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 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 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 The microtubule affinity regulating kinase MARK4 promotes axoneme extension during early ciliogenesis

2013 ◽  
Vol 200 (4) ◽  
pp. 505-522 ◽  
Author(s):  
Stefanie Kuhns ◽  
Kerstin N. Schmidt ◽  
Jürgen Reymann ◽  
Daniel F. Gilbert ◽  
Annett Neuner ◽  
...  
Keyword(s):  
Rna Interference ◽  
Protein Kinases ◽  
Basal Body ◽  
Kinase Activity ◽  
Complete Removal ◽  
Cilia Formation ◽  
Mother Centriole ◽  
Functional Analyses ◽  
Novel Protein

Despite the critical contributions of cilia to embryonic development and human health, key regulators of cilia formation await identification. In this paper, a functional RNA interference–based screen linked 30 novel protein kinases with ciliogenesis. Of them, we have studied the role of the microtubule (MT)-associated protein/MT affinity regulating kinase 4 (MARK4) in depth. MARK4 associated with the basal body and ciliary axoneme in human and murine cell lines. Ultrastructural and functional analyses established that MARK4 kinase activity was required for initiation of axoneme extension. We identified the mother centriolar protein ODF2 as an interaction partner of MARK4 and showed that ODF2 localization to the centriole partially depended on MARK4. Our data indicated that, upon MARK4 or ODF2 knockdown, the ciliary program arrested before the complete removal of the CP110–Cep97 inhibitory complex from the mother centriole, suggesting that these proteins act at this level of axonemal extension. We propose that MARK4 is a critical positive regulator of early steps in ciliogenesis.

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 pseudo GTPase CENP-M drives human kinetochore assembly

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Federica Basilico ◽  
Stefano Maffini ◽  
John R Weir ◽  
Daniel Prumbaum ◽  
Ana M Rojas ◽  
...  
Keyword(s):  
Cell Division ◽  
Small Gtpases ◽  
Conformational Switching ◽  
Point Mutant ◽  
Kinetochore Assembly ◽  
Gtp Binding ◽  
Chromosome Alignment ◽  
Spindle Microtubules ◽  
And Function

Kinetochores, multi-subunit complexes that assemble at the interface with centromeres, bind spindle microtubules to ensure faithful delivery of chromosomes during cell division. The configuration and function of the kinetochore–centromere interface is poorly understood. We report that a protein at this interface, CENP-M, is structurally and evolutionarily related to small GTPases but is incapable of GTP-binding and conformational switching. We show that CENP-M is crucially required for the assembly and stability of a tetramer also comprising CENP-I, CENP-H, and CENP-K, the HIKM complex, which we extensively characterize through a combination of structural, biochemical, and cell biological approaches. A point mutant affecting the CENP-M/CENP-I interaction hampers kinetochore assembly and chromosome alignment and prevents kinetochore recruitment of the CENP-T/W complex, questioning a role of CENP-T/W as founder of an independent axis of kinetochore assembly. Our studies identify a single pathway having CENP-C as founder, and CENP-H/I/K/M and CENP-T/W as CENP-C-dependent followers.

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 Separate to operate: the centriole-free inner core of the centrosome regulates the assembly of the intranuclear spindle in Toxoplasma gondii

2022 ◽  
Author(s):  
Ramiro Tomasina ◽  
Érica S Martins-Duarte ◽  
Philippe Bastin ◽  
Mathieu Gissot ◽  
Maria E Francia
Keyword(s):  
Cell Division ◽  
Toxoplasma Gondii ◽  
Mitotic Spindle ◽  
Inner Core ◽  
Cell Formation ◽  
Outer Core ◽  
Structural Defects ◽  
Microtubule Organizing Center ◽  
Pericentriolar Material

Centrosomes are the main microtubule-organizing center of the cell. They are normally formed by two centrioles, embedded in a cloud of proteins known as pericentriolar material. The PCM ascribes centrioles with their microtubule nucleation capacity. Toxoplasma gondii, the causative agent of toxoplasmosis, divides by endodyogeny. Successful cell division is critical for pathogenesis. The centrosome, plays central roles in orchestrating the temporal and physical coordination of major organelle segregation and daughter cell formation. The T. gondii centrosome is formed by two domains; an outer core, distal from the nucleus, and an inner core, proximal to the nucleus. This dual organization has been proposed to underlie T. gondii’s cell division plasticity. However, the role of the inner core remains undeciphered. Here, we focus on the role of its only known molecular marker; TgCEP250L1. We show that upon conditional degradation of TgCEP250L1, parasites exhibit nuclear segregation defects, whilst normally forming daughter cells. In addition, the centrioles, disconnect from the nucleus. We explore the structural defects underlying these phenotypes by high resolution microscopy. We show that TgCEP250L1’s location is dynamic and encompasses the formation of the mitotic spindle. Moreover, we show that in the absence of TgCEP250L1, the microtubule binding protein TgEB1, fails to translocate from the nucleus to the mitotic spindle, while polyploid nuclei accumulate. Overall, our data supports a model in which the inner core of the T. gondii centrosome critically participates in cell division by directly impacting the formation or stability of the mitotic spindle.

