Actomyosin Cortical Mechanical Properties in Nonadherent Cells Determined by Atomic Force Microscopy.

Abstract:

:The organization of filamentous actin and myosin II molecular motor contractility is known to modify the mechanical properties of the cell cortical actomyosin cytoskeleton. Here we describe a novel method, to our knowledge, for using force spectroscopy approach curves with tipless cantilevers to determine the actomyosin cortical tension, elastic modulus, and intracellular pressure of nonadherent cells. We validated the method by measuring the surface tension of water in oil microdrops deposited on a glass surface. We extracted an average tension of T ∼ 20.25 nN/μm, which agrees with macroscopic experimental methods. We then measured cortical mechanical properties in nonadherent human foreskin fibroblasts and THP-1 human monocytes before and after pharmacological perturbations of actomyosin activity. Our results show that myosin II activity and actin polymerization increase cortex tension and intracellular pressure, whereas branched actin networks decreased them. Interestingly, myosin II activity stiffens the cortex and branched actin networks soften it, but actin polymerization has no effect on cortex stiffness. Our method is capable of detecting changes in cell mechanical properties in response to perturbations of the cytoskeleton, allowing characterization with physically relevant parameters. Altogether, this simple method should be of broad application for deciphering the molecular regulation of cell cortical mechanical properties.

journal_name

Biophys J

journal_title

Biophysical journal

authors

Cartagena-Rivera AX,Logue JS,Waterman CM,Chadwick RS

doi

10.1016/j.bpj.2016.04.034

subject

Has Abstract

pub_date

2016-06-07 00:00:00

pages

2528-2539

issue

11

eissn

0006-3495

issn

1542-0086

pii

S0006-3495(16)30237-5

journal_volume

110

pub_type

杂志文章
  • Benjamin Franklin, Philadelphia's favorite son, was a membrane biophysicist.

    abstract::Benjamin Franklin, mostly known for his participation in writing The Declaration of Independence and work on electricity, was also one of the first scientists to seek to understand the properties of oil monolayers on water surfaces. During one of his many voyages across the Atlantic Ocean, Franklin observed that oil h...

    journal_title:Biophysical journal

    pub_type: 传,历史文章,杂志文章

    doi:10.1016/j.bpj.2012.12.028

    authors: Wang DN,Stieglitz H,Marden J,Tamm LK

    更新日期:2013-01-22 00:00:00

  • Improved resolution of tertiary structure elasticity in muscle protein.

    abstract::Rearrangement of tertiary structure in response to mechanical force (termed tertiary structure elasticity) in the tandem Ig chain is the first mode of elastic response for muscle protein titin. Tertiary structure elasticity occurs at low stretching forces (few tens of pN), and was described at atomic resolution in a r...

    journal_title:Biophysical journal

    pub_type: 信件

    doi:10.1016/j.bpj.2011.01.019

    authors: Hsin J,Schulten K

    更新日期:2011-02-16 00:00:00

  • Asymmetrical membranes and surface tension.

    abstract::The (31)P-nuclear magnetic resonance chemical shift of phosphatidic acid in a membrane is sensitive to the lipid head group packing and can report qualitatively on membrane lateral compression near the aqueous interface. We have used high-resolution (31)P-nuclear magnetic resonance to evaluate the lateral compression ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(02)73915-5

    authors: Traïkia M,Warschawski DE,Lambert O,Rigaud JL,Devaux PF

    更新日期:2002-09-01 00:00:00

  • Real-time control of neutrophil metabolism by very weak ultra-low frequency pulsed magnetic fields.

    abstract::In adherent and motile neutrophils NAD(P)H concentration, flavoprotein redox potential, and production of reactive oxygen species and nitric oxide, are all periodic and exhibit defined phase relationships to an underlying metabolic oscillation of approximately 20 s. Utilizing fluorescence microscopy, we have shown in ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.104.056663

    authors: Rosenspire AJ,Kindzelskii AL,Simon BJ,Petty HR

    更新日期:2005-05-01 00:00:00

  • Deuterium solid-state NMR investigations of exchange labeled oriented purple membranes at different hydration levels.

    abstract::Oriented purple membranes were equilibrated under controlled (2)H(2)O relative humidity ranging from 15% to 93% and introduced into the magnetic field of an NMR spectrometer with the membrane normal parallel to the magnetic field direction. Deuterium solid-state NMR spectra of these samples resolved four deuteron popu...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(03)74480-4

    authors: Bechinger B,Weik M

    更新日期:2003-07-01 00:00:00

  • Improving signal/noise resolution in single-molecule experiments using molecular constructs with short handles.

