Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization
Caballero Mancebo S, Shinde R, Bolger-Munro M, Peruzzo M, Szep G, Steccari I, Labrousse Arias D, Zheden V, Merrin J, Callan-Jones A, Voituriez R, Heisenberg C-PJ. 2024. Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization. Nature Physics. 20, 310–321.
Download
Journal Article
| Published
| English
Scopus indexed
Author
Caballero Mancebo, SilviaISTA ;
Shinde, Rushikesh;
Bolger-Munro, MadisonISTA ;
Peruzzo, MatildaISTA ;
Szep, GregoryISTA;
Steccari, IreneISTA;
Labrousse Arias, DavidISTA;
Zheden, VanessaISTA ;
Merrin, JackISTA ;
Callan-Jones, Andrew;
Voituriez, Raphaël;
Heisenberg, Carl-Philipp ISTA
All
All
Corresponding author has ISTA affiliation
Department
Abstract
Contraction and flow of the actin cell cortex have emerged as a common principle by which cells reorganize their cytoplasm and take shape. However, how these cortical flows interact with adjacent cytoplasmic components, changing their form and localization, and how this affects cytoplasmic organization and cell shape remains unclear. Here we show that in ascidian oocytes, the cooperative activities of cortical actomyosin flows and deformation of the adjacent mitochondria-rich myoplasm drive oocyte cytoplasmic reorganization and shape changes following fertilization. We show that vegetal-directed cortical actomyosin flows, established upon oocyte fertilization, lead to both the accumulation of cortical actin at the vegetal pole of the zygote and compression and local buckling of the adjacent elastic solid-like myoplasm layer due to friction forces generated at their interface. Once cortical flows have ceased, the multiple myoplasm buckles resolve into one larger buckle, which again drives the formation of the contraction pole—a protuberance of the zygote’s vegetal pole where maternal mRNAs accumulate. Thus, our findings reveal a mechanism where cortical actomyosin network flows determine cytoplasmic reorganization and cell shape by deforming adjacent cytoplasmic components through friction forces.
Publishing Year
Date Published
2024-02-01
Journal Title
Nature Physics
Publisher
Springer Nature
Acknowledgement
We would like to thank A. McDougall, E. Hannezo and the Heisenberg lab for fruitful discussions and reagents. We also thank E. Munro for the iMyo-YFP and Bra>iMyo-mScarlet constructs. This research was supported by the Scientific Service Units of the Institute of Science and Technology Austria through resources provided by the Electron Microscopy Facility, Imaging and Optics Facility and the Nanofabrication Facility. This work was supported by a Joint Project Grant from the FWF (I 3601-B27).
Acknowledged SSUs
Volume
20
Page
310-321
ISSN
eISSN
IST-REx-ID
Cite this
Caballero Mancebo S, Shinde R, Bolger-Munro M, et al. Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization. Nature Physics. 2024;20:310-321. doi:10.1038/s41567-023-02302-1
Caballero Mancebo, S., Shinde, R., Bolger-Munro, M., Peruzzo, M., Szep, G., Steccari, I., … Heisenberg, C.-P. J. (2024). Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization. Nature Physics. Springer Nature. https://doi.org/10.1038/s41567-023-02302-1
Caballero Mancebo, Silvia, Rushikesh Shinde, Madison Bolger-Munro, Matilda Peruzzo, Gregory Szep, Irene Steccari, David Labrousse Arias, et al. “Friction Forces Determine Cytoplasmic Reorganization and Shape Changes of Ascidian Oocytes upon Fertilization.” Nature Physics. Springer Nature, 2024. https://doi.org/10.1038/s41567-023-02302-1.
S. Caballero Mancebo et al., “Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization,” Nature Physics, vol. 20. Springer Nature, pp. 310–321, 2024.
Caballero Mancebo S, Shinde R, Bolger-Munro M, Peruzzo M, Szep G, Steccari I, Labrousse Arias D, Zheden V, Merrin J, Callan-Jones A, Voituriez R, Heisenberg C-PJ. 2024. Friction forces determine cytoplasmic reorganization and shape changes of ascidian oocytes upon fertilization. Nature Physics. 20, 310–321.
Caballero Mancebo, Silvia, et al. “Friction Forces Determine Cytoplasmic Reorganization and Shape Changes of Ascidian Oocytes upon Fertilization.” Nature Physics, vol. 20, Springer Nature, 2024, pp. 310–21, doi:10.1038/s41567-023-02302-1.
All files available under the following license(s):
Creative Commons Attribution 4.0 International Public License (CC-BY 4.0):
Main File(s)
File Name
Access Level
Open Access
Date Uploaded
2024-07-16
MD5 Checksum
7891ebe7c900ae47469ab127031dd1ec
External material:
Press Release
Description
News on ISTA Website
Export
Marked PublicationsOpen Data ISTA Research Explorer
Sources
PMID: 38370025
PubMed | Europe PMC