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Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis

Mechanical forces are critical for the emergence of diverse three-dimensional morphologies of multicellular systems. However, it remains unclear what kind of mechanical parameters at cellular level substantially contribute to tissue morphologies. This is largely due to technical limitations of live...

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Autores principales: Koyama, Hiroshi, Okumura, Hisashi, Ito, Atsushi M., Nakamura, Kazuyuki, Otani, Tetsuhisa, Kato, Kagayaki, Fujimori, Toshihiko
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434874/
https://www.ncbi.nlm.nih.gov/pubmed/37549166
http://dx.doi.org/10.1371/journal.pcbi.1011306
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author Koyama, Hiroshi
Okumura, Hisashi
Ito, Atsushi M.
Nakamura, Kazuyuki
Otani, Tetsuhisa
Kato, Kagayaki
Fujimori, Toshihiko
author_facet Koyama, Hiroshi
Okumura, Hisashi
Ito, Atsushi M.
Nakamura, Kazuyuki
Otani, Tetsuhisa
Kato, Kagayaki
Fujimori, Toshihiko
author_sort Koyama, Hiroshi
collection PubMed
description Mechanical forces are critical for the emergence of diverse three-dimensional morphologies of multicellular systems. However, it remains unclear what kind of mechanical parameters at cellular level substantially contribute to tissue morphologies. This is largely due to technical limitations of live measurements of cellular forces. Here we developed a framework for inferring and modeling mechanical forces of cell–cell interactions. First, by analogy to coarse-grained models in molecular and colloidal sciences, we approximated cells as particles, where mean forces (i.e. effective forces) of pairwise cell–cell interactions are considered. Then, the forces were statistically inferred by fitting the mathematical model to cell tracking data. This method was validated by using synthetic cell tracking data resembling various in vivo situations. Application of our method to the cells in the early embryos of mice and the nematode Caenorhabditis elegans revealed that cell–cell interaction forces can be written as a pairwise potential energy in a manner dependent on cell–cell distances. Importantly, the profiles of the pairwise potentials were quantitatively different among species and embryonic stages, and the quantitative differences correctly described the differences of their morphological features such as spherical vs. distorted cell aggregates, and tightly vs. non-tightly assembled aggregates. We conclude that the effective pairwise potential of cell–cell interactions is a live measurable parameter whose quantitative differences can be a parameter describing three-dimensional tissue morphologies.
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spelling pubmed-104348742023-08-18 Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis Koyama, Hiroshi Okumura, Hisashi Ito, Atsushi M. Nakamura, Kazuyuki Otani, Tetsuhisa Kato, Kagayaki Fujimori, Toshihiko PLoS Comput Biol Research Article Mechanical forces are critical for the emergence of diverse three-dimensional morphologies of multicellular systems. However, it remains unclear what kind of mechanical parameters at cellular level substantially contribute to tissue morphologies. This is largely due to technical limitations of live measurements of cellular forces. Here we developed a framework for inferring and modeling mechanical forces of cell–cell interactions. First, by analogy to coarse-grained models in molecular and colloidal sciences, we approximated cells as particles, where mean forces (i.e. effective forces) of pairwise cell–cell interactions are considered. Then, the forces were statistically inferred by fitting the mathematical model to cell tracking data. This method was validated by using synthetic cell tracking data resembling various in vivo situations. Application of our method to the cells in the early embryos of mice and the nematode Caenorhabditis elegans revealed that cell–cell interaction forces can be written as a pairwise potential energy in a manner dependent on cell–cell distances. Importantly, the profiles of the pairwise potentials were quantitatively different among species and embryonic stages, and the quantitative differences correctly described the differences of their morphological features such as spherical vs. distorted cell aggregates, and tightly vs. non-tightly assembled aggregates. We conclude that the effective pairwise potential of cell–cell interactions is a live measurable parameter whose quantitative differences can be a parameter describing three-dimensional tissue morphologies. Public Library of Science 2023-08-07 /pmc/articles/PMC10434874/ /pubmed/37549166 http://dx.doi.org/10.1371/journal.pcbi.1011306 Text en © 2023 Koyama et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Koyama, Hiroshi
Okumura, Hisashi
Ito, Atsushi M.
Nakamura, Kazuyuki
Otani, Tetsuhisa
Kato, Kagayaki
Fujimori, Toshihiko
Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title_full Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title_fullStr Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title_full_unstemmed Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title_short Effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
title_sort effective mechanical potential of cell–cell interaction explains three-dimensional morphologies during early embryogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10434874/
https://www.ncbi.nlm.nih.gov/pubmed/37549166
http://dx.doi.org/10.1371/journal.pcbi.1011306
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