Global tissue tension anisotropy has been shown to trigger stereotypical cell division orientation by elongating mitotic cells along the main tension axis. Yet, how tissue tension elongates mitotic cells despite those cells undergoing mitotic rounding (MR) by globally upregulating cortical actomyosin tension remains unclear. We addressed this question by taking advantage of ascidian embryos, consisting of a small number of interphasic and mitotic blastomeres and displaying an invariant division pattern. We found that blastomeres undergo MR by locally relaxing cortical tension at their apex, thereby allowing extrinsic pulling forces from neighboring interphasic blastomeres to polarize their shape and thus division orientation. Consistently, interfering with extrinsic forces by reducing the contractility of interphasic blastomeres or disrupting the establishment of asynchronous mitotic domains leads to aberrant mitotic cell division orientations. Thus, apical relaxation during MR constitutes a key mechanism by which tissue tension anisotropy controls stereotypical cell division orientation.
We thank members of the Heisenberg and McDougall groups for technical advice and discussion, Hitoyoshi Yasuo for sharing lab equipment, Lucas Leclère and Hitoyoshi Yasuo for their comments on a preliminary version of the manuscript, and Philippe Dru for the Rose plots. We are grateful to the Bioimaging and Nanofabrication facilities of IST Austria and the Imaging Platform (PIM) and animal facility (CRB) of Institut de la Mer de Villefranche (IMEV), which is supported by EMBRC-France, whose French state funds are managed by the ANR within the Investments of the Future program under reference ANR-10-INBS-0, for continuous support. This work was supported by a grant from the French Government funding agency Agence National de la Recherche (ANR “MorCell”: ANR-17-CE 13-002 8).
Godard BG, Dumollard R, Munro E, et al. Apical relaxation during mitotic rounding promotes tension-oriented cell division. Developmental Cell. 2020;55(6):695-706. doi:10.1016/j.devcel.2020.10.016
Godard, B. G., Dumollard, R., Munro, E., Chenevert, J., Hebras, C., Mcdougall, A., & Heisenberg, C.-P. J. (2020). Apical relaxation during mitotic rounding promotes tension-oriented cell division. Developmental Cell. Elsevier. https://doi.org/10.1016/j.devcel.2020.10.016
Godard, Benoit G, Rémi Dumollard, Edwin Munro, Janet Chenevert, Céline Hebras, Alex Mcdougall, and Carl-Philipp J Heisenberg. “Apical Relaxation during Mitotic Rounding Promotes Tension-Oriented Cell Division.” Developmental Cell. Elsevier, 2020. https://doi.org/10.1016/j.devcel.2020.10.016.
B. G. Godard et al., “Apical relaxation during mitotic rounding promotes tension-oriented cell division,” Developmental Cell, vol. 55, no. 6. Elsevier, pp. 695–706, 2020.
Godard BG, Dumollard R, Munro E, Chenevert J, Hebras C, Mcdougall A, Heisenberg C-PJ. 2020. Apical relaxation during mitotic rounding promotes tension-oriented cell division. Developmental Cell. 55(6), 695–706.
Godard, Benoit G., et al. “Apical Relaxation during Mitotic Rounding Promotes Tension-Oriented Cell Division.” Developmental Cell, vol. 55, no. 6, Elsevier, 2020, pp. 695–706, doi:10.1016/j.devcel.2020.10.016.
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