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      The centrosome – diverse functions in fertilization and development across species

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          ABSTRACT

          The centrosome is a non-membrane-bound organelle that is conserved across most animal cells and serves various functions throughout the cell cycle. In dividing cells, the centrosome is known as the spindle pole and nucleates a robust microtubule spindle to separate genetic material equally into two daughter cells. In non-dividing cells, the mother centriole, a substructure of the centrosome, matures into a basal body and nucleates cilia, which acts as a signal-transducing antenna. The functions of centrosomes and their substructures are important for embryonic development and have been studied extensively using in vitro mammalian cell culture or in vivo using invertebrate models. However, there are considerable differences in the composition and functions of centrosomes during different aspects of vertebrate development, and these are less studied. In this Review, we discuss the roles played by centrosomes, highlighting conserved and divergent features across species, particularly during fertilization and embryonic development.

          Abstract

          Summary: Delving into centrosomes, this Review discusses their versatile roles in animal cells, emphasizing their diverse functions during fertilization and embryonic development across species.

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          Cellular signalling by primary cilia in development, organ function and disease

          Zeinab Anvarian, Kirk Mykytyn, Saikat Mukhopadhyay … (2019)
          Primary cilia project in a single copy from the surface of most vertebrate cell types; they detect and transmit extracellular cues to regulate diverse cellular processes during development and to maintain tissue homeostasis. The sensory capacity of primary cilia relies on the coordinated trafficking and temporal localization of specific receptors and associated signal transduction modules in the cilium. The canonical hedgehog (HH) pathway, for example, is a bona fide ciliary signalling system that regulates cell fate and self-renewal in development and tissue homeostasis. Specific receptors and associated signal transduction proteins can also localize to primary cilia in a cell type-dependent manner; available evidence suggests that the ciliary constellation of these proteins can temporally change to allow the cell to adapt to specific developmental and homeostatic cues. Consistent with important roles for primary cilia in signalling, mutations that lead to their dysfunction underlie a pleiotropic group of diseases and syndromic disorders termed ciliopathies, which affect many different tissues and organs of the body. In this review we highlight central mechanisms by which primary cilia coordinate HH, G-protein-coupled receptor, WNT, receptor tyrosine kinase and TGFβ/BMP signalling, and illustrate how defects in the balanced output of ciliary signalling events are coupled to developmental disorders and disease progression.
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            Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes.

            Melina Schuh, Jan Ellenberg (2007)
            Chromosome segregation in mammalian oocytes is driven by a microtubule spindle lacking centrosomes. Here, we analyze centrosome-independent spindle assembly by quantitative high-resolution confocal imaging in live maturing mouse oocytes. We show that spindle assembly proceeds by the self-organization of over 80 microtubule organizing centers (MTOCs) that form de novo from a cytoplasmic microtubule network in prophase and that functionally replace centrosomes. Initially distributed throughout the ooplasm, MTOCs congress at the center of the oocyte, where they contribute to a massive, Ran-dependent increase of the number of microtubules after nuclear envelope breakdown and to the individualization of clustered chromosomes. Through progressive MTOC clustering and activation of kinesin-5, the multipolar MTOC aggregate self-organizes into a bipolar intermediate, which then elongates and thereby establishes chromosome biorientation. Finally, a stable barrel-shaped acentrosomal metaphase spindle with oscillating chromosomes and astral-like microtubules forms that surprisingly exhibits key properties of a centrosomal spindle.
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              Centriole distal appendages promote membrane docking, leading to cilia initiation.

              Barbara E Tanos, Meng-Fu Tsou, J. M. Asara … (2013)
              The distal appendages (DAPs) of centrioles have been proposed to anchor cilia to the plasma membrane, but their molecular composition, assembly, and exact function in ciliogenesis remain poorly understood. Using quantitative centrosome proteomics and superresolution microscopy, we identified five DAP components, including one previously described (CEP164), one partially characterized (CEP89 [ccdc123]), and three novel (CEP83 [ccdc41], SCLT1, and FBF1) DAP proteins. Analyses of DAP assembly revealed a hierarchy. CEP83 recruits both SCLT1 and CEP89 to centrioles. Subsequent recruitment of FBF1 and CEP164 is independent of CEP89 but mediated by SCLT1. All five DAP components are essential for ciliogenesis; loss of CEP83 specifically blocks centriole-to-membrane docking. Undocked centrioles fail to recruit TTBK2 or release CP110, the two earliest modifications found on centrioles prior to cilia assembly, revealing centriole-to-membrane docking as a temporal and spatial cue promoting cilia initiation.
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                Author and article information

                Contributors
                Abrar Aljiboury:
                ORCID: http://orcid.org/0000-0002-0420-4399
                Heidi Hehnly:
                ORCID: http://orcid.org/0000-0001-6660-5254
                Journal
                Journal ID (nlm-ta): J Cell Sci
                Journal ID (iso-abbrev): J Cell Sci
                Journal ID (publisher-id): JCS
                Title: Journal of Cell Science
                Publisher: The Company of Biologists Ltd
                ISSN (Print): 0021-9533
                ISSN (Electronic): 1477-9137
                Publication date Collection: 1 December 2023
                Publication date (Electronic): 1 December 2023
                Publication date PMC-release: 1 December 2023
                Volume: 136
                Issue: 23
                Electronic Location Identifier: jcs261387
                Affiliations
                [ 1 ]Syracuse University , Department of Biology, 107 College Place, Syracuse, NY 13244, USA
                [ 2 ]Syracuse University, BioInspired Institute , Syracuse, NY 13244, USA
                Author notes
                [* ]Authors for correspondence ( aaatiyaa@ 123456syr.edu , hhehnly@ 123456syr.edu )

                Competing interests

                The authors declare no competing or financial interests.

                Author information
                http://orcid.org/0000-0002-0420-4399
                http://orcid.org/0000-0001-6660-5254
                Article
                Publisher ID: JCS261387
                DOI: 10.1242/jcs.261387
                PMC ID: 10730021
                PubMed ID: 38038054
                SO-VID: 3e67e4a6-f83c-4c4f-87f3-7f895b9ca818
                Copyright © © 2023. Published by The Company of Biologists Ltd
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                Funding
                Funded by: National Institutes of Health, http://dx.doi.org/10.13039/100000002;
                Award ID: R01GM-127621
                Award ID: R01GM-130874
                Funded by: U.S. Department of Defense, http://dx.doi.org/10.13039/100000005;
                Award ID: W81XWH-20-1-0585
                Categories
                Subject: Review

                ScienceOpen disciplines: Cell biology
                Keywords: centriol appendages,centrioles,centrosome,cilia,pericentriolar matrix
                Data availability:
                ScienceOpen disciplines: Cell biology
                Keywords: centriol appendages, centrioles, centrosome, cilia, pericentriolar matrix

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