Three-dimensional geometry controls division symmetry in stem cell colonies

Chaigne A, Smith MB, Cavestany RL, Hannezo EB, Chalut KJ, Paluch EK. 2021. Three-dimensional geometry controls division symmetry in stem cell colonies. Journal of Cell Science. 134(14), jcs255018.

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Journal Article | Published | English

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Author
Chaigne, Agathe; Smith, Matthew B.; Cavestany, R. L.; Hannezo, Edouard IST Austria ; Chalut, Kevin J.; Paluch, Ewa K.
Department
Abstract
Proper control of division orientation and symmetry, largely determined by spindle positioning, is essential to development and homeostasis. Spindle positioning has been extensively studied in cells dividing in two-dimensional (2D) environments and in epithelial tissues, where proteins such as NuMA (also known as NUMA1) orient division along the interphase long axis of the cell. However, little is known about how cells control spindle positioning in three-dimensional (3D) environments, such as early mammalian embryos and a variety of adult tissues. Here, we use mouse embryonic stem cells (ESCs), which grow in 3D colonies, as a model to investigate division in 3D. We observe that, at the periphery of 3D colonies, ESCs display high spindle mobility and divide asymmetrically. Our data suggest that enhanced spindle movements are due to unequal distribution of the cell–cell junction protein E-cadherin between future daughter cells. Interestingly, when cells progress towards differentiation, division becomes more symmetric, with more elongated shapes in metaphase and enhanced cortical NuMA recruitment in anaphase. Altogether, this study suggests that in 3D contexts, the geometry of the cell and its contacts with neighbors control division orientation and symmetry.
Publishing Year
Date Published
2021-07-01
Journal Title
Journal of Cell Science
Acknowledgement
We would like to thank the entire Paluch and Baum laboratories at the MRC-LMCB and the Chalut lab at the Cambridge SCI for discussions and feedback throughout the project, and the MRC-LMCB microscopy platform, in particular Andrew Vaughan, for technical support.
Volume
134
Issue
14
Article Number
jcs255018
ISSN
eISSN
IST-REx-ID

Cite this

Chaigne A, Smith MB, Cavestany RL, Hannezo EB, Chalut KJ, Paluch EK. Three-dimensional geometry controls division symmetry in stem cell colonies. Journal of Cell Science. 2021;134(14). doi:10.1242/jcs.255018
Chaigne, A., Smith, M. B., Cavestany, R. L., Hannezo, E. B., Chalut, K. J., & Paluch, E. K. (2021). Three-dimensional geometry controls division symmetry in stem cell colonies. Journal of Cell Science. The Company of Biologists. https://doi.org/10.1242/jcs.255018
Chaigne, Agathe, Matthew B. Smith, R. L. Cavestany, Edouard B Hannezo, Kevin J. Chalut, and Ewa K. Paluch. “Three-Dimensional Geometry Controls Division Symmetry in Stem Cell Colonies.” Journal of Cell Science. The Company of Biologists, 2021. https://doi.org/10.1242/jcs.255018.
A. Chaigne, M. B. Smith, R. L. Cavestany, E. B. Hannezo, K. J. Chalut, and E. K. Paluch, “Three-dimensional geometry controls division symmetry in stem cell colonies,” Journal of Cell Science, vol. 134, no. 14. The Company of Biologists, 2021.
Chaigne A, Smith MB, Cavestany RL, Hannezo EB, Chalut KJ, Paluch EK. 2021. Three-dimensional geometry controls division symmetry in stem cell colonies. Journal of Cell Science. 134(14), jcs255018.
Chaigne, Agathe, et al. “Three-Dimensional Geometry Controls Division Symmetry in Stem Cell Colonies.” Journal of Cell Science, vol. 134, no. 14, jcs255018, The Company of Biologists, 2021, doi:10.1242/jcs.255018.
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2021-08-23
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