    abstract::We investigate unfolding/folding force kinetics in DNA hairpins exhibiting two and three states with newly designed short dsDNA handles (29 bp) using optical tweezers. We show how the higher stiffness of the molecular setup moderately enhances the signal/noise ratio (SNR) in hopping experiments as compared to conventi...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2011.01.071

    authors: Forns N,de Lorenzo S,Manosas M,Hayashi K,Huguet JM,Ritort F

    更新日期:2011-04-06 00:00:00

  • Dynamic Allostery in PLCγ1 and Its Modulation by a Cancer Mutation Revealed by MD Simulation and NMR.

    abstract::Phosphatidylinositol phospholipase Cγ (PLCγ) is an intracellular membrane-associated second-messenger signaling protein activated by tyrosine kinases such as fibroblast growth factor receptor 1. PLCγ contains the regulatory γ-specific array (γSA) comprising a tandem Src homology 2 (SH2) pair, an SH3 domain, and a spli...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2018.05.031

    authors: Koss H,Bunney TD,Esposito D,Martins M,Katan M,Driscoll PC

    更新日期:2018-07-03 00:00:00

  • Atomic force microscopy studies of functional and dysfunctional pulmonary surfactant films. I. Micro- and nanostructures of functional pulmonary surfactant films and the effect of SP-A.

    abstract::Monolayers of a functional pulmonary surfactant (PS) can reach very low surface tensions well below their equilibrium value. The mechanism by which PS monolayers reach such low surface tensions and maintain film stability remains unknown. As shown previously by fluorescence microscopy, phospholipid phase transition an...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.107.122648

    authors: Zuo YY,Keating E,Zhao L,Tadayyon SM,Veldhuizen RA,Petersen NO,Possmayer F

    更新日期:2008-05-01 00:00:00

  • Kinetic constants of the acetylcholine (ACh) receptor reaction deduced from the rise in open probability after steps in ACh concentration.

    abstract::Outside-out patches of enzymatically dissociated adult and denervated mouse muscle fibers were superfused repetitively by pulses of acetylcholine (ACh) containing solution. Up to 300 channels opened simultaneously 300 microseconds after the beginning of a 1,000 microM ACh pulse corresponding to a peak current i of alm...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(91)82138-5

    authors: Franke C,Hatt H,Parnas H,Dudel J

    更新日期:1991-11-01 00:00:00

  • Comparative Molecular Dynamics Analysis of RNase-S Complex Formation.

    abstract::Limited proteolysis of RNase-A yields a short N-terminal S-peptide segment and the larger S-protein. Binding of S-peptide to S-protein results in the formation of an enzymatically active RNase-S protein. S-peptide undergoes a transition from intrinsic disorder to an ordered helical state upon association with S-protei...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2017.08.008

    authors: Luitz MP,Bomblies R,Zacharias M

    更新日期:2017-10-03 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

  • Molecular dynamics computations and solid state nuclear magnetic resonance of the gramicidin cation channel.

    abstract::This paper reports on a coupled approach to determining the structure of the gramicidin A ion channel, utilizing solid state nuclear magnetic resonance (NMR) of isotopically labeled gramicidin channels aligned parallel to the magnetic field direction, and molecular dynamics (MD). MD computations using an idealized rig...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(91)82131-2

    authors: Chiu SW,Nicholson LK,Brenneman MT,Subramaniam S,Teng Q,McCammon JA,Cross TA,Jakobsson E

    更新日期:1991-10-01 00:00:00

  • Three-dimensional dynamic structure of the liquid-ordered domain in lipid membranes as examined by pulse-EPR oxygen probing.

    abstract::Membranes made of dimyristoylphosphatidylcholine and cholesterol, one of the simplest paradigms for the study of liquid ordered-disordered phase separation, were investigated using a pulse-EPR spin-labeling method in which bimolecular collision of molecular oxygen with the nitroxide spin label is measured. This method...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.106.097568

    authors: Subczynski WK,Wisniewska A,Hyde JS,Kusumi A

    更新日期:2007-03-01 00:00:00

  • Investigation of the image contrast of tapping-mode atomic force microscopy using protein-modified cantilever tips.

