. Thus, PCM recruitment in fly embryos does not appear to require cytosolic S-CAP complexes.

scholarly journals A centriole's subdistal appendages: contributions to cell division, ciliogenesis and differentiation

Open Biology ◽  
2021 ◽  
Vol 11 (2) ◽  
pp. 200399
Author(s):  
Nicole A. Hall ◽  
Heidi Hehnly
Keyword(s):  
Cell Division ◽  
Cell Differentiation ◽  
Final Stage ◽  
Eukaryotic Species ◽  
Chromosome Alignment ◽  
Cilia Formation ◽  
Mother Centriole ◽  
Pericentriolar Material ◽  
Daughter Centriole

The centrosome is a highly conserved structure composed of two centrioles surrounded by pericentriolar material. The mother, and inherently older, centriole has distal and subdistal appendages, whereas the daughter centriole is devoid of these appendage structures. Both appendages have been primarily linked to functions in cilia formation. However, subdistal appendages present with a variety of potential functions that include spindle placement, chromosome alignment, the final stage of cell division (abscission) and potentially cell differentiation. Subdistal appendages are particularly interesting in that they do not always display a conserved ninefold symmetry in appendage organization on the mother centriole across eukaryotic species, unlike distal appendages. In this review, we aim to differentiate both the morphology and role of the distal and subdistal appendages, with a particular focus on subdistal appendages.

scholarly journals Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Olivier Mercey ◽  
Adel Al Jord ◽  
Philippe Rostaing ◽  
Alexia Mahuzier ◽  
Aurélien Fortoul ◽  
...  
Keyword(s):  
Additional Data ◽  
De Novo ◽  
Fluid Flows ◽  
Structural Defects ◽  
Centrosome Duplication ◽  
Focal Region ◽  
Mother Centriole ◽  
Pericentriolar Material ◽  
Daughter Centriole

Abstract Reproductive and respiratory organs, along with brain ventricles, are lined by multiciliated epithelial cells (MCC) that generate cilia-powered fluid flows. MCC hijack the centrosome duplication pathway to form hundreds of centrioles and nucleate motile cilia. In these cells, the large majority of procentrioles are formed associated with partially characterized organelles called deuterosomes. We recently challenged the paradigm that deuterosomes and procentrioles are formed de novo by providing data, in brain MCC, suggesting that they are nucleated from the pre-existing centrosomal younger centriole. However, the origin of deuterosomes and procentrioles is still under debate. Here, we further question centrosome importance for deuterosome and centriole amplification. First, we provide additional data confirming that centriole amplification occurs sequentially from the centrosomal region, and that the first procentriole-loaded deuterosomes are associated with the daughter centriole or in the centrosomal centriole vicinity. Then, to further test the requirement of the centrosome in deuterosome and centriole formation, we depleted centrosomal centrioles using a Plk4 inhibitor. We reveal unexpected limited consequences in deuterosome/centriole number in absence of centrosomal centrioles. Notably, in absence of the daughter centriole only, deuterosomes are not seen associated with the mother centriole. In absence of both centrosomal centrioles, procentrioles are still amplified sequentially and with no apparent structural defects. They seem to arise from a focal region, characterized by microtubule convergence and pericentriolar material (PCM) assembly. The relevance of deuterosome association with the daughter centriole as well as the role of the PCM in the focal and sequential genesis of centrioles in absence of centrosomal centrioles are discussed.

scholarly journals α-/γ-Taxilin are required for centriolar subdistal appendage assembly and microtubule organization

2021 ◽  
Author(s):  
Dandan Ma ◽  
Rongyi Wang ◽  
Fulin Wang ◽  
Zhiquan Chen ◽  
Ning Huang ◽  
...  
Keyword(s):  
Coiled Coil ◽  
Animal Cells ◽  
Microtubule Organization ◽  
Hierarchical Assembly ◽  
Mother And Daughter ◽  
Mother Centriole ◽  
Functional Understanding ◽  
Pericentriolar Material ◽  
Functional Analyses ◽  
Molecular Components

