DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: A generalized Flory-Stockmayer kinetic theory of connectivity percolation and rigidity percolation of cytoskeletal networks

Journal Article · · PLoS Computational Biology (Online)
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Rice Univ., Houston, TX (United States). Center for Theoretical Biological Physics; Rice Univ., Houston, TX (United States)
  2. Rice Univ., Houston, TX (United States). Center for Theoretical Biological Physics; Rice Univ., Houston, TX (United States); Univ. of Houston, TX (United States); Pacific Northwest National Lab. (PNNL), Seattle, WA (United States)

Actin networks are essential for living cells to move, reproduce, and sense their environments. The dynamic and rheological behavior of actin networks is modulated by actin-binding proteins such as α-actinin, Arp2/3, and myosin. There is experimental evidence that actin-binding proteins modulate the cooperation of myosin motors by connecting the actin network. In this work, we present an analytical mean field model, using the Flory-Stockmayer theory of gelation, to understand how different actin-binding proteins change the connectivity of the actin filaments as the networks are formed. We follow the kinetics of the networks and estimate the concentrations of actin-binding proteins that are needed to reach connectivity percolation as well as to reach rigidity percolation. We find that Arp2/3 increases the actomyosin connectivity in the network in a non-monotonic way. We also describe how changing the connectivity of actomyosin networks modulates the ability of motors to exert forces, leading to three possible phases of the networks with distinctive dynamical characteristics: a sol phase, a gel phase, and an active phase. Thus, changes in the concentration and activity of actin-binding proteins in cells lead to a phase transition of the actin network, allowing the cells to perform active contraction and change their rheological properties.

Research Organization:
Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
Sponsoring Organization:
USDOE
Grant/Contract Number:
AC05-76RL01830
OSTI ID:
1878293
Report Number(s):
PNNL-SA-168287
Journal Information:
PLoS Computational Biology (Online), Journal Name: PLoS Computational Biology (Online) Journal Issue: 5 Vol. 18; ISSN 1553-7358
Publisher:
Public Library of ScienceCopyright Statement
Country of Publication:
United States
Language:
English

References (63)

