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Cytokinetic abscission is part of the mid-blastula transition switch in early zebrafish embryogenesis

Shai Adar-Levor, View ORCID ProfileDikla Nachmias, View ORCID ProfileShani T. Gal-Oz, Yarden M. Jahn, Nadine Peyrieras, View ORCID ProfileAssaf Zaritsky, View ORCID ProfileRamon Y. Birnbaum, View ORCID ProfileNatalie Elia
doi: https://doi.org/10.1101/2020.07.26.221515
Shai Adar-Levor
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
2National Institute for Biotechnology in the Negev (NIBN), Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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Dikla Nachmias
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
2National Institute for Biotechnology in the Negev (NIBN), Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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Shani T. Gal-Oz
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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Yarden M. Jahn
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
2National Institute for Biotechnology in the Negev (NIBN), Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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Nadine Peyrieras
3BioEmergences Laboratory (USR3695), CNRS, Université Paris-Saclay, Gif-sur-Yvette, France
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Assaf Zaritsky
4Department of Software and Information Systems Engineering, Ben-Gurion University of the Negev, Beer-Sheva 84105, Israel
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Ramon Y. Birnbaum
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
5Center of Evolutionary Genomics and Medicine, The Ben-Gurion University of the Negev 84105, Israel
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  • For correspondence: elianat@post.bgu.ac.il ramonb@bgu.ac.il
Natalie Elia
1Department of Life Sciences, Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
2National Institute for Biotechnology in the Negev (NIBN), Ben-Gurion University of the Negev, Beer Sheva 84105, Israel
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  • For correspondence: elianat@post.bgu.ac.il ramonb@bgu.ac.il
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ABSTRACT

Animal cytokinesis ends with the formation of a thin intercellular membrane bridge connecting the two newly formed sibling cells that is ultimately resolved by abscission. While mitosis is completed within 15 minutes, 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 potential role of intercellular bridges during embryogenesis have not been fully elucidated. Here, we found that in early zebrafish (Danio rerio) embryogenesis, abscission is delayed and cells do not resolve their intercellular bridges until midblastula transition (MBT), giving rise to the formation of small inter-connected cell clusters. Interestingly, abscission commences during the MBT switch, which is manifested by cell cycle elongation, loss of synchronized divisions and genome activation. Moreover, depletion of Chmp4bb which is an essential ESCRT-III component for scission, delayed abscission beyond the MBT switch. Hallmark features of MBT, including transcription onset and cell shape changes, were similar in sibling cells connected by intercellular bridges, proposing a role for intercellular bridges in maintaining cell-cell communication in the embryo. Taken together, our data suggest that abscission is part of the cellular changes that occur during MBT and that cells coordinate their behavior during this critical embryonic phase through persisted intercellular bridges.

Significance Statement In this work we show that the last step of cytokinesis, termed abscission, is inhibited in early zebrafish embryos. As a result, sibling cells remain connected to one another for several cycles and mutually time their developmental progress including transcription onset. Abscission commences at the 10th cell cycle, when embryos enter the midblastula transition (MBT) switch in which embryonic cells become individualized and exhibit the characteristics of mature cells. Our data suggest that abscission is part of the MBT switch and that embryonic sibling cells mutually time their developmental progress by maintaining physical connections between them in the early embryo.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Cytokinetic abscission is part of the mid-blastula transition switch in early zebrafish embryogenesis
Shai Adar-Levor, Dikla Nachmias, Shani T. Gal-Oz, Yarden M. Jahn, Nadine Peyrieras, Assaf Zaritsky, Ramon Y. Birnbaum, Natalie Elia
bioRxiv 2020.07.26.221515; doi: https://doi.org/10.1101/2020.07.26.221515
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Cytokinetic abscission is part of the mid-blastula transition switch in early zebrafish embryogenesis
Shai Adar-Levor, Dikla Nachmias, Shani T. Gal-Oz, Yarden M. Jahn, Nadine Peyrieras, Assaf Zaritsky, Ramon Y. Birnbaum, Natalie Elia
bioRxiv 2020.07.26.221515; doi: https://doi.org/10.1101/2020.07.26.221515

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