Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue

Sahu P, Schwarz JM, Manning ML. 2021. Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue. New Journal of Physics. 23(9), 093043.

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Author
Sahu, PreetiISTA; Schwarz, J. M.; Manning, M. Lisa
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Abstract
In dense biological tissues, cell types performing different roles remain segregated by maintaining sharp interfaces. To better understand the mechanisms for such sharp compartmentalization, we study the effect of an imposed heterotypic tension at the interface between two distinct cell types in a fully 3D Voronoi model for confluent tissues. We find that cells rapidly sort and self-organize to generate a tissue-scale interface between cell types, and cells adjacent to this interface exhibit signature geometric features including nematic-like ordering, bimodal facet areas, and registration, or alignment, of cell centers on either side of the two-tissue interface. The magnitude of these features scales directly with the magnitude of the imposed tension, suggesting that biologists can estimate the magnitude of tissue surface tension between two tissue types simply by segmenting a 3D tissue. To uncover the underlying physical mechanisms driving these geometric features, we develop two minimal, ordered models using two different underlying lattices that identify an energetic competition between bulk cell shapes and tissue interface area. When the interface area dominates, changes to neighbor topology are costly and occur less frequently, which generates the observed geometric features.
Publishing Year
Date Published
2021-09-29
Journal Title
New Journal of Physics
Acknowledgement
We thank Paula Sanematsu, Matthias Merkel, Daniel Sussman, Cristina Marchetti and Edouard Hannezo for helpful discussions, and M Merkel for developing and sharing the original version of the 3D Voronoi code. This work was primarily funded by NSF-PHY-1607416, NSF-PHY-2014192 , and are in the division of physics at the National Science Foundation. PS and MLM acknowledge additional support from Simons Grant No. 454947.
Volume
23
Issue
9
Article Number
093043
eISSN
IST-REx-ID

Cite this

Sahu P, Schwarz JM, Manning ML. Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue. New Journal of Physics. 2021;23(9). doi:10.1088/1367-2630/ac23f1
Sahu, P., Schwarz, J. M., & Manning, M. L. (2021). Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue. New Journal of Physics. IOP Publishing. https://doi.org/10.1088/1367-2630/ac23f1
Sahu, Preeti, J. M. Schwarz, and M. Lisa Manning. “Geometric Signatures of Tissue Surface Tension in a Three-Dimensional Model of Confluent Tissue.” New Journal of Physics. IOP Publishing, 2021. https://doi.org/10.1088/1367-2630/ac23f1.
P. Sahu, J. M. Schwarz, and M. L. Manning, “Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue,” New Journal of Physics, vol. 23, no. 9. IOP Publishing, 2021.
Sahu P, Schwarz JM, Manning ML. 2021. Geometric signatures of tissue surface tension in a three-dimensional model of confluent tissue. New Journal of Physics. 23(9), 093043.
Sahu, Preeti, et al. “Geometric Signatures of Tissue Surface Tension in a Three-Dimensional Model of Confluent Tissue.” New Journal of Physics, vol. 23, no. 9, 093043, IOP Publishing, 2021, doi:10.1088/1367-2630/ac23f1.
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