Salt-Mediated Stiffening, Destruction, and Resculpting of Actomyosin Network

Bekele J. Gurmessa; Michael J. Rust; Moumita Das; Jennifer L. Ross; Rae M. Robertson-Anderson

doi:10.3389/fphy.2021.760340

journal article Open Access Nov 19, 2021

Salt-Mediated Stiffening, Destruction, and Resculpting of Actomyosin Network

Bekele J. Gurmessa Michael J. Rust Moumita Das

Jennifer L. Ross

Rae M. Robertson-Anderson

Frontiers in Physics Vol. 9 · Frontiers Media SA

View at Publisher Save 10.3389/fphy.2021.760340

Abstract

Cells dynamically change their viscoelastic properties by restructuring networks of actin filaments in the cytoskeleton, enabling diverse mechanical processes such as mobility and apoptosis. This restructuring is modulated, in part, by actin-binding proteins, such as myosin II, as well as counterions such as Mg2+ and K+. While high concentrations of Mg2+ can induce bundling and crosslinking of actin filaments, high concentrations of K+ destabilize myosin II minifilaments necessary to crosslink actin filaments. Here, we elucidate how the mechanics and structure of actomyosin networks evolve under competing effects of varying Mg2+ and K+ concentrations. Specifically, we couple microfluidics with optical tweezers microrheology to measure the time-varying linear viscoelastic moduli of actin networks crosslinked via myosin II as we cycle between low and high Mg2+ and K+ concentrations. Our complementary confocal imaging experiments correlate the time-varying viscoelastic properties with salt-mediated structural evolution. We find that the elastic modulus displays an intriguing non-monotonic time dependence in high-salt conditions, that correlates with structural changes, and that this process is irreversible, with the network evolving to a new steady-state as Mg2+ and K+ decrease back to their initial concentrations.

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References

65

[1]

Insall "Actin in 2021" Curr Biol (2021) 10.1016/j.cub.2021.04.013

[2]

Gardel "Chapter 19 Mechanical Response of Cytoskeletal Networks" Methods Cel Biol (2008) 10.1016/s0091-679x(08)00619-5

[3]

Actin Dynamics, Architecture, and Mechanics in Cell Motility

Laurent Blanchoin, Rajaa Boujemaa-Paterski, Cécile Sykes et al.

Physiological Reviews 2014 10.1152/physrev.00018.2013

[4]

Svitkina "The Actin Cytoskeleton and Actin-Based Motility" Cold Spring Harb Perspect Biol (2018) 10.1101/cshperspect.a018267

[5]

Cooper "Structure and Organization of Actin Filaments" (2000)

[6]

Bausch "A Bottom-Up Approach to Cell Mechanics" Nat Phys (2006) 10.1038/nphys260

[7]

Schmoller "Structural and Viscoelastic Properties of Actin/filamin Networks: Cross-Linked versus Bundled Networks" Biophysical J (2009) 10.1016/j.bpj.2009.04.040

[8]

Castaneda "Regulation of Actin Bundle Mechanics and Structure by Intracellular Environmental Factors" Front Phys (2021) 10.3389/fphy.2021.675885

[9]

Lieleg "Structural Polymorphism in Heterogeneous Cytoskeletal Networks" Soft Matter (2009) 10.1039/b814555p

[10]

Tharmann "Viscoelasticity of Isotropically Cross-Linked Actin Networks" Phys Rev Lett (2007) 10.1103/physrevlett.98.088103

[11]

Shin "Bending Stiffness of a Crystalline Actin Bundle" J Mol Biol (2004) 10.1016/j.jmb.2004.01.028

[12]

Lieleg "Mechanics of Bundled Semiflexible Polymer Networks" Phys Rev Lett (2007) 10.1103/physrevlett.99.088102

[13]

Mechanics of the F-actin cytoskeleton

Jonathan Stricker, Tobias Falzone, Margaret L. Gardel

Journal of Biomechanics 2010 10.1016/j.jbiomech.2009.09.003

[14]

Janmey "The Mechanical Properties of Actin Gels. Elastic Modulus and Filament Motions" J Biol Chem (1994) 10.1016/s0021-9258(18)31663-6

[15]

Käs "F-actin, a Model Polymer for Semiflexible Chains in Dilute, Semidilute, and Liquid Crystalline Solutions" Biophysical J (1996) 10.1016/s0006-3495(96)79630-3

[16]

Koenderink "High-frequency Stress Relaxation in Semiflexible Polymer Solutions and Networks" Phys Rev Lett (2006) 10.1103/physrevlett.96.138307

[17]

Liu "Visualizing the Strain Field in Semiflexible Polymer Networks: Strain Fluctuations and Nonlinear Rheology ofF-Actin Gels" Phys Rev Lett (2007) 10.1103/physrevlett.98.198304

[18]

Broedersz "Measurement of Nonlinear Rheology of Cross-Linked Biopolymer Gels" Soft Matter (2010) 10.1039/c0sm00285b

[19]

Claessens "Actin-binding Proteins Sensitively Mediate F-Actin Bundle Stiffness" Nat Mater (2006) 10.1038/nmat1718

[20]

Lieleg "Slow Dynamics and Internal Stress Relaxation in Bundled Cytoskeletal Networks" Nat Mater (2011) 10.1038/nmat2939

[21]

Ideses "Myosin Ii Does it All: Assembly, Remodeling, and Disassembly of Actin Networks Are Governed by Myosin Ii Activity" Soft Matter (2013) 10.1039/c3sm50309g

[22]

