Special Issue "Comparative Biology of Centrosomal Structures in Eukaryotes"

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

Deadline for manuscript submissions: 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

Manuscript Submission Information

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Keywords

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

Published Papers (3 papers)

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Research

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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

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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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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Author: Prof. Tomer Avidor-Reiss
Affiliation: Associate Professor, University of Toledo, Toledo, USA
Tentative title: The Typical and Atypical Centrioles of Animal Sperm
Abstract: Centrioles are ancient subcellular organelles, which maintain a conserved structure across many groups of eukaryotes. Typical centrioles are barrel-shape structures with a nine-folds symmetry of microtubules, which are essential for cilium nucleation. In animal cells, centrioles have an additional role, recruiting pericentriolar material (PCM) to form a centrosome. To accomplish their specialized roles, centriole number in the cells is tightly controlled, and new centrioles must be formed by duplication of preexisting centrioles. It is striking, therefore, that in animal spermatozoa the centrioles have a remarkable diversity of structures and therefore are referred as atypical centrioles. The atypical centrioles maintain the ability to form a centrosome and duplicate but appear to be incapable of forming cilia. Here, we propose that the diversity in sperm centriole structure is due to rapid evolution in the microtubules based mechanisms that shape the spermatozoa head and neck. The enhanced diversity may be driven by a combination of direct selection for novel centriole functions and pleiotropy that eliminates centriole properties that are dispensable in the spermatozoa and postfertilization in the early embryo.

Author: Julie C. Nielsen, Cathrine Nordgaard, Maxim A.X. Tollenaere, and Simon Bekker-Jensen
Affiliation: Center for Healthy Aging, Department of Cellular and Molecular Medicine, University of Copenhagen, Blegdamsvej 3B, DK-2200 Copenhagen, Denmark
Tentative title: Dynamic regulation of centriolar satellites
Abstract: Centriolar satellites (CS) are small and proteinaceous granules that cluster tightly around the centrosome, and are likely functioning as trafficking containers for centrosomal proteins. Two decades of research has helped us identify the molecular components and biological functions of CS, and it is generally accepted that CS support various canonical and specialized centrosomal tasks. Global mass spectrometry based screens have been paramount in uncovering hundreds of novel putative CS-residing proteins and have revealed that many of such proteins are subject to post-translational modifications. Such studies have highlighted that the molecular composition and functions of CS are highly dynamic, and can be altered upon various extra- and intracellular cues. In this mini-review, we summarize the latest advances made regarding the dynamic regulation of CS and we present novel data of CS integrity in response to various cellular stressors.

Authors: Marisa Tillery, Caitlyn Blake-Hedges, Rebecca Buchwalter, Yiming Zheng and Dr. Timothy Megraw
Affiliation: Florida State Univ, USA
Tentative title: Centrosomal and Non-centrosomal MTOCs in the Development of Drosophila melanogaster
Abstract: The centrosome, often touted as the major microtubule-organizing center (MTOC) of the cell, has historically overshadowed the more humble non-centrosomal microtubule-organizing centers (ncMTOCs) that have more recently begun to be appreciated and functionally dissected. In Drosophila, a functional centrosome is not required zygotically to achieve full animal development. However, centrosomes are essential maternally for cleavage cycles in the early embryo, for male meiotic divisions, and for efficient division of epithelial cells in the imaginal wing disk. Throughout Drosophila development several excellent models to study unique and lesser-known MTOCs emerge such as: the membrane MTOC in the Drosophila oocyte, the poorly understood ncMTOC in the imaginal eye disc, the apical membrane MTOC in tracheal epithelial cells, the apical adherens junction MTOC in the wing epithelium, the perinuclear MTOC in the muscle, the dendritic branch site MTOCs in neurons, the mitochondrial MTOC in the testis, and the recently-discovered perinuclear MTOC in the larval fat body. Some of these cell types also utilize the canonical centrosomal MTOC, while others rely exclusively on ncMTOCs. The impressive variety of ncMTOCs being discovered provides novel insight into the development of diverse differentiated cells and tissues. This review will highlight our current knowledge of the composition, mechanism of assembly, and functional role(s) of centrosomal and non-centrosomal MTOCs throughout Drosophila development.

Author: T. Müller-Reichert (Dresden) and Kevin O’Connell (Bethesda).
Tentative title: Revisiting centrosomes in nematodes: historic achievements and current topics

Title: Cep161 is an essential scaffolding protein of the corona of the Dictyostelium centrosome
Authors: Valentin Pitzen, Sophie Askarzada, Ralph Gräf and Irene Meyer*
Affiliation: University of Potsdam, Department of Cell Biology, Karl-Liebknecht-Str. 24-25, 14476 Potsdam-Golm, Germany
Abstract: Acentriolar Dictyostelium centrosomes consist of a nucleus-associated cylindrical, three-layered core structure surrounded by a corona. While the core structure is the replicating unit, the corona contains microtubule-nucleation complexes embedded in a scaffold of large coiled-coil proteins. One of them is the conserved CDK5RAP2 protein (also named Cep161 in Dictyostelium) encoded by the CepL gene. In contrast to previously published work we focus on the role of CDK5RAP2 for maintenance of centrosome integrity, its interaction partners and its dynamic behavior during interphase and mitosis. Knock-down of CDK5RAP2 by RNAi results in a complete disorganization of microtubules with no clearly discernible MTOC, reminiscent of a previously published CP148-RNAi strain. Core structures were distributed in the cytosol with no connection to the nucleus and classical corona proteins suggesting that CDK5RAP2, like CP148, is required for integrity of the corona and its association to the core structure. Its role as a scaffolding protein within the corona is underscored by its low mobility in FRAP experiments in a CDK5RAP2-GFP knock-in strain. CDK5RAP2 is present at the centrosome during the entire cell cycle except from a short period during prophase, correlating with the normal disassembly of all microtubules at this stage. Surprisingly, expression of GFP-CDK5RAP2 carrying a deletion of one or both predicted CDK1 phosphorylation sites strongly increased the presence of the core protein CP55 at mitotic centrosomes indicating a functional interaction of both proteins. This is in agreement with the findings that CP55, together with CP91, localizes to cytosolic foci of overexpressed GFP-CP161 and that both CP55 and CP91 interact with CDK5RAP2 in BioID analyses. These results suggest a further role of CDK5RAP2 in linkage of the corona to the core layers, putatively together with CP148, which in turn is required to bind CDK5RAP2 at centrosomes.

