An interplay between cytoplasmic flow and cell morphology during cytokinesis simulated by the moving-particle semi-implicit method

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Abstract

Cells are composite mechanical systems: a viscoelastic cytoplasm enclosed by a deformable cell cortex. These two components exchange forces continuously—fluid motion deforms the cortex, and cortical deformation in turn redirects intracellular flow. Yet most cellular mechanics simulations treat either the fluid or the cortex in isolation, leaving their mechanical interplay largely unexplored. To address this gap, we developed a fluid–structure interaction framework based on the moving-particle semi-implicit (MPS) method that solves the coupled dynamics of cytoplasmic flow, internal pressure, and cortical elasticity. We applied this framework to cytokinesis, focusing on how the cleavage plane is positioned. While the mitotic spindle is known to specify the furrow site, prior work has emphasized biochemical cues emanating from the spindle, whereas a direct mechanical cue has been difficult to interrogate. Our simulations show that spindle elongation generates cytoplasmic flows that create a pressure minimum near the spindle midzone; when the cortex is modeled as an elastic shell, this pressure landscape drives a localized cortical invagination at that site. We therefore propose that spindle-driven cytoplasmic flow provides a mechanical positional cue for cleavage-furrow initiation. Author Summary Dividing cells exhibit two contrasting properties: dynamic state changes and the maintenance of homeostasis. During cell division, a dividing cell breaks its identity while successful daughter cells inherit a certain set of its components for survival. Heterogeneous physical properties such as cell shape, cytoplasmic flow, and internal pressure interact to maintain an appropriate range of cellular conditions. The interaction of such physical components is highly dynamic; therefore, simulation studies play an important role in understanding the mechanisms. We constructed a model based on the moving-particle semi-implicit method that recapitulates the behavior of highly dynamic physical objects such as cytoplasmic fluid with practical computational time. The simulation showed that the change in cell shape is caused by internal cell pressure, which is evoked by cytoplasmic flow during elongation of spindle microtubules. The developed simulation platform provided a tool to integrate physical measurements to understand the mechanisms that balance physical dynamics during cell division. Such quantitative simulation combined with the data from molecular or genetic experiments may predict how internal dynamics maintain homeostasis during drastic changes in the cell state.
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Abstract Cells are composite mechanical systems: a viscoelastic cytoplasm enclosed by a deformable cell cortex. These two components exchange forces continuously—fluid motion deforms the cortex, and cortical deformation in turn redirects intracellular flow. Yet most cellular mechanics simulations treat either the fluid or the cortex in isolation, leaving their mechanical interplay largely unexplored. To address this gap, we developed a fluid–structure interaction framework based on the moving-particle semi-implicit (MPS) method that solves the coupled dynamics of cytoplasmic flow, internal pressure, and cortical elasticity. We applied this framework to cytokinesis, focusing on how the cleavage plane is positioned. While the mitotic spindle is known to specify the furrow site, prior work has emphasized biochemical cues emanating from the spindle, whereas a direct mechanical cue has been difficult to interrogate. Our simulations show that spindle elongation generates cytoplasmic flows that create a pressure minimum near the spindle midzone; when the cortex is modeled as an elastic shell, this pressure landscape drives a localized cortical invagination at that site. We therefore propose that spindle-driven cytoplasmic flow provides a mechanical positional cue for cleavage-furrow initiation. Author Summary Dividing cells exhibit two contrasting properties: dynamic state changes and the maintenance of homeostasis. During cell division, a dividing cell breaks its identity while successful daughter cells inherit a certain set of its components for survival. Heterogeneous physical properties such as cell shape, cytoplasmic flow, and internal pressure interact to maintain an appropriate range of cellular conditions. The interaction of such physical components is highly dynamic; therefore, simulation studies play an important role in understanding the mechanisms. We constructed a model based on the moving-particle semi-implicit method that recapitulates the behavior of highly dynamic physical objects such as cytoplasmic fluid with practical computational time. The simulation showed that the change in cell shape is caused by internal cell pressure, which is evoked by cytoplasmic flow during elongation of spindle microtubules. The developed simulation platform provided a tool to integrate physical measurements to understand the mechanisms that balance physical dynamics during cell division. Such quantitative simulation combined with the data from molecular or genetic experiments may predict how internal dynamics maintain homeostasis during drastic changes in the cell state. Competing Interest Statement The authors have declared no competing interest.

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License: CC-BY-4.0