A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers

Qiu, Yuqing; Nguyen, Michael; Hocky, Glen M.; Dinner, Aaron R.; Vaikuntanathan, Suriyanarayanan

doi:10.1073/pnas.2102881118

Cited by 6 publications

(3 citation statements)

References 42 publications

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“…We established the so-called Onsager matrix 𝐿 50,51 (Methods). In Onsager's theory, when the system is near equilibrium, there is a linear force-flux relationship [52][53][54] , based on which the Onsager matrix is constructed via 𝒥 = 𝐿 • ℱ with equal off-diagonal coefficients, i.e., 𝐿 𝐴𝐵 = 𝐿 𝐵𝐴 (𝐴 ≠ 𝐵), making 𝐿 symmetric. In our case, we have three signals (𝑅, 𝐹, and 𝒗 𝑐 ), so 𝐿 is a 3×3 matrix.…”

Section: Onsager Reciprocity Suggests Energy Partitioning In a Fixed ...mentioning

confidence: 99%

Energy partitioning in the cell cortex

Chen,

Seara,

Michaud

et al. 2024

Preprint

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Living systems are driven far from thermodynamic equilibrium through the continuous consumption of ambient energy (1). In the cell cortex, this energy is invested in the formation of diverse patterns in chemical and mechanical activities, whose unique spatial and temporal dynamics determine cell phenotypes and behaviors (2-6). However, how cells partition internal energy between chemical and mechanical work is unknown (7-9). Here we measured the entropy production rate (EPR) of both the chemical and mechanical subsystems of the cell cortex across a broad range of periodic patterns as the system is driven further from equilibrium via manipulation of the Rho GTPase pathway, which controls cortical actin filaments (F-actin) and myosin-II. We find that at lower levels of Rho GAP (GTPase activating protein) expression, which produce pulses or "choppy" Rho and F-actin waves, energy is comparably partitioned between the chemical and mechanical subsystems and is subject to the constraint of Onsager reciprocity. Within the range of reciprocity, the EPR is maximized in choppy waves that resemble the waves associated with cell division3,10. However, as the cortex is driven even further from equilibrium into elaborate labyrinthine or spiral traveling wave trains via increased GAP expression, reciprocity is broken, marking an increasingly differential partitioning of energy and an uncoupling of chemical and mechanical activities. We further demonstrate that energy partitioning and reciprocity are determined by the competition between the timescales of chemical reaction and mechanical relaxation. These results indicate that even within coupled cellular subsystems, both the relative proportions of energy partitioned to each subsystem and the ultimate phenotypic outcome vary dramatically as a function of the overall energy investment.

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Section: Onsager Reciprocity Suggests Energy Partitioning In a Fixed ...mentioning

confidence: 99%

Energy partitioning in the cell cortex

Chen,

Seara,

Michaud

et al. 2024

Preprint

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“…We show that a thermodynamic analysis of the nonequilibrium driving forces in the model is sufficient to bound the load response of the system. Previous work has investigated thermodynamic relationships between driving forces and resulting configurations in polymer-like self-assembly systems [20, 21]. This previous work explored simpler systems, but we expand the framework to describe the dynamics of branched network assembly.…”

Section: Introductionmentioning

confidence: 99%

A thermodynamic framework for nonequilibrium self-assembly and force morphology tradeoffs in branched actin networks

Rennert,

Vaikuntanathan

2023

Preprint

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Branched actin networks are involved in a variety of cellular processes, most notably the formation of lamellipodia in the leading edge of the cell. These systems adapt to varying loads through force dependant assembly rates that allow the network density and material properties to be modulated. Recent experimental work has described growth and force feedback mechanisms in these systems. We seek to create a minimal model of this nonequilibrium self assembly process incorporating these mechanisms. Our results will show how constraints from stochastic thermodynamics and non-equilibrium thermodynamics may bound or constrain the structures that result in such processes. This will allow us to develop a minimal yet predictive thermodynamic framework for these kinds of force generating processes.

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“…The actin cytoskeleton is a paradigmatic example of an adaptive biomaterial that regulates important biophysical properties of the cell, such as its structural integrity, motility, and signaling, by adopting various nonequilibrium morphologies [1][2][3]. While there have been many efforts to unravel the driving forces responsible for sustaining many of these structures [1,[4][5][6][7][8][9], a clear thermodynamic understanding of the underlying principles governing their adaptive properties has remained elusive [10]. Here, using tools from large deviation theory [11], we provide evidence that a nonequilibrium thermodynamic control framework can indeed predict and rationalize adaptive structural transitions in cytoskeletal networks.…”

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confidence: 99%

Thermodynamic Control of Activity Patterns in Cytoskeletal Networks

et al. 2022

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Biological materials, such as the actin cytoskeleton, exhibit remarkable structural adaptability to various external stimuli by consuming different amounts of energy. In this Letter, we use methods from large deviation theory to identify a thermodynamic control principle for structural transitions in a model cytoskeletal network. Specifically, we demonstrate that biasing the dynamics with respect to the work done by nonequilibrium components effectively renormalizes the interaction strength between such components, which can eventually result in a morphological transition. Our work demonstrates how a thermodynamic quantity can be used to renormalize effective interactions, which in turn can tune structure in a predictable manner, suggesting a thermodynamic principle for the control of cytoskeletal structure and dynamics.

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A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers

Cited by 6 publications

References 42 publications

Energy partitioning in the cell cortex

Energy partitioning in the cell cortex

A thermodynamic framework for nonequilibrium self-assembly and force morphology tradeoffs in branched actin networks

Thermodynamic Control of Activity Patterns in Cytoskeletal Networks

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