Epithelial cell chirality emerges through the dynamic concentric pattern of actomyosin cytoskeleton
- RIKEN Center for Biosystems Dynamics Research, Japan
- Kyushu University, Japan
Abstract
The chirality of tissues and organs is essential for their proper function and development. Tissue-level chirality derives from the chirality of individual cells that comprise the tissue, and cellular chirality is considered to emerge through the organization of chiral molecules within the cell. However, the principle of how molecular chirality leads to cellular chirality remains unresolved. To address this fundamental question, we experimentally studied the chiral behaviors of isolated epithelial cells derived from a carcinoma line and developed a theoretical understanding of how their behaviors arise from molecular-level chirality. We first found that the nucleus undergoes clockwise rotation, accompanied by robust cytoplasmic circulation in the same direction. During the rotation, actin and Myosin IIA assemble into the stress fibers with a vortex-like chiral orientation at the ventral side of the cell periphery, concurrently forming a concentric pattern at the dorsal side. Further analysis revealed that the intracellular rotation is driven by the concentric actomyosin filaments located dorsally, not by the ventral vortex-like chiral stress fibers. To elucidate how these concentric actomyosin filaments induce chiral rotation, we analyzed a theoretical model developed based on the theory of active chiral fluid. This model demonstrated that the observed cell-scale unidirectional rotation is driven by the molecular-scale chirality of actomyosin filaments even in the absence of cell-scale chiral orientational order. Our study thus provides novel mechanistic insights into how the molecular chirality is organized into the cellular chirality, representing an important step towards understanding left-right symmetry breaking in tissues and organs.
Data availability
Source data for all graphs and original code for the numerical integration of the model have been deposited and is publicly available at https://doi.org/10.5281/zenodo.8254364.
Article and author information
Author details
Masatoshi Takeichi
Funding
Japan Society for the Promotion of Science (19K16096)
- Takaki Yamamoto
Japan Society for the Promotion of Science (23K14186)
- Tomoki Ishibashi
Japan Society for the Promotion of Science (22H05170)
- Tatsuo Shibata
Japan Society for the Promotion of Science (23H02455)
- Tatsuo Shibata
Core Research for Evolutional Science and Technology (JPMJCR1852)
- Tatsuo Shibata
RIKEN Center for Biosystems Dynamics Research
- Tatsuo Shibata
Japan Society for the Promotion of Science (18J01239)
- Takaki Yamamoto
Japan Society for the Promotion of Science (22KJ3145)
- Tomoki Ishibashi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2025, Yamamoto et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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Epithelial cell chirality emerges through the dynamic concentric pattern of actomyosin cytoskeleton
eLife 14:e102296.
https://doi.org/10.7554/eLife.102296
