Special Issue "Comparative Biology of Centrosomal Structures in Eukaryotes"

A special issue of Cells (ISSN 2073-4409).

Deadline for manuscript submissions: closed (30 June 2018)

Special Issue Editor

Guest Editor
Prof. Dr. Ralph Gräf

Department of Cell Biology, Institute for Biochemistry and Biology, University of Potsdam, Potsdam-Golm, Germany
Website | E-Mail
Interests: centrosome; nuclear lamina; microtubules; Dictyostelium

Special Issue Information

Dear Colleagues,

Centrosome-like organelles are the main microtubule-organizing center in animals, fungi and lower eukaryotes. They duplicate once, and only once, in the cell cycle prior to mitosis, and during mitosis they are critically involved in spindle formation, chromosome segregation and cytokinesis. Due to their central role in microtubule organization, centrosomes are also crucial for cell architecture in all organisms using microtubules for organelle positioning. They generally consist of a central, highly organized structure serving as a scaffold for microtubule nucleation complexes. Different types of centrosomal organelles have emerged during eukaryotic evolution. The most common type, the centriole-containing centrosome, is found among Opisthokonta in animals, in some Amoebozoa and among Bikonta, for example, in lower plants. All these organisms use centrioles also as basal bodies of cilia. However, organisms having lost locomotion by cilia or flagellae, such as many fungi and amoebae, contain no centrioles and possess acentriolar centrosomes, which are sometimes called nucleus-associated bodies (NABs) or spindle pole bodies (SPBs). In the light of evolution, our current understanding of centrosome biogenesis and function is primarily based on studies in only one eukaryotic supergroup, the Opisthokonta, which includes metazoans and fungi. This Special Issue of Cells should improve our understanding of centrosome function and evolution by including researchers working not only with Opisthokonts but also model organisms from other eukaryotic supergroups, i.e., Amoebozoa, Archaeplastida, Excavata and SAR (Stramenopile, Alveolata, Rhizaria). Comparing centrosome structure, function and association with nuclear structures will also improve our understanding of ancient centrosomal functions that are independent of the formation of centrioles.

Prof. Dr. Ralph Gräf
Guest Editor

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Keywords

  • centrosome
  • spindle-pole body
  • nucleus associated body
  • mitosis

Published Papers (10 papers)

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Research

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Open AccessFeature PaperArticle Osmotic Stress Blocks Mobility and Dynamic Regulation of Centriolar Satellites
Received: 25 May 2018 / Revised: 19 June 2018 / Accepted: 20 June 2018 / Published: 22 June 2018
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Abstract
Centriolar satellites (CS) are small proteinaceous granules that cluster around the centrosome and serve as cargo vehicles for centrosomal proteins. It is generally accepted that CS support a number of canonical and specialized centrosome functions. Consequently, these highly dynamic structures are the target
[...] Read more.
Centriolar satellites (CS) are small proteinaceous granules that cluster around the centrosome and serve as cargo vehicles for centrosomal proteins. It is generally accepted that CS support a number of canonical and specialized centrosome functions. Consequently, these highly dynamic structures are the target of regulation by several cellular signalling pathways. Two decades of research have led to the identification of a large number of molecular components and new biological roles of CS. Here, we summarize the latest advances in the continuous efforts to uncover the compositional, functional, dynamic and regulatory aspects of CS. We also report on our discovery that osmotic stress conditions render CS immobile and insensitive to remodelling. Upon a range of p38-activating stimuli, MK2 phosphorylates the CS component CEP131, resulting in 14-3-3 binding and a block to CS formation. This normally manifests as a rapid cellular depletion of satellites. In the case of osmotic stress, a potent inducer of p38 activity, CS translocation and dissolution is blocked, with the net result that satellites persist in an immobile state directly adjacent to the centrosome. Our results highlight a unique scenario where p38 activation and CS depletion is uncoupled, with potential implications for physiological and pathological osmotic stress responses. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperArticle CDK5RAP2 Is an Essential Scaffolding Protein of the Corona of the Dictyostelium Centrosome
Received: 3 April 2018 / Revised: 18 April 2018 / Accepted: 20 April 2018 / Published: 23 April 2018
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Abstract
Dictyostelium centrosomes consist of a nucleus-associated cylindrical, three-layered core structure surrounded by a corona consisting of microtubule-nucleation complexes embedded in a scaffold of large coiled-coil proteins. One of them is the conserved CDK5RAP2 protein. Here we focus on the role of Dictyostelium CDK5RAP2
[...] Read more.
Dictyostelium centrosomes consist of a nucleus-associated cylindrical, three-layered core structure surrounded by a corona consisting of microtubule-nucleation complexes embedded in a scaffold of large coiled-coil proteins. One of them is the conserved CDK5RAP2 protein. Here we focus on the role of Dictyostelium CDK5RAP2 for maintenance of centrosome integrity, its interaction partners and its dynamic behavior during interphase and mitosis. GFP-CDK5RAP2 is present at the centrosome during the entire cell cycle except from a short period during prophase, correlating with the normal dissociation of the corona at this stage. RNAi depletion of CDK5RAP2 results in complete disorganization of centrosomes and microtubules suggesting that CDK5RAP2 is required for organization of the corona and its association to the core structure. This is in line with the observation that overexpressed GFP-CDK5RAP2 elicited supernumerary cytosolic MTOCs. The phenotype of CDK5RAP2 depletion was very reminiscent of that observed upon depletion of CP148, another scaffolding protein of the corona. BioID interaction assays revealed an interaction of CDK5RAP2 not only with the corona markers CP148, γ-tubulin, and CP248, but also with the core components Cep192, CP75, and CP91. Furthermore, protein localization studies in both depletion strains revealed that CP148 and CDK5RAP2 cooperate in corona organization. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Review