scholarly journals Regulation of the Min Cell Division Inhibition Complex by the Rcs Phosphorelay in Proteus mirabilis

2015 ◽  
Vol 197 (15) ◽  
pp. 2499-2507 ◽  
Author(s):  
Kristen E. Howery ◽  
Katy M. Clemmer ◽  
Emrah Şimşek ◽  
Minsu Kim ◽  
Philip N. Rather
Keyword(s):  
Cell Division ◽  
Cell Differentiation ◽  
Proteus Mirabilis ◽  
Cell Elongation ◽  
Response Regulator ◽  
Swarmer Cell ◽  
Content Type ◽  
Expression Of Genes ◽  
Rapid Amplification

ABSTRACTA key regulator of swarming inProteus mirabilisis the Rcs phosphorelay, which repressesflhDC, encoding the master flagellar regulator FlhD4C2. Mutants inrcsB, the response regulator in the Rcs phosphorelay, hyperswarm on solid agar and differentiate into swarmer cells in liquid, demonstrating that this system also influences the expression of genes central to differentiation. To gain a further understanding of RcsB-regulated genes involved in swarmer cell differentiation, transcriptome sequencing (RNA-Seq) was used to examine the RcsB regulon. Among the 133 genes identified,minCandminD, encoding cell division inhibitors, were identified as RcsB-activated genes. A third gene,minE, was shown to be part of an operon withminCD. To examineminCDEregulation, theminpromoter was identified by 5′ rapid amplification of cDNA ends (5′-RACE), and both transcriptionallacZfusions and quantitative real-time reverse transcriptase (qRT) PCR were used to confirm that theminCDEoperon was RcsB activated. Purified RcsB was capable of directly binding theminCpromoter region. To determine the role of RcsB-mediated activation ofminCDEin swarmer cell differentiation, a polarminCmutation was constructed. This mutant formed minicells during growth in liquid, produced shortened swarmer cells during differentiation, and exhibited decreased swarming motility.IMPORTANCEThis work describes the regulation and role of the MinCDE cell division system inP. mirabilisswarming and swarmer cell elongation. Prior to this study, the mechanisms that inhibit cell division and allow swarmer cell elongation were unknown. In addition, this work outlines for the first time the RcsB regulon inP. mirabilis. Taken together, the data presented in this study begin to address howP. mirabiliselongates upon contact with a solid surface.

scholarly journals The postmitotic midbody: Regulating polarity, stemness, and proliferation

2019 ◽  
Vol 218 (12) ◽  
pp. 3903-3911 ◽  
Author(s):  
Eric Peterman ◽  
Rytis Prekeris
Keyword(s):  
Cell Division ◽  
Cell Polarity ◽  
Final Stage ◽  
Cell Membranes ◽  
Daughter Cell ◽  
Endocytic Trafficking ◽  
Microtubule Severing ◽  
Daughter Cells ◽  
Cytoskeleton Dynamics

Abscission, the final stage of cell division, requires well-orchestrated changes in endocytic trafficking, microtubule severing, actin clearance, and the physical sealing of the daughter cell membranes. These processes are highly regulated, and any missteps in localized membrane and cytoskeleton dynamics often lead to a delay or a failure in cell division. The midbody, a microtubule-rich structure that forms during cytokinesis, is a key regulator of abscission and appears to function as a signaling platform coordinating cytoskeleton and endosomal dynamics during the terminal stages of cell division. It was long thought that immediately following abscission and the conclusion of cell division, the midbody is either released or rapidly degraded by one of the daughter cells. Recently, the midbody has gained prominence for exerting postmitotic functions. In this review, we detail the role of the midbody in orchestrating abscission, as well as discuss the relatively new field of postabscission midbody biology, particularly focusing on how it may act to regulate cell polarity and its potential to regulate cell tumorigenicity or stemness.

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