Nonlinear Actin Deformations Lead to Network Stiffening, Yielding, and Nonuniform Stress Propagation.

Abstract:

:We use optical tweezers microrheology and fluorescence microscopy to apply nonlinear microscale strains to entangled and cross-linked actin networks, and measure the resulting stress and actin filament deformations. We couple nonlinear stress response and relaxation to the velocities and displacements of individual fluorescent-labeled actin segments, at varying times throughout the strain and varying distances from the strain path, to determine the underlying molecular dynamics that give rise to the debated nonlinear response and stress propagation of cross-linked and entangled actin networks at the microscale. We show that initial stress stiffening arises from acceleration of strained filaments due to molecular extension along the strain, while softening and yielding is coupled to filament deceleration, halting, and recoil. We also demonstrate a surprising nonmonotonic dependence of filament deformation on cross-linker concentration. Namely, networks with no cross-links or substantial cross-links both exhibit fast initial filament velocities and reduced molecular recoil while intermediate cross-linker concentrations display reduced velocities and increased recoil. We show that these collective results are due to a balance of network elasticity and force-induced cross-linker unbinding and rebinding. We further show that cross-links dominate entanglement dynamics when the length between cross-linkers becomes smaller than the length between entanglements. In accord with recent simulations, we demonstrate that post-strain stress can be long-lived in cross-linked networks by distributing stress to a small fraction of highly strained connected filaments that span the network and sustain the load, thereby allowing the rest of the network to recoil and relax.

journal_name

Biophys J

journal_title

Biophysical journal

authors

Gurmessa B,Ricketts S,Robertson-Anderson RM

doi

10.1016/j.bpj.2017.01.012

subject

Has Abstract

pub_date

2017-10-03 00:00:00

pages

1540-1550

issue

7

eissn

0006-3495

issn

1542-0086

pii

S0006-3495(17)30107-8

journal_volume

113

pub_type

杂志文章
  • Fast dynamics and stabilization of proteins: binary glasses of trehalose and glycerol.

    abstract::We present elastic and inelastic incoherent neutron scattering data from a series of trehalose glasses diluted with glycerol. A strong correlation with recently published protein stability data in the same series of glasses illustrates that the dynamics at Q >or= 0.71 A(-1) and omega > 200 MHz are important to stabili...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.103.035519

    authors: Cicerone MT,Soles CL

    更新日期:2004-06-01 00:00:00

  • Contractile mechanisms in flagella.

    abstract::The elastic theory of flexural waves in thin rods accurately predicts the velocity of flagellar bending waves over a wide range of viscosities. This shows that flagella behave as a purely mechanical system for the transmission of these waves. An evaluation of the total bending moment reveals that this moment occurs in...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(71)86227-6

    authors: Rikmenspoel R

    更新日期:1971-05-01 00:00:00

  • Solutions to axon equations.

    abstract::The solutions to a general class of axon partial differential equations proposed by FitzHugh which includes the Hodgkin-Huxley equations are studied. It is shown that solutions to the partial differential equations are exactly the solutions to a related set of integral equations. An iterative procedure for constructin...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(70)86355-X

    authors: Evans J,Shenk N

    更新日期:1970-11-01 00:00:00

  • A transient excited state model for sodium permeability changes in excitable membranes.

    abstract::In this paper we explore the properties of a mathematical model for the passive sodium permeability system of excitable membranes. This model is distinguished by the explicit inclusion of a rate constant which depends not on instantaneous voltage, but on rate of voltage change. Actually, the model is a rather modest m...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(75)85840-1

    authors: Jakobsson E,Scudiero C

    更新日期:1975-06-01 00:00:00

  • A Dynamic Biochemomechanical Model of Geometry-Confined Cell Spreading.

    abstract::Cell spreading is involved in many physiological and pathological processes. The spreading behavior of a cell significantly depends on its microenvironment, but the biochemomechanical mechanisms of geometry-confined cell spreading remain unclear. A dynamic model is here established to investigate the spreading of cell...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2017.04.044

    authors: Zhao ZL,Liu ZY,Du J,Xu GK,Feng XQ

    更新日期:2017-06-06 00:00:00

  • Molecular dynamics simulation of dipalmitoylphosphatidylcholine membrane with cholesterol sulfate.