    abstract::In this work we have designed a simple system to investigate empirically the image contrast of tapping-mode atomic force microscopy (TMAFM). We modified the cantilever tips with protein molecules (bovine serum albumin or goat anti-biotin antibody) and used these protein-modified cantilevers to scan poly-L-lysine films...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(97)78354-1

    authors: You H,Yu L

    更新日期:1997-12-01 00:00:00

  • Oxygen permeability of the limiting layers of the cornea.

    abstract::Using polarography and suitable mathematical analysis, the oxygen permeability of an individual layer of a bilayered tissue may be determined if the oxygen consumption and permeability of the other layer are known. Results obtained on rabbit cornea indicate that the permeability of the epithelium is about four times t...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(72)86083-1

    authors: Freeman RD,Fatt I

    更新日期:1972-03-01 00:00:00

  • An electron spin resonance study of synaptosome opiate receptors. The preparation and use of a spin labeled morphine.

    abstract::Morphine spin labeled on the phenolic hydroxy group has been prepared using commercially available reagents and characterized by thin layer chromatography, mass spectroscopy, and electron spin resonance spectroscopy. It has been shown that morphine modified in this way retains some opiate activity, does not pass throu...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(75)85889-9

    authors: Copeland ES,Boykin ME,Kelley JA,Kullberg MP

    更新日期:1975-11-01 00:00:00

  • The effect of ionic strength, temperature, and pressure on the interaction potential of dense protein solutions: from nonlinear pressure response to protein crystallization.

    abstract::Understanding the intermolecular interaction potential, V(r), of proteins under the influence of temperature, pressure, and salt concentration is essential for understanding protein aggregation, crystallization, and protein phase behavior in general. Here, we report small-angle x-ray scattering studies on dense lysozy...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2012.04.043

    authors: Möller J,Schroer MA,Erlkamp M,Grobelny S,Paulus M,Tiemeyer S,Wirkert FJ,Tolan M,Winter R

    更新日期:2012-06-06 00:00:00

  • Characterization of PROPPIN-Phosphoinositide Binding and Role of Loop 6CD in PROPPIN-Membrane Binding.

    abstract::PROPPINs (β-propellers that bind polyphosphoinositides) are a family of PtdIns3P- and PtdIns(3,5)P2-binding proteins that play an important role in autophagy. We analyzed PROPPIN-membrane binding through isothermal titration calorimetry (ITC), stopped-flow measurements, mutagenesis studies, and molecular dynamics (MD)...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2015.03.045

    authors: Busse RA,Scacioc A,Krick R,Pérez-Lara Á,Thumm M,Kühnel K

    更新日期:2015-05-05 00:00:00

  • Peptide aggregation in finite systems.

    abstract::Universal features of the peptide aggregation process suggest a common mechanism, with a first-order phase transition in aqueous solutions of the peptides being the driving force. Small system sizes strongly affect the stability of the minor phase in the two-phase region. We show manifestations of this effect in aqueo...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.108.136226

    authors: Singh G,Brovchenko I,Oleinikova A,Winter R

    更新日期:2008-10-01 00:00:00

  • Kinetics of intracellular ice formation in one-dimensional arrays of interacting biological cells.

    abstract::Although cell-cell interactions are known to significantly affect the kinetics of intracellular ice formation (IIF) during tissue freezing, this effect is not well understood. Progress in elucidating the mechanism and role of intercellular ice propagation in tissue freezing has been hampered in part by limitations in ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.104.048355

    authors: Irimia D,Karlsson JO

    更新日期:2005-01-01 00:00:00

  • Stalk model of membrane fusion: solution of energy crisis.

    abstract::Membrane fusion proceeds via formation of intermediate nonbilayer structures. The stalk model of fusion intermediate is commonly recognized to account for the major phenomenology of the fusion process. However, in its current form, the stalk model poses a challenge. On one hand, it is able to describe qualitatively th...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(02)75450-7

    authors: Kozlovsky Y,Kozlov MM

    更新日期:2002-02-01 00:00:00

  • Penetration depth of surfactant peptide KL4 into membranes is determined by fatty acid saturation.

    abstract::KL(4) is a 21-residue functional peptide mimic of lung surfactant protein B, an essential protein for lowering surface tension in the alveoli. Its ability to modify lipid properties and restore lung compliance was investigated with circular dichroism, differential scanning calorimetry, and solid-state NMR spectroscopy...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2008.12.3966

    authors: Antharam VC,Elliott DW,Mills FD,Farver RS,Sternin E,Long JR

    更新日期:2009-05-20 00:00:00

  • Friction from Transduction Channels' Gating Affects Spontaneous Hair-Bundle Oscillations.