Jump to: Research

Open AccessFeature PaperReview Centrosomal and Non-Centrosomal Microtubule-Organizing Centers (MTOCs) in Drosophila melanogaster
Received: 30 July 2018 / Revised: 19 August 2018 / Accepted: 20 August 2018 / Published: 28 August 2018
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Abstract
The centrosome is the best-understood microtubule-organizing center (MTOC) and is essential in particular cell types and at specific stages during Drosophila development. The centrosome is not required zygotically for mitosis or to achieve full animal development. Nevertheless, centrosomes are essential maternally during cleavage
[...] Read more.
The centrosome is the best-understood microtubule-organizing center (MTOC) and is essential in particular cell types and at specific stages during Drosophila development. The centrosome is not required zygotically for mitosis or to achieve full animal development. Nevertheless, centrosomes are essential maternally during cleavage cycles in the early embryo, for male meiotic divisions, for efficient division of epithelial cells in the imaginal wing disc, and for cilium/flagellum assembly in sensory neurons and spermatozoa. Importantly, asymmetric and polarized division of stem cells is regulated by centrosomes and by the asymmetric regulation of their microtubule (MT) assembly activity. More recently, the components and functions of a variety of non-centrosomal microtubule-organizing centers (ncMTOCs) have begun to be elucidated. Throughout Drosophila development, a wide variety of unique ncMTOCs form in epithelial and non-epithelial cell types at an assortment of subcellular locations. Some of these cell types also utilize the centrosomal MTOC, while others rely exclusively on ncMTOCs. The impressive variety of ncMTOCs being discovered provides novel insight into the diverse functions of MTOCs in cells and tissues. This review highlights our current knowledge of the composition, assembly, and functional roles of centrosomal and non-centrosomal MTOCs in Drosophila. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Revisiting Centrioles in Nematodes—Historic Findings and Current Topics
Received: 6 July 2018 / Revised: 23 July 2018 / Accepted: 24 July 2018 / Published: 8 August 2018
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Abstract
Theodor Boveri is considered as the “father” of centrosome biology. Boveri’s fundamental findings have laid the groundwork for decades of research on centrosomes. Here, we briefly review his early work on centrosomes and his first description of the centriole. Mainly focusing on centriole
[...] Read more.
Theodor Boveri is considered as the “father” of centrosome biology. Boveri’s fundamental findings have laid the groundwork for decades of research on centrosomes. Here, we briefly review his early work on centrosomes and his first description of the centriole. Mainly focusing on centriole structure, duplication, and centriole assembly factors in C. elegans, we will highlight the role of this model in studying germ line centrosomes in nematodes. Last but not least, we will point to future directions of the C. elegans centrosome field. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Chlamydomonas Basal Bodies as Flagella Organizing Centers
Received: 12 June 2018 / Revised: 9 July 2018 / Accepted: 10 July 2018 / Published: 17 July 2018
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Abstract
During ciliogenesis, centrioles convert to membrane-docked basal bodies, which initiate the formation of cilia/flagella and template the nine doublet microtubules of the flagellar axoneme. The discovery that many human diseases and developmental disorders result from defects in flagella has fueled a strong interest
[...] Read more.
During ciliogenesis, centrioles convert to membrane-docked basal bodies, which initiate the formation of cilia/flagella and template the nine doublet microtubules of the flagellar axoneme. The discovery that many human diseases and developmental disorders result from defects in flagella has fueled a strong interest in the analysis of flagellar assembly. Here, we will review the structure, function, and development of basal bodies in the unicellular green alga Chlamydomonas reinhardtii, a widely used model for the analysis of basal bodies and flagella. Intraflagellar transport (IFT), a flagella-specific protein shuttle critical for ciliogenesis, was first described in C. reinhardtii. A focus of this review will be on the role of the basal bodies in organizing the IFT machinery. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Animal Female Meiosis: The Challenges of Eliminating Centrosomes