    abstract::Using the molecular dynamics simulation technique, we studied the changes occurring in a dipalmitoylphosphatidylcholine (DPPC):cholesterol (CH) membrane at 50 mol% sterol when cholesterol is replaced with cholesterol sulfate (CS). Our simulations were performed at constant pressure and temperature on a nanosecond time...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(00)76719-1

    authors: Smondyrev AM,Berkowitz ML

    更新日期:2000-04-01 00:00:00

  • Long-time dynamics of Met-enkephalin: comparison of theory with Brownian dynamics simulations.

    abstract::A recent theory for the long time dynamics of flexible chain molecules is applied for the first time to a peptide of biological importance, the neurotransmitter met-enkephalin. The dynamics of met-enkephalin is considerably more complicated than that of the previously studied glycine oligomers; met-enkephalin contains...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(99)77185-7

    authors: Kostov KS,Freed KF

    更新日期:1999-01-01 00:00:00

  • Observing secretory granules with a multiangle evanescent wave microscope.

    abstract::In total internal reflection fluorescence microscopy (TIRFM), fluorophores near a surface can be excited with evanescent waves, which decay exponentially with distance from the interface. Penetration depths of evanescent waves from 60 nm to 300 nm were generated by varying the angle of incidence of a laser beam. With ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(00)76808-1

    authors: Rohrbach A

    更新日期:2000-05-01 00:00:00

  • Equilibrium thermodynamics of cell-cell adhesion mediated by multiple ligand-receptor pairs.

    abstract::In many situations, cell-cell adhesion is mediated by multiple ligand-receptor pairs. For example, the interaction between T cells and antigen-presenting cells of the immune system is mediated not only by T cell receptors and their ligands (peptide-major histocompatibility complex) but also by binding of intracellular...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(04)74211-3

    authors: Coombs D,Dembo M,Wofsy C,Goldstein B

    更新日期:2004-03-01 00:00:00

  • Measured effects of diacylglycerol on structural and elastic properties of phospholipid membranes.

    abstract::Diacylglycerol, a biological membrane second messenger, is a strong perturber of phospholipid planar bilayers. It converts multibilayers to the reverse hexagonal phase (HII), composed of highly curved monolayers. We have used x-ray diffraction and osmotic stress of the HII phase to measure structural dimensions, spont...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(96)79454-7

    authors: Leikin S,Kozlov MM,Fuller NL,Rand RP

    更新日期:1996-11-01 00:00:00

  • Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine.

    abstract::Deuterium magnetic resonance is applied to the study of the liquid crystalline and gel phases, and of the phase transition, of a multilamellar dispersion of chain perdeuterated (d62)-dipalmitoyl phosphatidylcholine/H2O. Analysis of the deuterium spectra in terms of the moments of the spectra allows one to make quantit...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(79)85222-4

    authors: Davis JH

    更新日期:1979-09-01 00:00:00

  • A Coiled-Coil Peptide Shaping Lipid Bilayers upon Fusion.

    abstract::A system based on two designed peptides, namely the cationic peptide K, (KIAALKE)3, and its complementary anionic counterpart called peptide E, (EIAALEK)3, has been used as a minimal model for membrane fusion, inspired by SNARE proteins. Although the fact that docking of separate vesicle populations via the formation ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2016.10.010

    authors: Rabe M,Aisenbrey C,Pluhackova K,de Wert V,Boyle AL,Bruggeman DF,Kirsch SA,Böckmann RA,Kros A,Raap J,Bechinger B

    更新日期:2016-11-15 00:00:00

  • Simultaneous tether extraction from endothelial cells and leukocytes: observation, mechanics, and significance.

    abstract::It has been hypothesized, from earlier studies on single-tether extraction from individual leukocytes and human umbilical vein endothelial cells, that during rolling of leukocytes on the endothelium, simultaneous extraction of membrane nanotubes (tethers) occurs, resulting in enhancement of the force decrease on the a...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.107.109298

    authors: Girdhar G,Shao JY

    更新日期:2007-12-01 00:00:00

  • State vector description of the proliferation of mammalian cells in tissue culture. I. Exponential growth.