AbstractThe centrosome, composed of a pair of centrioles (mother and daughter centrioles) and pericentriolar material, is mainly responsible for microtubule nucleation and anchorage in animal cells. The subdistal appendage (SDA) is a centriolar structure located at the subdistal region on the mother centriole, and it functions in microtubule anchorage. However, the molecular composition and detailed structure of SDA remain largely unknown. Here, we identified a-taxilin and r-taxilin as new SDA components, which form a complex via their coiled-coil domains and serve as a new subgroup during SDA hierarchical assembly. Their SDA localization is dependent on ODF2, and α-taxilin recruits CEP170 to the SDA. Functional analyses suggest that α-taxilin and γ-taxilin are responsible for centrosomal microtubule anchorage during interphase, as well as for proper spindle orientation during metaphase. Altogether, our results shed light on the molecular components and functional understanding of the SDA hierarchical assembly and microtubule organization.

scholarly journals Dynamics of centriole amplification in centrosome-depleted brain multiciliated progenitors

2018 ◽  
Author(s):  
Olivier Mercey ◽  
Adel Al Jord ◽  
Philippe Rostaing ◽  
Alexia Mahuzier ◽  
Aurélien Fortoul ◽  
...  
Keyword(s):  
Cell Cycle ◽  
Self Assembly ◽  
De Novo ◽  
Focal Region ◽  
Multiciliated Cells ◽  
Pericentriolar Material ◽  
Cell Type Specific ◽  
The Relationship ◽  
Daughter Centriole

AbstractCentrioles 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 pre-existing 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. Interestingly, in absence of centrosomal centrioles, procentrioles are still amplified sequentially from a single focal region, characterized by microtubule convergence and pericentriolar material (PCM) self-assembly. The relevance of deuterosome association with the daughter centriole as well as the role of the PCM in the focal and sequential genesis of centrioles in absence of centrosomal centrioles are discussed.

scholarly journals The daughter centriole controls ciliogenesis by regulating Neurl-4 localization at the centrosome

2017 ◽  
Vol 216 (5) ◽  
pp. 1287-1300 ◽  
Author(s):  
Abdelhalim Loukil ◽  
Kati Tormanen ◽  
Christine Sütterlin
Keyword(s):  
Ubiquitin Ligase ◽  
Data Support ◽  
Multiciliated Cells ◽  
Mother Centriole ◽  
And Function ◽  
Dependent Processes ◽  
Daughter Centriole ◽  
In Cells

The two centrioles of the centrosome differ in age and function. Although the mother centriole mediates most centrosome-dependent processes, the role of the daughter remains poorly understood. A recent study has implicated the daughter centriole in centriole amplification in multiciliated cells, but its contribution to primary ciliogenesis is unclear. We found that manipulations that prevent daughter centriole formation or induce its separation from the mother abolish ciliogenesis. This defect was caused by stabilization of the negative ciliogenesis regulator CP110 and was corrected by CP110 depletion. CP110 dysregulation may be caused by effects on Neurl-4, a daughter centriole–associated ubiquitin ligase cofactor, which was required for ciliogenesis. Centrosome-targeted Neurl-4 was sufficient to restore ciliogenesis in cells with manipulated daughter centrioles. Interestingly, early during ciliogenesis, Neurl-4 transiently associated with the mother centriole in a process that required mother–daughter centriole proximity. Our data support a model in which the daughter centriole promotes ciliogenesis through Neurl-4–dependent regulation of CP110 levels at the mother centriole.

scholarly journals PLK4-phosphorylated NEDD1 facilitates cartwheel assembly and centriole biogenesis initiations

2020 ◽  
Vol 220 (1) ◽  
Author(s):  
Wangfei Chi ◽  
Gang Wang ◽  
Guangwei Xin ◽  
Qing Jiang ◽  
Chuanmao Zhang
Keyword(s):  
Cell Cycle ◽  
Amino Acid ◽  
Amino Acid Residue ◽  
Centrosome Duplication ◽  
Spatiotemporal Regulation ◽  
Mother Centriole ◽  
Pericentriolar Material ◽  
Daughter Centriole

