Three-dimensional chiral morphodynamics of chemomechanical active shells

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 49; p. e2206159119
• Main Authors: Yin, Sifan, Li, Bo, Feng, Xi-Qiao
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 06.12.2022
• Subjects: Actin Cytoskeleton; Actomyosin; Bifurcations; Biochemistry; 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; morphodynamics; active shell; chiral pattern; chemomechanical coupling
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2206159119

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.