Cargando…

The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo

In embryos of most animal species, the zygotic centrosome is assembled by the centriole derived from the sperm cell and pericentriolar proteins present in the oocyte. This zygotic centrosome acts as a microtubule organizing center (MTOC) to assemble the sperm aster and mitotic spindle. As MTOC forma...

Descripción completa

Detalles Bibliográficos
Autores principales: Willekers, Sven, Tessadori, Federico, van der Vaart, Babet, Henning, Heiko H., Stucchi, Riccardo, Altelaar, Maarten, Roelen, Bernard A. J., Akhmanova, Anna, Bakkers, Jeroen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481976/
https://www.ncbi.nlm.nih.gov/pubmed/35980365
http://dx.doi.org/10.1242/dev.198762
_version_ 1784791358459871232
author Willekers, Sven
Tessadori, Federico
van der Vaart, Babet
Henning, Heiko H.
Stucchi, Riccardo
Altelaar, Maarten
Roelen, Bernard A. J.
Akhmanova, Anna
Bakkers, Jeroen
author_facet Willekers, Sven
Tessadori, Federico
van der Vaart, Babet
Henning, Heiko H.
Stucchi, Riccardo
Altelaar, Maarten
Roelen, Bernard A. J.
Akhmanova, Anna
Bakkers, Jeroen
author_sort Willekers, Sven
collection PubMed
description In embryos of most animal species, the zygotic centrosome is assembled by the centriole derived from the sperm cell and pericentriolar proteins present in the oocyte. This zygotic centrosome acts as a microtubule organizing center (MTOC) to assemble the sperm aster and mitotic spindle. As MTOC formation has been studied mainly in adult cells, very little is known about the formation of the zygotic MTOC. Here, we show that zebrafish (Danio rerio) embryos lacking either maternal or paternal Cfap53, a centriolar satellite protein, arrest during the first cell cycle. Although Cfap53 is dispensable for sperm aster function, it aids proper formation of the mitotic spindle. During cell division, Cfap53 colocalizes with γ-tubulin and with other centrosomal and centriolar satellite proteins at the MTOC. Furthermore, we find that γ-tubulin localization at the MTOC is impaired in the absence of Cfap53. Based on these results, we propose a model in which Cfap53 deposited in the oocyte and the sperm participates in the organization of the zygotic MTOC to allow mitotic spindle formation.
format Online
Article
Text
id pubmed-9481976
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher The Company of Biologists Ltd
record_format MEDLINE/PubMed
spelling pubmed-94819762022-10-25 The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo Willekers, Sven Tessadori, Federico van der Vaart, Babet Henning, Heiko H. Stucchi, Riccardo Altelaar, Maarten Roelen, Bernard A. J. Akhmanova, Anna Bakkers, Jeroen Development Research Article In embryos of most animal species, the zygotic centrosome is assembled by the centriole derived from the sperm cell and pericentriolar proteins present in the oocyte. This zygotic centrosome acts as a microtubule organizing center (MTOC) to assemble the sperm aster and mitotic spindle. As MTOC formation has been studied mainly in adult cells, very little is known about the formation of the zygotic MTOC. Here, we show that zebrafish (Danio rerio) embryos lacking either maternal or paternal Cfap53, a centriolar satellite protein, arrest during the first cell cycle. Although Cfap53 is dispensable for sperm aster function, it aids proper formation of the mitotic spindle. During cell division, Cfap53 colocalizes with γ-tubulin and with other centrosomal and centriolar satellite proteins at the MTOC. Furthermore, we find that γ-tubulin localization at the MTOC is impaired in the absence of Cfap53. Based on these results, we propose a model in which Cfap53 deposited in the oocyte and the sperm participates in the organization of the zygotic MTOC to allow mitotic spindle formation. The Company of Biologists Ltd 2022-08-18 /pmc/articles/PMC9481976/ /pubmed/35980365 http://dx.doi.org/10.1242/dev.198762 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Research Article
Willekers, Sven
Tessadori, Federico
van der Vaart, Babet
Henning, Heiko H.
Stucchi, Riccardo
Altelaar, Maarten
Roelen, Bernard A. J.
Akhmanova, Anna
Bakkers, Jeroen
The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title_full The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title_fullStr The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title_full_unstemmed The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title_short The centriolar satellite protein Cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
title_sort centriolar satellite protein cfap53 facilitates formation of the zygotic microtubule organizing center in the zebrafish embryo
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481976/
https://www.ncbi.nlm.nih.gov/pubmed/35980365
http://dx.doi.org/10.1242/dev.198762
work_keys_str_mv AT willekerssven thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT tessadorifederico thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT vandervaartbabet thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT henningheikoh thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT stucchiriccardo thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT altelaarmaarten thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT roelenbernardaj thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT akhmanovaanna thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT bakkersjeroen thecentriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT willekerssven centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT tessadorifederico centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT vandervaartbabet centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT henningheikoh centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT stucchiriccardo centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT altelaarmaarten centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT roelenbernardaj centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT akhmanovaanna centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo
AT bakkersjeroen centriolarsatelliteproteincfap53facilitatesformationofthezygoticmicrotubuleorganizingcenterinthezebrafishembryo