Dynamics of perinuclear actin ring regulating nuclear morphology

• Published in: Applied mathematics and mechanics Vol. 45; no. 8; pp. 1415 - 1428
• Main Authors: Yang, Haoxiang, Sun, Houbo, Shen, Jinghao, Wu, Hao, Jiang, Hongyuan
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01.08.2024; Springer Nature B.V; CAS Key Laboratory of Mechanical Behavior and Design of Materials,Department of Modern Mechanics,University of Science and Technology of China,Hefei 230026,China
• Edition: English ed.
• Subjects: Applications of Mathematics; Assembly; Classical Mechanics; Compressive properties; Depolymerization; Endothelial cells; Fluid- and Aerodynamics; In vivo methods and tests; Mathematical Modeling and Industrial Mathematics; Mathematics; Mathematics and Statistics; Morphology; Partial Differential Equations; Ring structures; Shear flow; Transient response; Q66; 92C42; 92C10; O39; 92C05; compressive stress; actin dynamics; nucleus; mechanical force; perinuclear actin ring
• ISSN: 0253-4827; 1573-2754
• DOI: 10.1007/s10483-024-3129-8

Cells are capable of sensing and responding to the extracellular mechanical microenvironment via the actin skeleton. In vivo, tissues are frequently subject to mechanical forces, such as the rapid and significant shear flow encountered by vascular endothelial cells. However, the investigations about the transient response of intracellular actin networks under these intense external mechanical forces, their intrinsic mechanisms, and potential implications are very limited. Here, we observe that when cells are subject to the shear flow, an actin ring structure could be rapidly assembled at the periphery of the nucleus. To gain insights into the mechanism underlying this perinuclear actin ring assembly, we develop a computational model of actin dynamics. We demonstrate that this perinuclear actin ring assembly is triggered by the depolymerization of cortical actin, Arp2/3-dependent actin filament polymerization, and myosin-mediated actin network contraction. Furthermore, we discover that the compressive stress generated by the perinuclear actin ring could lead to a reduction in the nuclear spreading area, an increase in the nuclear height, and a decrease in the nuclear volume. The present model thus explains the mechanism of the perinuclear actin ring assembly under external mechanical forces and suggests that the spontaneous contraction of this actin structure can significantly impact nuclear morphology.