Cargando…

Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis

Animal cytokinesis ends with the formation of a thin intercellular membrane bridge that connects the two newly formed sibling cells, which is ultimately resolved by abscission. While mitosis is completed within 15 min, the intercellular bridge can persist for hours, maintaining a physical connection...

Descripción completa

Detalles Bibliográficos
Autores principales: Adar-Levor, Shai, Nachmias, Dikla, Gal-Oz, Shani T., Jahn, Yarden M., Peyrieras, Nadine, Zaritsky, Assaf, Birnbaum, Ramon Y., Elia, Natalie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8053991/
https://www.ncbi.nlm.nih.gov/pubmed/33837152
http://dx.doi.org/10.1073/pnas.2021210118
_version_ 1783680226126987264
author Adar-Levor, Shai
Nachmias, Dikla
Gal-Oz, Shani T.
Jahn, Yarden M.
Peyrieras, Nadine
Zaritsky, Assaf
Birnbaum, Ramon Y.
Elia, Natalie
author_facet Adar-Levor, Shai
Nachmias, Dikla
Gal-Oz, Shani T.
Jahn, Yarden M.
Peyrieras, Nadine
Zaritsky, Assaf
Birnbaum, Ramon Y.
Elia, Natalie
author_sort Adar-Levor, Shai
collection PubMed
description Animal cytokinesis ends with the formation of a thin intercellular membrane bridge that connects the two newly formed sibling cells, which is ultimately resolved by abscission. While mitosis is completed within 15 min, the intercellular bridge can persist for hours, maintaining a physical connection between sibling cells and allowing exchange of cytosolic components. Although cell–cell communication is fundamental for development, the role of intercellular bridges during embryogenesis has not been fully elucidated. In this work, we characterized the spatiotemporal characteristics of the intercellular bridge during early zebrafish development. We found that abscission is delayed during the rapid division cycles that occur in the early embryo, giving rise to the formation of interconnected cell clusters. Abscission was accelerated when the embryo entered the midblastula transition (MBT) phase. Components of the ESCRT machinery, which drives abscission, were enriched at intercellular bridges post-MBT and, interfering with ESCRT function, extended abscission beyond MBT. Hallmark features of MBT, including transcription onset and cell shape modulations, were more similar in interconnected sibling cells compared to other neighboring cells. Collectively, our findings suggest that delayed abscission in the early embryo allows clusters of cells to coordinate their behavior during embryonic development.
format Online
Article
Text
id pubmed-8053991
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher National Academy of Sciences
record_format MEDLINE/PubMed
spelling pubmed-80539912021-05-04 Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis Adar-Levor, Shai Nachmias, Dikla Gal-Oz, Shani T. Jahn, Yarden M. Peyrieras, Nadine Zaritsky, Assaf Birnbaum, Ramon Y. Elia, Natalie Proc Natl Acad Sci U S A Biological Sciences Animal cytokinesis ends with the formation of a thin intercellular membrane bridge that connects the two newly formed sibling cells, which is ultimately resolved by abscission. While mitosis is completed within 15 min, the intercellular bridge can persist for hours, maintaining a physical connection between sibling cells and allowing exchange of cytosolic components. Although cell–cell communication is fundamental for development, the role of intercellular bridges during embryogenesis has not been fully elucidated. In this work, we characterized the spatiotemporal characteristics of the intercellular bridge during early zebrafish development. We found that abscission is delayed during the rapid division cycles that occur in the early embryo, giving rise to the formation of interconnected cell clusters. Abscission was accelerated when the embryo entered the midblastula transition (MBT) phase. Components of the ESCRT machinery, which drives abscission, were enriched at intercellular bridges post-MBT and, interfering with ESCRT function, extended abscission beyond MBT. Hallmark features of MBT, including transcription onset and cell shape modulations, were more similar in interconnected sibling cells compared to other neighboring cells. Collectively, our findings suggest that delayed abscission in the early embryo allows clusters of cells to coordinate their behavior during embryonic development. National Academy of Sciences 2021-04-13 2021-04-07 /pmc/articles/PMC8053991/ /pubmed/33837152 http://dx.doi.org/10.1073/pnas.2021210118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Adar-Levor, Shai
Nachmias, Dikla
Gal-Oz, Shani T.
Jahn, Yarden M.
Peyrieras, Nadine
Zaritsky, Assaf
Birnbaum, Ramon Y.
Elia, Natalie
Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title_full Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title_fullStr Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title_full_unstemmed Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title_short Cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
title_sort cytokinetic abscission is part of the midblastula transition in early zebrafish embryogenesis
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8053991/
https://www.ncbi.nlm.nih.gov/pubmed/33837152
http://dx.doi.org/10.1073/pnas.2021210118
work_keys_str_mv AT adarlevorshai cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT nachmiasdikla cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT galozshanit cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT jahnyardenm cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT peyrierasnadine cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT zaritskyassaf cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT birnbaumramony cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis
AT elianatalie cytokineticabscissionispartofthemidblastulatransitioninearlyzebrafishembryogenesis