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Title: Adaptive nonequilibrium design of actin-based metamaterials: Fundamental and practical limits of control

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
ORCiD logo [1];  [1];  [1]; ORCiD logo [2]
  1. Department of Chemistry, Stanford University, Stanford, CA 94305
  2. Department of Chemistry, Stanford University, Stanford, CA 94305, Institute for Computational and Mathematical Engineering, Stanford University, Stanford, CA 94305

The adaptive and surprising emergent properties of biological materials self-assembled in far-from-equilibrium environments serve as an inspiration for efforts to design nanomaterials. In particular, controlling the conditions of self-assembly can modulate material properties, but there is no systematic understanding of either how to parameterize external control or how controllable a given material can be. Here, we demonstrate that branched actin networks can be encoded with metamaterial properties by dynamically controlling the applied force under which they grow and that the protocols can be selected using multi-task reinforcement learning. These actin networks have tunable responses over a large dynamic range depending on the chosen external protocol, providing a pathway to encoding “memory” within these structures. Interestingly, we obtain a bound that relates the dissipation rate and the rate of “encoding” that gives insight into the constraints on control—both physical and information theoretical. Taken together, these results emphasize the utility and necessity of nonequilibrium control for designing self-assembled nanostructures.

Sponsoring Organization:
USDOE
Grant/Contract Number:
SC0022917
OSTI ID:
2305554
Alternate ID(s):
OSTI ID: 2472118
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 8 Vol. 121; ISSN 0027-8424
Publisher:
Proceedings of the National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (57)

Cellular Motility Driven by Assembly and Disassembly of Actin Filaments journal February 2003
Allostery of actin filaments: Molecular dynamics simulations and coarse-grained analysis journal August 2005
MEDYAN: Mechanochemical Simulations of Contraction and Polarity Alignment in Actomyosin Networks journal April 2016
Two competing orientation patterns explain experimentally observed anomalies in growing actin networks journal March 2010
The Principle of Independent Bond-Level Response: Tuning by Pruning to Exploit Disorder for Global Behavior journal June 2015
Thermodynamic Control of Activity Patterns in Cytoskeletal Networks journal September 2022
Thermodynamic Metrics and Optimal Paths journal May 2012
Plastic Deformation and Fragmentation of Strained Actin Filaments journal August 2019
Loading history determines the velocity of actin-network growth journal November 2005
Molecular Transport Modulates the Adaptive Response of Branched Actin Networks to an External Force journal September 2013
Geometric approach to optimal nonequilibrium control: Minimizing dissipation in nanomagnetic spin systems journal January 2017
Reversible stress softening of actin networks journal January 2007
Total Internal Reflection Fluorescence (TIRF) Microscopy journal August 2022
Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells journal January 2006
Inferring dissipation from current fluctuations journal April 2017
Cellular motions and thermal fluctuations: the Brownian ratchet journal July 1993
Quantifying Dissipation in Actomyosin Networks journal February 2019
Nonequilibrium detailed fluctuation theorem for repeated discrete feedback journal December 2010
Force Generation by Actin Polymerization II: The Elastic Ratchet and Tethered Filaments journal March 2003
The molecular mechanism of load adaptation by branched actin networks journal June 2022
Load fluctuations drive actin network growth journal October 2007
A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers journal September 2021
Associative Pattern Recognition Through Macro-molecular Self-Assembly journal April 2017
Mechanical Integration of Actin and Adhesion Dynamics in Cell Migration journal November 2010
Unified, Geometric Framework for Nonequilibrium Protocol Optimization journal March 2023
Thermodynamic Geometry of Microscopic Heat Engines journal January 2020
Polymer Motors: Pushing out the Front and Pulling up the Back journal September 2003
Understanding cytoskeletal avalanches using mechanical stability analysis journal October 2021
Active Biological Materials journal May 2009
Communication: Dominance of extreme statistics in a prototype many-body Brownian ratchet journal October 2014
Cell Mechanics: Integrating Cell Responses to Mechanical Stimuli journal August 2007
Probing the theoretical and computational limits of dissipative design journal November 2021
Cell motility driven by actin polymerization journal December 1996
Design principles for nonequilibrium self-assembly journal November 2016
Nonlinear elasticity in biological gels journal May 2005
Thermodynamic Uncertainty Relation for Biomolecular Processes journal April 2015
Inverse design of discrete mechanical metamaterials journal September 2019
Elasticity of Semiflexible Biopolymer Networks journal December 1995
Designing self-assembling kinetics with differentiable statistical physics models journal March 2021
Thermodynamics of information journal February 2015
Optimization of non-equilibrium self-assembly protocols using Markov state models journal December 2022
Regulation of Actin Filament Assembly by Arp2/3 Complex and Formins journal June 2007
Force Feedback Controls Motor Activity and Mechanical Properties of Self-Assembling Branched Actin Networks journal January 2016
Membrane-induced bundling of actin filaments journal August 2008
The Statistical Mechanics of Dynamic Pathways to Self-Assembly journal April 2015
Designing allostery-inspired response in mechanical networks journal February 2017
Minimum energetic cost to maintain a target nonequilibrium state journal April 2017
Dissipation Bounds All Steady-State Current Fluctuations journal March 2016
Tissue Cells Feel and Respond to the Stiffness of Their Substrate journal November 2005
Self-organization of a propulsive actin network as an evolutionary process journal September 2001
Self-organization of actin filament orientation in the dendritic-nucleation/array-treadmilling model journal April 2007
A Versatile Framework for Simulating the Dynamic Mechanical Structure of Cytoskeletal Networks journal July 2017
Actin, a Central Player in Cell Shape and Movement journal November 2009
The Cytoskeleton and Cell Signaling: Component Localization and Mechanical Coupling journal January 1998
Nonequilibrium thermodynamics of feedback control journal February 2012
Actin filament alignment causes mechanical hysteresis in cross-linked networks journal January 2021
Structure of Arp2/3 complex at a branched actin filament junction resolved by single-particle cryo-electron microscopy journal May 2022