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Three-dimensional chiral morphodynamics of chemomechanical active shells

Morphogenesis of active shells such as cells is a fundamental chemomechanical process that often exhibits three-dimensional (3D) large deformations and chemical pattern dynamics simultaneously. Here, we establish a chemomechanical active shell theory accounting for mechanical feedback and biochemica...

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Autores principales: Yin, Sifan, Li, Bo, Feng, Xi-Qiao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894169/
https://www.ncbi.nlm.nih.gov/pubmed/36442097
http://dx.doi.org/10.1073/pnas.2206159119
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author Yin, Sifan
Li, Bo
Feng, Xi-Qiao
author_facet Yin, Sifan
Li, Bo
Feng, Xi-Qiao
author_sort Yin, Sifan
collection PubMed
description Morphogenesis of active shells such as cells is a fundamental chemomechanical process that often exhibits three-dimensional (3D) large deformations and chemical pattern dynamics simultaneously. Here, we establish a chemomechanical active shell theory accounting for mechanical feedback and biochemical regulation to investigate the symmetry-breaking and 3D chiral morphodynamics emerging in the cell cortex. The active bending and stretching of the elastic shells are regulated by biochemical signals like actomyosin and RhoA, which, in turn, exert mechanical feedback on the biochemical events via deformation-dependent diffusion and inhibition. We show that active deformations can trigger chemomechanical bifurcations, yielding pulse spiral waves and global oscillations, which, with increasing mechanical feedback, give way to traveling or standing waves subsequently. Mechanical feedback is also found to contribute to stabilizing the polarity of emerging patterns, thus ensuring robust morphogenesis. Our results reproduce and unravel the experimentally observed solitary and multiple spiral patterns, which initiate asymmetric cleavage in Xenopus and starfish embryogenesis. This study underscores the crucial roles of mechanical feedback in cell development and also suggests a chemomechanical framework allowing for 3D large deformation and chemical signaling to explore complex morphogenesis in living shell-like structures.
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spelling pubmed-98941692023-05-28 Three-dimensional chiral morphodynamics of chemomechanical active shells Yin, Sifan Li, Bo Feng, Xi-Qiao Proc Natl Acad Sci U S A Physical Sciences Morphogenesis of active shells such as cells is a fundamental chemomechanical process that often exhibits three-dimensional (3D) large deformations and chemical pattern dynamics simultaneously. Here, we establish a chemomechanical active shell theory accounting for mechanical feedback and biochemical regulation to investigate the symmetry-breaking and 3D chiral morphodynamics emerging in the cell cortex. The active bending and stretching of the elastic shells are regulated by biochemical signals like actomyosin and RhoA, which, in turn, exert mechanical feedback on the biochemical events via deformation-dependent diffusion and inhibition. We show that active deformations can trigger chemomechanical bifurcations, yielding pulse spiral waves and global oscillations, which, with increasing mechanical feedback, give way to traveling or standing waves subsequently. Mechanical feedback is also found to contribute to stabilizing the polarity of emerging patterns, thus ensuring robust morphogenesis. Our results reproduce and unravel the experimentally observed solitary and multiple spiral patterns, which initiate asymmetric cleavage in Xenopus and starfish embryogenesis. This study underscores the crucial roles of mechanical feedback in cell development and also suggests a chemomechanical framework allowing for 3D large deformation and chemical signaling to explore complex morphogenesis in living shell-like structures. National Academy of Sciences 2022-11-28 2022-12-06 /pmc/articles/PMC9894169/ /pubmed/36442097 http://dx.doi.org/10.1073/pnas.2206159119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Yin, Sifan
Li, Bo
Feng, Xi-Qiao
Three-dimensional chiral morphodynamics of chemomechanical active shells
title Three-dimensional chiral morphodynamics of chemomechanical active shells
title_full Three-dimensional chiral morphodynamics of chemomechanical active shells
title_fullStr Three-dimensional chiral morphodynamics of chemomechanical active shells
title_full_unstemmed Three-dimensional chiral morphodynamics of chemomechanical active shells
title_short Three-dimensional chiral morphodynamics of chemomechanical active shells
title_sort three-dimensional chiral morphodynamics of chemomechanical active shells
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9894169/
https://www.ncbi.nlm.nih.gov/pubmed/36442097
http://dx.doi.org/10.1073/pnas.2206159119
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