Journal Article

Three-dimensional chiral morphodynamics of chemomechanical active shells

Yin, Sifan, Li, Bo, Feng, Xi-Qiao

2022

Overview

SignificanceBiological morphogenesis involves rich symmetry-breaking events and orchestrated morphodynamics where chemical signaling and mechanical deformation are coupled. We propose a chemomechanical active elastic shell theory, which incorporates biochemical reaction–diffusion with mechanical feedback, to study the three-dimensional (3D) chiral pattern formation and evolution of the cell cortex. We show that the activity-driven chemomechanical bifurcations result in the formation of spiral waves, oscillations, traveling waves, and standing waves, accompanied by 3D large deformation. Our study demonstrates the significance of chemomechanical coupling in modulating pattern dynamics of cells and also provides a theoretical framework to explore 3D chemomechanical morphogenesis of other shell-like multicellular structures such as epithelial sheets, blastospheres, and organoids. 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.

• Publisher: National Academy of Sciences
• Subject: Actin Cytoskeleton / Actomyosin / Bifurcations / Biochemistry / Biophysics and Computational Biology / Broken symmetry / Cell Differentiation / Chemical Phenomena / Chemistry, Physical / Deformation / Elastic shells / Embryogenesis / Embryonic growth stage / Feedback / Morphogenesis / Oscillations / Physical Sciences / RhoA protein / Shell theory / Shells / Standing waves