Centrosome duplication occurs under strict spatiotemporal regulation once per cell cycle, and it begins with cartwheel assembly and daughter centriole biogenesis at the lateral sites of the mother centrioles. However, although much of this process is understood, how centrosome duplication is initiated remains unclear. Here, we show that cartwheel assembly followed by daughter centriole biogenesis is initiated on the NEDD1-containing layer of the pericentriolar material (PCM) by the recruitment of SAS-6 to the mother centriole under the regulation of PLK4. We found that PLK4-mediated phosphorylation of NEDD1 at its S325 amino acid residue directly promotes both NEDD1 binding to SAS-6 and recruiting SAS-6 to the centrosome. Overexpression of phosphomimicking NEDD1 mutant S325E promoted cartwheel assembly and daughter centriole biogenesis initiations, whereas overexpression of nonphosphorylatable NEDD1 mutant S325A abolished the initiations. Collectively, our results demonstrate that PLK4-regulated NEDD1 facilitates initiation of the cartwheel assembly and of daughter centriole biogenesis in mammals.

scholarly journals Daughter centrioles assemble preferentially towards the nuclear envelope in Drosophila syncytial embryos

2021 ◽  
Author(s):  
Neil Henry James Cunningham ◽  
Imene Bouhlel ◽  
Paul Thomas Conduit
Keyword(s):  
Nuclear Envelope ◽  
Single Mother ◽  
S Phase ◽  
Animal Cells ◽  
Simultaneous Formation ◽  
Centriole Duplication ◽  
External Cues ◽  
Mother Centriole ◽  
Pericentriolar Material ◽  
Daughter Centriole

Centrosomes are important organisers of microtubules within animal cells. They comprise a pair of centrioles surrounded by the pericentriolar material (PCM), which nucleates and organises the microtubules. To maintain centrosome numbers, centrioles must duplicate once and only once per cell cycle. During S-phase, a single new daughter centriole is built orthogonally on one side of each radially symmetric mother centriole. Mis-regulation of duplication can result in the simultaneous formation of multiple daughter centrioles around a single mother centriole, leading to centrosome amplification, a hallmark of cancer. It remains unclear how a single duplication site is established. It also remains unknown whether this site is pre-defined or randomly positioned around the mother centriole. Here, we show that within Drosophila syncytial embryos daughter centrioles preferentially assemble on the side of the mother facing the nuclear envelope, to which the centrosomes are closely attached. This positional preference is established early during duplication and remains stable throughout daughter centriole assembly, but is lost in centrosomes forced to lose their connection to the nuclear envelope. This shows that non-centrosomal cues influence centriole duplication and raises the possibility that these external cues could help establish a single duplication site.

Centrosome Fine Ultrastructure of the Osteocyte Mechanosensitive Primary Cilium

2012 ◽  
Vol 18 (6) ◽  
pp. 1430-1441 ◽  
Author(s):  
R.E. Uzbekov ◽  
D.B. Maurel ◽  
P.C. Aveline ◽  
S. Pallu ◽  
C.L. Benhamou ◽  
...  
Keyword(s):  
Primary Cilium ◽  
Ultrastructural Level ◽  
Mutual Orientation ◽  
Positive Staining ◽  
Microtubule Organization ◽  
Alpha Tubulin ◽  
Transmission Electron ◽  
Mother And Daughter ◽  
Mother Centriole ◽  
Daughter Centriole

AbstractThe centrosome is the principal microtubule organization center in cells, giving rise to microtubule-based organelles (e.g., cilia, flagella). The aim was to study the osteocyte centrosome morphology at an ultrastructural level in relation to its mechanosensitive function. Osteocyte centrosomes and cilia in tibial cortical bone were explored by acetylated alpha-tubulin (AαTub) immunostaining under confocal microscopy. For the first time, fine ultrastructure and spatial orientation of the osteocyte centrosome were explored by transmission electron microscopy on serial ultrathin sections. AαTub-positive staining was observed in 94% of the osteocytes examined (222/236). The mother centriole formed a short primary cilium and was longer than the daughter centriole due to an intermediate zone between centriole and cilium. The proximal end of the mother centriole was connected with the surface of daughter centriole by striated rootlets. The mother centriole exhibited distal appendages that interacted with the cell membrane and formed a particular structure called “cilium membrane prolongation.” The primary cilium was mainly oriented perpendicular to the long axis of bone. Mother and daughter centrioles change their original mutual orientation during the osteocyte differentiation process. The short primary cilium is hypothesized as a novel type of fluid-sensing organelle in osteocytes.

scholarly journals Distinct mechanisms eliminate mother and daughter centrioles in meiosis of starfish oocytes

