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

Abstract

Understanding the role of nonequilibrium driving in self-organization is crucial for developing a predictive description of biological systems, yet it is impeded by their complexity. The actin cytoskeleton serves as a paradigm for how equilibrium and nonequilibrium forces combine to give rise to self-organization. Motivated by recent experiments that show that actin filament growth rates can tune the morphology of a growing actin bundle cross-linked by two competing types of actin-binding proteins [S. L. Freedman et al., Proc. Natl. Acad. Sci. U.S.A. 116, 16192–16197 (2019)], we construct a minimal model for such a system and show that the dynamics of a growing actin bundle are subject to a set of thermodynamic constraints that relate its nonequilibrium driving, morphology, and molecular fluxes. The thermodynamic constraints reveal the importance of correlations between these molecular fluxes and offer a route to estimating microscopic driving forces from microscopy experiments.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1];  [1]
  1. James Franck Institute, University of Chicago, Chicago, IL 60637,, Department of Chemistry, University of Chicago, Chicago, IL 60637,
  2. Department of Chemistry, New York University, New York, NY 10003
Publication Date:
Research Org.:
Univ. of Chicago, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1821015
Alternate Identifier(s):
OSTI ID: 1853394
Grant/Contract Number:  
SC0019765; R35 GM138312.; R35 GM136381
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 118 Journal Issue: 38; Journal ID: ISSN 0027-8424
Publisher:
Proceedings of the National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Science & Technology - Other Topics; fluctuation–response relations; microscopic nonequilibrium driving; stochastic thermodynamics; actin bundling and growth

Citation Formats

Qiu, Yuqing, Nguyen, Michael, Hocky, Glen M., Dinner, Aaron R., and Vaikuntanathan, Suriyanarayanan. A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers. United States: N. p., 2021. Web. doi:10.1073/pnas.2102881118.
Qiu, Yuqing, Nguyen, Michael, Hocky, Glen M., Dinner, Aaron R., & Vaikuntanathan, Suriyanarayanan. A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers. United States. https://doi.org/10.1073/pnas.2102881118
Qiu, Yuqing, Nguyen, Michael, Hocky, Glen M., Dinner, Aaron R., and Vaikuntanathan, Suriyanarayanan. Mon . "A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers". United States. https://doi.org/10.1073/pnas.2102881118.
@article{osti_1821015,
title = {A strong nonequilibrium bound for sorting of cross-linkers on growing biopolymers},
author = {Qiu, Yuqing and Nguyen, Michael and Hocky, Glen M. and Dinner, Aaron R. and Vaikuntanathan, Suriyanarayanan},
abstractNote = {Understanding the role of nonequilibrium driving in self-organization is crucial for developing a predictive description of biological systems, yet it is impeded by their complexity. The actin cytoskeleton serves as a paradigm for how equilibrium and nonequilibrium forces combine to give rise to self-organization. Motivated by recent experiments that show that actin filament growth rates can tune the morphology of a growing actin bundle cross-linked by two competing types of actin-binding proteins [S. L. Freedman et al., Proc. Natl. Acad. Sci. U.S.A. 116, 16192–16197 (2019)], we construct a minimal model for such a system and show that the dynamics of a growing actin bundle are subject to a set of thermodynamic constraints that relate its nonequilibrium driving, morphology, and molecular fluxes. The thermodynamic constraints reveal the importance of correlations between these molecular fluxes and offer a route to estimating microscopic driving forces from microscopy experiments.},
doi = {10.1073/pnas.2102881118},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 38,
volume = 118,
place = {United States},
year = {Mon Sep 13 00:00:00 EDT 2021},
month = {Mon Sep 13 00:00:00 EDT 2021}
}

Journal Article:
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https://doi.org/10.1073/pnas.2102881118

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Works referenced in this record:

Speed, dissipation, and error in kinetic proofreading
journal, July 2012

  • Murugan, Arvind; Huse, David A.; Leibler, Stanislas
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 30
  • DOI: 10.1073/pnas.1119911109

Kinetics and thermodynamics of first-order Markov chain copolymerization
journal, July 2014

  • Gaspard, P.; Andrieux, D.
  • The Journal of Chemical Physics, Vol. 141, Issue 4
  • DOI: 10.1063/1.4890821

Nonequilibrium correlations in minimal dynamical models of polymer copying
journal, January 2019

  • Poulton, Jenny M.; ten Wolde, Pieter Rein; Ouldridge, Thomas E.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 6
  • DOI: 10.1073/pnas.1808775116

Mechanical and kinetic factors drive sorting of F-actin cross-linkers on bundles
journal, July 2019

  • Freedman, Simon L.; Suarez, Cristian; Winkelman, Jonathan D.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 33
  • DOI: 10.1073/pnas.1820814116

Internal stress in kinetically trapped actin bundle networks
journal, January 2008

  • Schmoller, Kurt M.; Lieleg, Oliver; Bausch, Andreas R.
  • Soft Matter, Vol. 4, Issue 12
  • DOI: 10.1039/b808582j

Mechanically tuning actin filaments to modulate the action of actin-binding proteins
journal, February 2021


F-Actin Cytoskeleton Network Self-Organization Through Competition and Cooperation
journal, October 2020


Thermodynamic Uncertainty Relation for Biomolecular Processes
journal, April 2015


Robust oscillations in multi-cyclic Markov state models of biochemical clocks
journal, February 2020