    abstract::Proliferation of mammalian cells, even under conditions of unlimited growth, presents a complex problem because of the interaction of deterministic and stochastic processes. Division of the cell cycle into a finite number of parts establishes a multidimensional vector space. In this space an arbitrary culture can be r...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(66)86656-0

    authors: Hahn GM

    更新日期:1966-05-01 00:00:00

  • Kinetic Mechanism of RNA Helix-Terminal Basepairing-A Kinetic Minima Network Analysis.

    abstract::RNA functions are often kinetically controlled. The folding kinetics of RNAs involves global structural changes and local nucleotide movement, such as base flipping. The most elementary step in RNA folding is the closing and opening of a basepair. By integrating molecular dynamics simulation, master equation, and kine...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2019.09.017

    authors: Wang F,Sun LZ,Cai P,Chen SJ,Xu X

    更新日期:2019-11-05 00:00:00

  • Application of fluorescence spectroscopy to quantify shear-induced protein conformation change.

    abstract::Rapid and robust methods are required to quantify the effect of hydrodynamic shear on protein conformation change. We evaluated such strategies in this work and found that the binding of the fluorescent probe 4,4'-dianilino-1,1'-binaphthyl-5,5'-disulfonic acid (bis-ANS) to hydrophobic pockets in the blood protein von ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2009.08.023

    authors: Themistou E,Singh I,Shang C,Balu-Iyer SV,Alexandridis P,Neelamegham S

    更新日期:2009-11-04 00:00:00

  • Force-velocity relation for growing microtubules.

    abstract::Forces generated by microtubule polymerization and depolymerization are important for the biological functioning of cells. The mean growth velocity, V, under an opposing force, F, has been measured by; Science 278:856-860) for single microtubules growing in vitro, but their analysis of the data suggested that V decrea...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(01)76002-X

    authors: Kolomeisky AB,Fisher ME

    更新日期:2001-01-01 00:00:00

  • Dependence of DNA polymerase replication rate on external forces: a model based on molecular dynamics simulations.

    abstract::Molecular dynamics simulations are presented for a Thermus aquaticus (Taq) DNA polymerase I complex (consisting of the protein, the primer-template DNA strands, and the incoming nucleotide) subjected to external forces. The results obtained with a force applied to the DNA template strand provide insights into the effe...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.103.039313

    authors: Andricioaei I,Goel A,Herschbach D,Karplus M

    更新日期:2004-09-01 00:00:00

  • Nanoparticles as fluorescence labels: is size all that matters?

    abstract::Fluorescent labels are often used in bioassays as a means to detect and characterize ligand-receptor binding. This is due in part to the inherently high sensitivity of fluorescence-based technology and the relative accessibility of the technique. There is often little concern raised as to whether or not the fluorescen...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.107.127688

    authors: Swift JL,Cramb DT

    更新日期:2008-07-01 00:00:00

  • Increasing sensitivity of Ca2+ spark detection in noisy images by application of a matched-filter object detection algorithm.

    abstract::Microscopic calcium (Ca2+) events (such as Ca2+ sparks) are an important area for study, as they help clarify the mechanism(s) underlying intracellular signaling. In the heart, Ca2+ sparks occur as a result of Ca2+ release from the sarcoendoplasmic reticulum, via ryanodine receptor channels. Measurement of Ca2+ spark ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.108.135251

    authors: Kong CH,Soeller C,Cannell MB

    更新日期:2008-12-15 00:00:00

  • Na-K-2Cl Cotransporter and Store-Operated Ca2+ Entry in Pacemaking by Interstitial Cells of Cajal.

    abstract::Pacemaker depolarization in interstitial cells of Cajal (ICCs) is believed to be induced by Ca2+ transients and activation of anoctamin-1 (Ano1) channels in the plasma membrane. However, block of store-operated calcium entry (SOCE) or the Na-K-2Cl cotransporter (NKCC1) terminates pacemaker activity in ICC, indicating ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2019.07.020

    authors: Youm JB,Zheng H,Koh SD,Sanders KM

    更新日期:2019-08-20 00:00:00

  • Reaction of C-type cytochromes with the iron hexacyanides. Mechanistic implications.

    abstract::The reaction of c-cytochromes with iron hexacyanides is similar in mechanism to the interaction of cytochromes with their physiological oxidants and reductants in that the formation of complexes precedes electron transfer. Analysis of the kinetics of oxidation and reduction of a number of c-cytochromes by solving the ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(81)84754-6

    authors: Ohno N,Cusanovich MA

    更新日期:1981-12-01 00:00:00

  • Looping dynamics of linear DNA molecules and the effect of DNA curvature: a study by Brownian dynamics simulation.