Title: Chlamydomonas basal bodies as organizing centers for flagella
Authors: Jenna Wingfield and Karl Lechtreck
Affiliation: University of Georgia, USA
Abstract: During ciliogenesis, centrioles convert to membrane-docked basal bodies, which will initiate the formation of cilia and template the nine doublet microtubules of the ciliary axoneme. The discovery that many human diseases and developmental disorders result from defects in cilia has fueled a strong interest in the analysis of cilia assembly. Here, we will review the basal body structure and function of the unicellular green alga Chlamydomonas reinhardtii. Intraflagellar transport (IFT), a cilia-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.

Title: Duplication and nuclear envelope insertion of the yeast microtubule organizing centre, the spindle pole body
Authors: Diana Rüthnick and Elmar Schiebel
Abstract: The main microtubule (MT) organising centre in the 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. In order to nucleate simultaneously nuclear and cytoplasmic MTs, it is therefore vital to embed the SPB at least during mitosis into the NE in a way similar to the nuclear pore complex (NPC). This review aims to embrace the current knowledge of the SPB duplication cycle with aspecial emphasis on the critical step of the insertion of the new SPB into the NE.

Title: Centrosome Evolution
Authors: Daisuke Ito and Mónica Bettencourt-Dias
Affiliation: Instituto Gulbenkian de Ciência, Oeiras, Portugal
Abstract: The centrosome is the major microtubule organizing center, and the canonical animal centrosome is composed of two centrioles surrounded by pericentriolar matrix (PCM). In contrast, yeasts and amoeba have lost centrioles and posses diverged “centriole-less” centrosomes, called the spindle pole body (SPB) and the nuclear associated body (NAB), respectively. Despite their difference in structure, canonical and non-canonical centrosomes share components, and the biogenesis is controlled by common regulators. In this review, we focus on the yeast centrosomes and speculate how the structures and molecular components evolved to non-canonical centrosome. Phylogenetic distribution of molecular components suggests that the yeasts have gained specific SPB structural components upon loss of centrioles but maintained the PCM components associated with the structure. It is possible that the PCM core structure remained the same during divergence of the centrosomes due to the indispensable function to nucleate microtubules. We propose that the yeast SPB has been formed by step-wise processes; 1) the SPB precursor appeared on the ancestral centriolar centrosome, 2) it interacted with the PCM and 3) it replaced the roles of centrioles. Non-canonical centrosomes should continue to be a great model to understand how the centrosomes evolved and biogenesis is regulated.

Title: Self assembly of meiotic spindles: the challenges of eliminating centrosomes
Author: Oliver J. Gruss
Affiliation: Institute of Genetics, University of Bonn, Karlrobert-Kreiten-Str. 13, 53115 Bonn, Germany
Abstract: Sexual reproduction requires generation of gametes that are highly specialised for fertilisation. Animal oocytes grow up to very large sizes while they accumulate energy stocks and store proteins as well as mRNAs that will enable rapid cell divisions after fertilisation. However, metazoan oocytes eliminate their centrosomes, i.e. major microtubule-organizing centres (MTOCs), during or right after the long growth phases of oogenesis. Centrosome elimination poses two key questions: first, how is the centrosome re-established after fertilisation? In general, metazoan oocytes use sperm components, i.e. the basal body of the sperm flagellum, as a platform to reinitiate centrosome production. The second issue is to understand how metazoan oocytes manage to assemble 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 by regulated self-assembly. This review discusses the experimental systems that have been exploited to investigate centrosome-free spindle formation. It summarises our current understanding of the molecular mechanism underlying self-assembly of meiotic spindles, its spatio-temporal regulation and the key players governing the process in animal oocytes.

Title: Cell cycle regulation by the spindle pole body in budding yeast.
Authors: Hiromi Maekawa and Gislene Pereira
Affiliation:
1 Center for Promotion of International Education and Research, Faculty of Agriculture, Kyushu University
2 Centre for Organismal Studies (COS), University of Heidelberg, Germany
3 German Cancer Research Centre (DKFZ), Molecular Biology of Centrosomes and Cilia Unit, Heidelberg, Germany
Abstract: Spindle positioning is pivotal for the appropriate inheritance of cellular materials to the daughter cell during asymmetric cell division. In budding yeast, where the site of cell division (named the bud neck) determines the cleavage plane before chromosome segregation, spindle positioning and orientation along the mother-bud axis is of particular importance for the success of chromosome partitioning. Cytoplasmic microtubules emanated from spindle pole bodies (SPBs, functional equivalent to mammalian centrosomes), play a central role in this regulation. When spindle orientation fails, the spindle orientation checkpoint (SPOC) delays mitotic exit until spindle orientation is corrected. The SPOC prevents activation of the mitotic exit network (MEN), an SPB-associated signalling pathway. The cytoplasmic side of the SPB provides a scaffolding platform for MEN and SPOC proteins. Here, we discuss how SPBs fulfil temporal and spatial regulatory roles in coordinating mitotic exit with spindle position with a particular focus on physical interactions that may alter their molecular dynamics.

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