Received: 17 May 2018 / Revised: 3 July 2018 / Accepted: 3 July 2018 / Published: 10 July 2018
Cited by 1 | PDF Full-text (997 KB) | HTML Full-text | XML Full-text
Abstract
Sexual reproduction requires the generation of gametes, which are highly specialised for fertilisation. Female reproductive cells, oocytes, grow up to large sizes when they accumulate energy stocks and store proteins as well as mRNAs to enable rapid cell divisions after fertilisation. At the
[...] Read more.
Sexual reproduction requires the generation of gametes, which are highly specialised for fertilisation. Female reproductive cells, oocytes, grow up to large sizes when they accumulate energy stocks and store proteins as well as mRNAs to enable rapid cell divisions after fertilisation. At the same time, metazoan oocytes eliminate their centrosomes, i.e., major microtubule-organizing centres (MTOCs), during or right after the long growth phases. Centrosome elimination poses two key questions: first, how can the centrosome be re-established after fertilisation? In general, metazoan oocytes exploit sperm components, i.e., the basal body of the sperm flagellum, as a platform to reinitiate centrosome production. Second, how do most metazoan oocytes manage to build up meiotic spindles without centrosomes? Oocytes have evolved mechanisms to assemble bipolar spindles solely around their chromosomes without the guidance of pre-formed MTOCs. Female animal meiosis involves microtubule nucleation and organisation into bipolar microtubule arrays in regulated self-assembly under the control of the Ran system and nuclear transport receptors. This review summarises our current understanding of the molecular mechanism underlying self-assembly of meiotic spindles, its spatio-temporal regulation, and the key players governing this process in animal oocytes. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Centrosome Remodelling in Evolution
Received: 26 May 2018 / Revised: 27 June 2018 / Accepted: 4 July 2018 / Published: 6 July 2018
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Abstract
The centrosome is the major microtubule organizing centre (MTOC) in animal cells. The canonical centrosome is composed of two centrioles surrounded by a pericentriolar matrix (PCM). In contrast, yeasts and amoebozoa have lost centrioles and possess acentriolar centrosomes—called the spindle pole body (SPB)
[...] Read more.
The centrosome is the major microtubule organizing centre (MTOC) in animal cells. The canonical centrosome is composed of two centrioles surrounded by a pericentriolar matrix (PCM). In contrast, yeasts and amoebozoa have lost centrioles and possess acentriolar centrosomes—called the spindle pole body (SPB) and the nucleus-associated body (NAB), respectively. Despite the difference in their structures, centriolar centrosomes and SPBs not only share components but also common biogenesis regulators. In this review, we focus on the SPB and speculate how its structures evolved from the ancestral centrosome. Phylogenetic distribution of molecular components suggests that yeasts gained specific SPB components upon loss of centrioles but maintained PCM components associated with the structure. It is possible that the PCM structure remained even after centrosome remodelling due to its indispensable function to nucleate microtubules. We propose that the yeast SPB has been formed by a step-wise process; (1) an SPB-like precursor structure appeared on the ancestral centriolar centrosome; (2) it interacted with the PCM and the nuclear envelope; and (3) it replaced the roles of centrioles. Acentriolar centrosomes should continue to be a great model to understand how centrosomes evolved and how centrosome biogenesis is regulated. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Rapid Evolution of Sperm Produces Diverse Centriole Structures that Reveal the Most Rudimentary Structure Needed for Function
Received: 30 May 2018 / Revised: 22 June 2018 / Accepted: 22 June 2018 / Published: 26 June 2018
Cited by 1 | PDF Full-text (3097 KB) | HTML Full-text | XML Full-text
Abstract
Centrioles are ancient subcellular protein-based organelles that maintain a conserved number and structure across many groups of eukaryotes. Centriole number (two per cells) is tightly regulated; each pre-existing centriole nucleates only one centriole as the cell prepares for division. The structure of centrioles