    abstract::A Brownian dynamics (BD) model described in the accompanying paper (Klenin, K., H. Merlitz, and J. Langowski. 1998. A Brownian dynamics program for the simulation of linear and circular DNA, and other wormlike chain polyelectrolytes. Biophys. J. 74:000-000) has been used for computing the end-to-end distance distribut...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(98)74002-0

    authors: Merlitz H,Rippe K,Klenin KV,Langowski J

    更新日期:1998-02-01 00:00:00

  • Swelling of skinned muscle fibers of the frog. Experimental observations.

    abstract::Frog skeletal muscle fibers, mechanically skinned under water-saturated silicone oil, swell upon transfer to aqueous relaxing medium (60 mM KCl; 3 mM MgCl(2); 3 mM ATP; 4 mM EGTA; 20 mM Tris maleate; pH = 7.0; ionic strength 0.15 M). Their cross-sectional areas, estimated with an elliptical approximation, increase 2.3...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(77)85573-2

    authors: Godt RE,Maughan DW

    更新日期:1977-08-01 00:00:00

  • Kinetic studies of calcium-induced calcium release in cardiac sarcoplasmic reticulum vesicles.

    abstract::Fast Ca(2+) release kinetics were measured in cardiac sarcoplasmic reticulum vesicles actively loaded with Ca(2+). Release was induced in solutions containing 1.2 mM free ATP and variable free [Ca(2+)] and [Mg(2+)]. Release rate constants (k) were 10-fold higher at pCa 6 than at pCa 5 whereas Ryanodine binding was hig...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(03)75037-1

    authors: Sánchez G,Hidalgo C,Donoso P

    更新日期:2003-04-01 00:00:00

  • Anomalous x-ray scattering from terbium-labeled parvalbumin in solution.

    abstract::We have used anomalous small-angle x-ray scattering as a structural probe for solutions of rabbit parvalbumin labeled with terbium. This technique makes use of the large changes in the terbium scattering factor that occur when the x-ray energy is tuned around an L3 absorption edge of this heavy-atom label. These chang...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(83)84440-3

    authors: Miake-Lye RC,Doniach S,Hodgson KO

    更新日期:1983-03-01 00:00:00

  • Single cell mechanotransduction and its modulation analyzed by atomic force microscope indentation.

    abstract::The skeleton adapts to its mechanical usage, although at the cellular level, the distribution and magnitude of strains generated and their detection are ill-understood. The magnitude and nature of the strains to which cells respond were investigated using an atomic force microscope (AFM) as a microindentor. A confocal...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(02)75638-5

    authors: Charras GT,Horton MA

    更新日期:2002-06-01 00:00:00

  • Sorting of lipids and proteins in membrane curvature gradients.

    abstract::The sorting of lipids and proteins in cellular trafficking pathways is a process of central importance in maintaining compartmentalization in eukaryotic cells. However, the mechanisms behind these sorting phenomena are currently far from being understood. Among several mechanistic suggestions, membrane curvature has b...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2008.11.067

    authors: Tian A,Baumgart T

    更新日期:2009-04-08 00:00:00

  • Sound velocity and elasticity of tetragonal lysozyme crystals by Brillouin spectroscopy.

    abstract::Quasilongitudinal sound velocities and the second-order elastic moduli of tetragonal hen egg-white lysozyme crystals were determined as a function of relative humidity (RH) by Brillouin scattering. In hydrated crystals the measured sound velocities in the [110] plane vary between 2.12 +/- 0.03 km/s along the [001] dir...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(03)74738-9

    authors: Speziale S,Jiang F,Caylor CL,Kriminski S,Zha CS,Thorne RE,Duffy TS

    更新日期:2003-11-01 00:00:00

  • k-Cone analysis: determining all candidate values for kinetic parameters on a network scale.

    abstract::The absence of comprehensive measured kinetic values and the observed inconsistency in the available in vitro kinetic data has hindered the formulation of network-scale kinetic models of biochemical reaction networks. To meet this challenge we present an approach to construct a convex space, termed the k-cone, which c...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.104.050385

    authors: Famili I,Mahadevan R,Palsson BO

    更新日期:2005-03-01 00:00:00