    abstract::Hair cells of the inner ear can power spontaneous oscillations of their mechanosensory hair bundle, resulting in amplification of weak inputs near the characteristic frequency of oscillation. Recently, dynamic force measurements have revealed that delayed gating of the mechanosensitive ion channels responsible for mec...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2017.11.019

    authors: Barral J,Jülicher F,Martin P

    更新日期:2018-01-23 00:00:00

  • Conformation of a peptide encompassing the proton translocation channel of vacuolar H(+)-ATPase.

    abstract::The structural properties of a crucial transmembrane helix for proton translocation in vacuolar ATPase are studied using double site-directed spin-labeling combined with electron spin resonance (ESR) (or electron paramagnetic resonance) and circular dichroism spectroscopy in sodium dodecyl sulfate micelles. For this p...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.106.089854

    authors: Vos WL,Vermeer LS,Hemminga MA

    更新日期:2007-01-01 00:00:00

  • Molecular dynamics simulation of the structure of dimyristoylphosphatidylcholine bilayers with cholesterol, ergosterol, and lanosterol.

    abstract::Five molecular dynamics computer simulations were performed on different phospholipid:sterol membrane systems in order to study the influence of sterol structure on membrane properties. Three of these simulated bilayer systems were composed of a 1:8 sterol:phospholipid ratio, each of which employed one of the sterol m...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(01)76137-1

    authors: Smondyrev AM,Berkowitz ML

    更新日期:2001-04-01 00:00:00

  • Interactions of the M2delta segment of the acetylcholine receptor with lipid bilayers: a continuum-solvent model study.

    abstract::M2delta, one of the transmembrane segments of the nicotinic acetylcholine receptor, is a 23-amino-acid peptide, frequently used as a model for peptide-membrane interactions. In this and the companion article we describe studies of M2delta-membrane interactions, using two different computational approaches. In the pres...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(03)74785-7

    authors: Kessel A,Haliloglu T,Ben-Tal N

    更新日期:2003-12-01 00:00:00

  • Conformational dynamics of bovine Cu, Zn superoxide dismutase revealed by time-resolved fluorescence spectroscopy of the single tyrosine residue.

    abstract::The structural dynamics of bovine erythrocyte Cu, Zn superoxide dismutase (BSOD) was studied by time-resolved fluorescence spectroscopy. BSOD is a homodimer containing a single tyrosine residue (and no tryptophan) per subunit. Frequency-domain fluorometry revealed a heterogeneous fluorescence decay that could be descr...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/S0006-3495(94)80901-4

    authors: Ferreira ST,Stella L,Gratton E

    更新日期:1994-04-01 00:00:00

  • Patch-clamp recording of charge movement, Ca2+ current, and Ca2+ transients in adult skeletal muscle fibers.

    abstract::Intramembrane charge movement (Q), Ca(2+) conductance (G(m)) through the dihydropyridine-sensitive L-type Ca(2+) channel (DHPR) and intracellular Ca(2+) fluorescence (F) have been recorded simultaneously in flexor digitorum brevis muscle fibers of adult mice, using the whole-cell configuration of the patch-clamp techn...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/s0006-3495(99)77104-3

    authors: Wang ZM,Messi ML,Delbono O

    更新日期:1999-11-01 00:00:00

  • Dynamics of DNA ejection from bacteriophage.

    abstract::The ejection of DNA from a bacterial virus (i.e., phage) into its host cell is a biologically important example of the translocation of a macromolecular chain along its length through a membrane. The simplest mechanism for this motion is diffusion, but in the case of phage ejection a significant driving force derives ...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1529/biophysj.105.070532

    authors: Inamdar MM,Gelbart WM,Phillips R

    更新日期:2006-07-15 00:00:00

  • Adhesion between human neutrophils and immobilized endothelial ligand vascular cell adhesion molecule 1: divalent ion effects.

    abstract::Integrin-mediated adhesion of circulating neutrophils to endothelium during inflammation involves multiple adhesion molecules on both neutrophils and endothelium. Most studies of neutrophil adhesion have focused on adhesion to ICAM-1 (mediated by beta(2) integrins), but interaction with the endothelial ligand vascular...

    journal_title:Biophysical journal

    pub_type: 杂志文章

    doi:10.1016/j.bpj.2008.10.001

    authors: Lomakina EB,Waugh RE

    更新日期:2009-01-01 00:00:00