  • del Junco, Clara; Vaikuntanathan, Suriyanarayanan
  • The Journal of Chemical Physics, Vol. 152, Issue 5
  • DOI: 10.1063/1.5143259

Force Feedback Controls Motor Activity and Mechanical Properties of Self-Assembling Branched Actin Networks
journal, January 2016


Entropy Production along a Stochastic Trajectory and an Integral Fluctuation Theorem
journal, July 2005


The interplay between activity and filament flexibility determines the emergent properties of active nematics
journal, January 2019

  • Joshi, Abhijeet; Putzig, Elias; Baskaran, Aparna
  • Soft Matter, Vol. 15, Issue 1
  • DOI: 10.1039/C8SM02202J

The free-energy cost of accurate biochemical oscillations
journal, July 2015

  • Cao, Yuansheng; Wang, Hongli; Ouyang, Qi
  • Nature Physics, Vol. 11, Issue 9
  • DOI: 10.1038/nphys3412

Thermodynamic uncertainty relations constrain non-equilibrium fluctuations
journal, November 2019


Design principles for enhancing phase sensitivity and suppressing phase fluctuations simultaneously in biochemical oscillatory systems
journal, April 2018


Models for actin polymerization motors
journal, July 2008


Exact stochastic simulation of coupled chemical reactions
journal, December 1977

  • Gillespie, Daniel T.
  • The Journal of Physical Chemistry, Vol. 81, Issue 25
  • DOI: 10.1021/j100540a008

Forcing cells into shape: the mechanics of actomyosin contractility
journal, July 2015

  • Murrell, Michael; Oakes, Patrick W.; Lenz, Martin
  • Nature Reviews Molecular Cell Biology, Vol. 16, Issue 8
  • DOI: 10.1038/nrm4012

Energy dissipation bounds for autonomous thermodynamic cycles
journal, February 2020

  • Bryant, Samuel J.; Machta, Benjamin B.
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 7
  • DOI: 10.1073/pnas.1915676117

Cell motility driven by actin polymerization
journal, December 1996


Dissipation Bounds All Steady-State Current Fluctuations
journal, March 2016


The role of the Arp2/3 complex in shaping the dynamics and structures of branched actomyosin networks
journal, April 2020

  • Liman, James; Bueno, Carlos; Eliaz, Yossi
  • Proceedings of the National Academy of Sciences, Vol. 117, Issue 20
  • DOI: 10.1073/pnas.1922494117

Nonequilibrium generation of information in copolymerization processes
journal, July 2008

  • Andrieux, D.; Gaspard, P.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 28
  • DOI: 10.1073/pnas.0802049105

Two competing orientation patterns explain experimentally observed anomalies in growing actin networks
journal, March 2010

  • Weichsel, J.; Schwarz, U. S.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 14
  • DOI: 10.1073/pnas.0913730107

Dissipation controls transport and phase transitions in active fluids: mobility, diffusion and biased ensembles
journal, January 2020

  • Fodor, Étienne; Nemoto, Takahiro; Vaikuntanathan, Suriyanarayanan
  • New Journal of Physics, Vol. 22, Issue 1
  • DOI: 10.1088/1367-2630/ab6353

Assembly Mechanism of the Contractile Ring for Cytokinesis by Fission Yeast
journal, December 2007


Self-straining of actively crosslinked microtubule networks
journal, September 2019


High chemical affinity increases the robustness of biochemical oscillations
journal, January 2020


Slow dynamics and internal stress relaxation in bundled cytoskeletal networks
journal, January 2011

  • Lieleg, O.; Kayser, J.; Brambilla, G.
  • Nature Materials, Vol. 10, Issue 3
  • DOI: 10.1038/nmat2939

The nonequilibrium mechanism for ultrasensitivity in a biological switch: Sensing by Maxwell's demons
journal, August 2008


Fascin- and α-Actinin-Bundled Networks Contain Intrinsic Structural Features that Drive Protein Sorting
journal, October 2016

  • Winkelman, Jonathan D.; Suarez, Cristian; Hocky, Glen M.
  • Current Biology, Vol. 26, Issue 20
  • DOI: 10.1016/j.cub.2016.07.080

Actin crosslinker competition and sorting drive emergent GUV size-dependent actin network architecture
journal, September 2021

  • Bashirzadeh, Yashar; Redford, Steven A.; Lorpaiboon, Chatipat
  • Communications Biology, Vol. 4, Issue 1
  • DOI: 10.1038/s42003-021-02653-6

Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity
journal, October 1974


Design principles for nonequilibrium self-assembly
journal, November 2016

  • Nguyen, Michael; Vaikuntanathan, Suriyanarayanan
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 50
  • DOI: 10.1073/pnas.1609983113

Stochastic thermodynamics of single enzymes and molecular motors
journal, March 2011


The energy–speed–accuracy trade-off in sensory adaptation
journal, March 2012

  • Lan, Ganhui; Sartori, Pablo; Neumann, Silke
  • Nature Physics, Vol. 8, Issue 5
  • DOI: 10.1038/nphys2276

Mechanical Integration of Actin and Adhesion Dynamics in Cell Migration
journal, November 2010


Mechanoregulated inhibition of formin facilitates contractile actomyosin ring assembly
journal, September 2017


Active colloids with collective mobility status and research opportunities
journal, January 2017

  • Zhang, Jie; Luijten, Erik; Grzybowski, Bartosz A.
  • Chemical Society Reviews, Vol. 46, Issue 18
  • DOI: 10.1039/C7CS00461C