[...] Read more.
Centrioles are ancient subcellular protein-based organelles that maintain a conserved number and structure across many groups of eukaryotes. Centriole number (two per cells) is tightly regulated; each pre-existing centriole nucleates only one centriole as the cell prepares for division. The structure of centrioles is barrel-shaped, with a nine-fold symmetry of microtubules. This organization of microtubules is essential for the ancestral function of centriole–cilium nucleation. In animal cells, centrioles have gained an additional role: recruiting pericentriolar material (PCM) to form a centrosome. Therefore, it is striking that in animal spermatozoa, the centrioles have a remarkable diversity of structures, where some are so anomalous that they are referred to as atypical centrioles and are barely recognizable. The atypical centriole maintains the ability to form a centrosome and nucleate a new centriole, and therefore reveals the most rudimentary structure that is needed for centriole function. However, the atypical centriole appears to be incapable of forming a cilium. Here, we propose that the diversity in sperm centriole structure is due to rapid evolution in the shape of the spermatozoa head and neck. The enhanced diversity may be driven by a combination of direct selection for novel centriole functions and pleiotropy, which eliminates centriole properties that are dispensable in the spermatozoa function. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Duplication and Nuclear Envelope Insertion of the Yeast Microtubule Organizing Centre, the Spindle Pole Body
Received: 19 April 2018 / Revised: 4 May 2018 / Accepted: 8 May 2018 / Published: 10 May 2018
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Abstract
The main microtubule organizing centre in the unicellular model organisms Saccharomyces cerevisiae and Schizosaccharomyces pompe is the spindle pole body (SPB). The SPB is a multilayer structure, which duplicates exactly once per cell cycle. Unlike higher eukaryotic cells, both yeast model organisms undergo
[...] Read more.
The main microtubule organizing centre in the unicellular model organisms Saccharomyces cerevisiae and Schizosaccharomyces pompe is the spindle pole body (SPB). The SPB is a multilayer structure, which duplicates exactly once per cell cycle. Unlike higher eukaryotic cells, both yeast model organisms undergo mitosis without breakdown of the nuclear envelope (NE), a so-called closed mitosis. Therefore, in order to simultaneously nucleate nuclear and cytoplasmic MTs, it is vital to embed the SPB into the NE at least during mitosis, similarly to the nuclear pore complex (NPC). This review aims to embrace the current knowledge of the SPB duplication cycle with special emphasis on the critical step of the insertion of the new SPB into the NE. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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Open AccessFeature PaperReview Centrosome Positioning in Dictyostelium: Moving beyond Microtubule Tip Dynamics
Received: 9 March 2018 / Revised: 10 April 2018 / Accepted: 10 April 2018 / Published: 12 April 2018
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Abstract
The variability in centrosome size, shape, and activity among different organisms provides an opportunity to understand both conserved and specialized actions of this intriguing organelle. Centrosomes in the model organism Dictyostelium sp. share some features with fungal systems and some with vertebrate cell
[...] Read more.
The variability in centrosome size, shape, and activity among different organisms provides an opportunity to understand both conserved and specialized actions of this intriguing organelle. Centrosomes in the model organism Dictyostelium sp. share some features with fungal systems and some with vertebrate cell lines and thus provide a particularly useful context to study their dynamics. We discuss two aspects, centrosome positioning in cells and their interactions with nuclei during division as a means to highlight evolutionary modifications to machinery that provide the most basic of cellular services. Full article
(This article belongs to the Special Issue Comparative Biology of Centrosomal Structures in Eukaryotes)
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