The design of MACs (minimal actin cortices) journal October 2013
Turnover versus treadmilling in actin network assembly and remodeling journal October 2019
α-Actinin structure and regulation journal May 2008
Computational Analysis of a Cross-linked Actin-like Network journal October 2007
Rigidity percolation in glassy structures journal November 1985
Affinity of alpha-actinin for actin determines the structure and mechanical properties of actin filament gels journal July 1993
Reconstitution of Contractile Actomyosin Bundles journal June 2011
Lateral Membrane Diffusion Modulated by a Minimal Actin Cortex journal April 2013
A Combination of Actin Treadmilling and Cross-Linking Drives Contraction of Random Actomyosin Arrays journal November 2015
A Versatile Framework for Simulating the Dynamic Mechanical Structure of Cytoskeletal Networks journal July 2017
The cell pushes back: The Arp2/3 complex is a key orchestrator of cellular responses to environmental forces journal February 2021
Architecture and Connectivity Govern Actin Network Contractility journal March 2016
Mechanics of the F-actin cytoskeleton journal January 2010
Resolution of sub-element length scales in Brownian dynamics simulations of biopolymer networks with geometrically exact beam finite elements journal December 2015
Novel Structures for α-Actinin:F-Actin Interactions and their Implications for Actin–Membrane Attachment and Tension Sensing in the Cytoskeleton journal April 2007
Molecular Size Distribution in Three Dimensional Polymers. I. Gelation 1 journal November 1941
Disordered actomyosin networks are sufficient to produce cooperative and telescopic contractility journal August 2016
Assembly kinetics determine the architecture of α-actinin crosslinked F-actin networks journal January 2012
Crosslinked actin networks show liquid crystal elastomer behaviour, including soft-mode elasticity journal March 2007
Forcing cells into shape: the mechanics of actomyosin contractility journal July 2015
Non-equilibrium cytoquake dynamics in cytoskeletal remodeling and stabilization journal January 2016
Force percolation of contractile active gels journal January 2017
Theory of Molecular Size Distribution and Gel Formation in Branched‐Chain Polymers journal February 1943
Gel Formation in Vinyl‐Divinyl Copolymers journal August 1943
The interplay of nonlinearity and architecture in equilibrium cytoskeletal mechanics journal January 2011
Cytoskeletal polymer networks: The molecular structure of cross-linkers determines macroscopic properties journal September 2006
Helical twist controls the thickness of F-actin bundles journal June 2008
Active multistage coarsening of actin networks driven by myosin motors journal May 2011
On the spontaneous collective motion of active matter journal August 2011
Active contractility in actomyosin networks journal April 2012
F-actin buckling coordinates contractility and severing in a biomimetic actomyosin cortex journal December 2012
Actomyosin dynamics drive local membrane component organization in an in vitro active composite layer journal February 2016
Mechanical and kinetic factors drive sorting of F-actin cross-linkers on bundles journal July 2019
Assemblies of calcium/calmodulin-dependent kinase II with actin and their dynamic regulation by calmodulin in dendritic spines journal August 2019
The role of the Arp2/3 complex in shaping the dynamics and structures of branched actomyosin networks journal April 2020
The interaction of Arp2/3 complex with actin: Nucleation, high affinity pointed end capping, and formation of branching networks of filaments journal May 1998
Molecular Mechanism of Fascin Function in Filopodial Formation journal January 2013
Interconversion of structural and contractile actin gels by insertion of myosin during assembly. journal December 1983
Quantifying dissipation in actomyosin networks journal April 2019
Actin and Actin-Binding Proteins journal March 2016
The Actin Cytoskeleton and Actin-Based Motility journal January 2018
Effective-medium theory of percolation on central-force elastic networks. II. Further results journal June 1985
Effective-medium theory of percolation on central-force elastic networks. III. The superelastic problem journal March 1986
Algorithms for three-dimensional rigidity analysis and a first-order percolation transition journal October 2007
Percolation of colloids with distinct interaction sites journal January 2010
Contractile Units in Disordered Actomyosin Bundles Arise from F-Actin Buckling journal June 2012
Rigidity Percolation and Molecular Clustering in Network Glasses journal June 1986
Generic Rigidity Percolation: The Pebble Game journal November 1995
Infinite-Cluster Geometry in Central-Force Networks journal February 1997
Microscopic Theory of Network Glasses journal February 2003
Self-organized stress patterns drive state transitions in actin cortices journal June 2018
Elastic Behavior of Cross-Linked and Bundled Actin Networks journal May 2004
Nonequilibrium Mechanics of Active Cytoskeletal Networks journal January 2007
Actin Network Architecture Can Determine Myosin Motor Activity journal June 2012
Generic phases of cross-linked active gels: Relaxation, oscillation and contractility journal November 2011
Role of cross-links in bundle formation, phase separation and gelation of long filaments journal July 2003
Remarkable structural transformations of actin bundles are driven by their initial polarity, motor activity, crosslinking, and filament treadmilling dataset January 2019
MEDYAN: Mechanochemical Simulations of Contraction and Polarity Alignment in Actomyosin Networks dataset January 2016
MEDYAN: Mechanochemical Simulations of Contraction and Polarity Alignment in Actomyosin Networks journal April 2016
Remarkable structural transformations of actin bundles are driven by their initial polarity, motor activity, crosslinking, and filament treadmilling journal July 2019
A Quantitative Analysis of Contractility in Active Cytoskeletal Protein Networks journal April 2008
Dendritic Actin Cytoskeleton: Structure, Functions, and Regulations journal May 2017
The role of the Arp2/3 complex in shaping the dynamics and structures of branched actomyosin networks dataset January 2020