Betapudi "Life without Double-Headed Non-muscle Myosin Ii Motor Proteins" Front Chem (2014) 10.3389/fchem.2014.00045

[23]

Soares e Silva "Time-resolved Microrheology of Actively Remodeling Actomyosin Networks" New J Phys (2014) 10.1088/1367-2630/16/7/075010

[24]

Laevsky "Cross-linking of Actin Filaments by Myosin Ii Is a Major Contributor to Cortical Integrity and Cell Motility in Restrictive Environments" J Cel Sci (2003) 10.1242/jcs.00684

[25]

Cross-linker dynamics determine the mechanical properties of actin gels

D.H. Wachsstock, W.H. Schwarz, T.D. Pollard

Biophysical Journal 1994 10.1016/s0006-3495(94)80856-2

[26]

Humphrey "Active Fluidization of Polymer Networks through Molecular Motors" Nature (2002) 10.1038/416413a

[27]

Koenderink "An Active Biopolymer Network Controlled by Molecular Motors" Proc Natl Acad Sci (2009) 10.1073/pnas.0903974106

[28]

Reichl "Interactions between Myosin and Actin Crosslinkers Control Cytokinesis Contractility Dynamics and Mechanics" Curr Biol (2008) 10.1016/j.cub.2008.02.056

[29]

Martens "Softening of the Actin Cytoskeleton by Inhibition of Myosin Ii" Pflugers Arch - Eur J Physiol (2008) 10.1007/s00424-007-0419-8

[30]

Rauzi "Cortical Forces in Cell Shape Changes and Tissue Morphogenesis" (2011) 10.1016/b978-0-12-385065-2.00004-9

[31]

Mizuno "Nonequilibrium Mechanics of Active Cytoskeletal Networks" Science (2007) 10.1126/science.1134404

[32]

Huxley "Fifty Years of Muscle and the Sliding Filament Hypothesis" Eur J Biochem (2004) 10.1111/j.1432-1033.2004.04044.x

[33]

Ricketts "Triggering Cation-Induced Contraction of Cytoskeleton Networks via Microfluidics" Front Phys (2020) 10.3389/fphy10.3389/fphy.2020.596699

[34]

Gurmessa "Counterion Crossbridges Enable Robust Multiscale Elasticity in Actin Networks" Phys Rev Res (2019) 10.1103/physrevresearch.1.013016

[35]

MacKintosh "Active Cellular Materials" Curr Opin Cel Biol (2010) 10.1016/j.ceb.2010.01.002

[36]

Wen "Polymer Physics of the Cytoskeleton" Curr Opin Solid State Mater Sci (2011) 10.1016/j.cossms.2011.05.002

[37]

Cooper "The Cell: A Molecular Approach" Nat Med (1997) 10.1038/nm0997-1042

[38]

Deshpande "Real-time Dynamics of Emerging Actin Networks in Cell-Mimicking Compartments" PloS one (2015) 10.1371/journal.pone.0116521

[39]

Huber "Counterion-induced Formation of Regular Actin Bundle Networks" Soft Matter (2012) 10.1039/c1sm06019h

[40]

Huber "Formation of Regularly Spaced Networks as a General Feature of Actin Bundle Condensation by Entropic Forces" New J Phys (2015) 10.1088/1367-2630/17/4/043029

[41]

Castaneda "Cations Modulate Actin Bundle Mechanics, Assembly Dynamics, and Structure" J Phys Chem B (2018) 10.1021/acs.jpcb.8b00663

[42]

Strehle "Transiently Crosslinked F-Actin Bundles" Eur Biophys J (2011) 10.1007/s00249-010-0621-z

[43]

Kaminer "Myosin Filamentogenesis: Effects of Ph and Ionic Concentration" J Mol Biol (1966) 10.1016/0022-2836(66)90070-2

[44]

Matsuda "Myosin-driven Fragmentation of Actin Filaments Triggers Contraction of a Disordered Actin Network" bioRxiv (2018)

[45]

Isambert "Dynamics and Rheology of Actin Solutions" Macromolecules (1996) 10.1021/ma946418x

[46]

Active microrheology determines scale-dependent material properties of Chaetopterus mucus

W. J. Weigand, A. Messmore, J. Tu et al.

PLoS ONE 2017 10.1371/journal.pone.0176732

[47]

Chapman "Onset of Non-continuum Effects in Microrheology of Entangled Polymer Solutions" Macromolecules (2014) 10.1021/ma401615m

[48]

Francis "Non-monotonic Dependence of Stiffness on Actin Crosslinking in Cytoskeleton Composites" Soft Matter (2019) 10.1039/c9sm01550g

[49]

Park "A Thin Permeable-Membrane Device for Single-Molecule Manipulation" Rev Scientific Instr (2016) 10.1063/1.4939197

[50]

Gurmessa "Triggered Disassembly and Reassembly of Actin Networks Induces Rigidity Phase Transitions" Soft matter (2019) 10.1039/c8sm01912f

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Details

Published: Nov 19, 2021
Vol/Issue: 9
License: View

Authors

Department of Physics; University of Massachusetts Amherst; USA

R

Rae M. Robertson-Anderson

Funding

National Science Foundation

W. M. Keck Foundation

Cite This Article

Bekele J. Gurmessa, Michael J. Rust, Moumita Das, et al. (2021). Salt-Mediated Stiffening, Destruction, and Resculpting of Actomyosin Network. Frontiers in Physics, 9. https://doi.org/10.3389/fphy.2021.760340

Salt-Mediated Stiffening, Destruction, and Resculpting of Actomyosin Network

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