2016 ◽  
Vol 212 (7) ◽  
pp. 815-827 ◽  
Author(s):  
Joana Borrego-Pinto ◽  
Kálmán Somogyi ◽  
Matthia A. Karreman ◽  
Julia König ◽  
Thomas Müller-Reichert ◽  
...  
Keyword(s):  
Meiotic Spindle ◽  
Female Meiosis ◽  
Elimination Process ◽  
Fluorescent Markers ◽  
Polar Bodies ◽  
Embryonic Cleavage ◽  
Mother And Daughter ◽  
Mother Centriole ◽  
Dual Mechanism ◽  
Daughter Centriole

Centriole elimination is an essential process that occurs in female meiosis of metazoa to reset centriole number in the zygote at fertilization. How centrioles are eliminated remains poorly understood. Here we visualize the entire elimination process live in starfish oocytes. Using specific fluorescent markers, we demonstrate that the two older, mother centrioles are selectively removed from the oocyte by extrusion into polar bodies. We show that this requires specific positioning of the second meiotic spindle, achieved by dynein-driven transport, and anchorage of the mother centriole to the plasma membrane via mother-specific appendages. In contrast, the single daughter centriole remaining in the egg is eliminated before the first embryonic cleavage. We demonstrate that these distinct elimination mechanisms are necessary because if mother centrioles are artificially retained, they cannot be inactivated, resulting in multipolar zygotic spindles. Thus, our findings reveal a dual mechanism to eliminate centrioles: mothers are physically removed, whereas daughters are eliminated in the cytoplasm, preparing the egg for fertilization.

CEP110 and ninein are located in a specific domain of the centrosome associated with centrosome maturation

2002 ◽  
Vol 115 (9) ◽  
pp. 1825-1835 ◽  
Author(s):  
Young Y. Ou ◽  
Gary J. Mack ◽  
Meifeng Zhang ◽  
Jerome B. Rattner
Keyword(s):  
Cell Cycle ◽  
Protein Interactions ◽  
Protein Function ◽  
Similar Distribution ◽  
Microtubule Organizing Center ◽  
Specific Domain ◽  
The Reformation ◽  
Mother And Daughter ◽  
Organizing Center ◽  
Pericentriolar Material

The mammalian centrosome consists of a pair of centrioles surrounded by pericentriolar material (PCM). The architecture and composition of the centrosome, especially the PCM, changes during the cell cycle. Recently, a subset of PCM proteins have been shown to be arranged in a tubular conformation with an open and a closed end within the centrosome. The presence of such a specific configuration can be used as a landmark for mapping proteins in both a spatial and a temporal fashion. Such mapping studies can provide information about centrosome organization, protein dynamics,protein-protein interactions as well as protein function. In this study, the centrosomal proteins CEP110 and ninein were mapped in relationship to the tubular configuration. Both proteins were found to exhibit a similar distribution pattern. In the mother centrosome, they were found at both ends of the centrosome tube, including the site of centrosome duplication. However,in the daughter centrosome they were present only at the closed end. At the closed end of the mother and daughter centrosome tube, both CEP110 and ninein co-localized with the centriolar protein CEP250/c-Nap1, which confirms ninein's centriole association and places CEP110 in association with this structure. Importantly, the appearance of CEP110 and ninein at the open end of the daughter centrosome occurred during the telophase-G1 transition of the next cell cycle, concomitant with the maturation of the daughter centrosome into a mother centrosome. Microinjection of antibodies against either CEP110 or ninein into metaphase HeLa cells disrupted the reformation of the tubular conformation of proteins within the centrosome following cell division and consequently led to dispersal of centrosomal material throughout the cytosol. Further, microinjection of antibodies to either CEP110 or ninein into metaphase PtK2 cells not only disrupted the tubular configuration within the centrosome but also affected the centrosome's ability to function as a microtubule organizing center (MTOC). This MTOC function was also disrupted when the antibodies were injected into postmitotic cells. Taken together, our results indicate that: (1) a population of CEP110 and ninein is located in a specific domain within the centrosome, which corresponds to the open end of the centrosome tube and is the site of protein addition associated with maturation of a daughter centrosome into a mother centrosome; and (2) the addition of CEP110 and ninein are essential for the reformation of specific aspects of the interphase centrosome architecture following mitosis as well as being required for the centrosome to function as a MTOC.

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