Measurement of the Elastic Modulus for Red Cell Membrane Using a Fluid Mechanical Technique

Hochmuth, Robert M.; Mohandas, Narla; Blackshear, Perry L.

doi:10.1016/s0006-3495(73)86021-7

Cited by 293 publications

(226 citation statements)

References 7 publications

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“…Such membrane tethers have also been observed on various whole cells by different methods (e.g. [789][790][791]). The force required to extend such a tube is F % 4prg, where g is the surface tension of a lipid bilayer and r is the radius of the tube.…”

Section: Force Curves On Lipid Bilayersmentioning

confidence: 87%

Force measurements with the atomic force microscope: Technique, interpretation and applications

Butt

Cappella

Kappl

2005

Surface Science Reports

3,210

2,949

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Section: Force Curves On Lipid Bilayersmentioning

confidence: 87%

Force measurements with the atomic force microscope: Technique, interpretation and applications

Butt

Cappella

Kappl

2005

Surface Science Reports

3,210

2,949

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“…The assumption in the adhesion energy model that the bilayer-cytoskeletal adhesion is a continuum property of the membrane is not rigorously true, because integral proteins are known to create discrete attachments of the spectrin network to the lipid bilayer. Therefore, we use our two-component model with N v = 23,867 to predict the bilayercytoskeletal interaction force explicitly and directly at the molecular level when the bilayer-cytoskeletal bonds rupture occurs under a certain threshold value of shear stress (∼1.5 dyn/cm 2 or 0.15 pN/μm 2 ) during the tethering process in channel flow (18). The detailed simulation setup can be found in SI Text.…”

Section: Resultsmentioning

confidence: 99%

“…The specific characteristics of these interactions influence, in different ways, the mechanical property data inferred from several different experiments, such as micropipette aspiration and vesiculation (12,13), membrane thermal fluctuations (14-16), tank-treading motion (17), and tethering of the lipid bilayer in channel flow (18). In the present study, we investigate the effects of the bilayer-cytoskeletal interactions in these experiments, using a unique two-component mesoscale RBC model implemented in dissipative particle dynamics (DPD).…”

mentioning

confidence: 99%

Lipid bilayer and cytoskeletal interactions in a red blood cell

Peng

Pivkin

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

163

150

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We study the biomechanical interactions between the lipid bilayer and the cytoskeleton in a red blood cell (RBC) by developing a general framework for mesoscopic simulations. We treated the lipid bilayer and the cytoskeleton as two distinct components and developed a unique whole-cell model of the RBC, using dissipative particle dynamics (DPD). The model is validated by comparing the predicted results with measurements from four different and independent experiments. First, we simulated the micropipette aspiration and quantified the cytoskeletal deformation. Second, we studied the membrane fluctuations of healthy RBCs and RBCs parasitized to different intraerythrocytic stages by the malaria-inducing parasite Plasmodium falciparum. Third, we subjected the RBC to shear flow and investigated the dependence of its tank-treading frequency on shear rate. Finally, we simulated the bilayer-cytoskeletal detachment in channel flow to quantify the strength of such interactions when the corresponding bonds break. Taken together, these experiments and corresponding systematic DPD simulations probe the governing constitutive response of the cytoskeleton, elastic stiffness, viscous friction, and strength of bilayer-cytoskeletal interactions as well as membrane viscosities. Hence, the DPD simulations and comparisons with available independent experiments serve as validation of the unique two-component model and lead to useful insights into the biomechanical interactions between the lipid bilayer and the cytoskeleton of the RBC. Furthermore, they provide a basis for further studies to probe cell mechanistic processes in health and disease in a manner that guides the design and interpretation of experiments and to develop simulations of phenomena that cannot be studied systematically by experiments alone.coarse graining | worm-like chain | multiscale modeling | adhesion energy | erythrocyte T he red blood cell (RBC) membrane consists of two components: a lipid bilayer and an attached 2D spectrin network that acts as the cytoskeleton. The resistance of the lipid bilayer to bending is controlled by the bending rigidity, k c , whereas the spectrin network's resistance to shear strain is characterized by the in-plane shear modulus, μ s . Under normal conditions, the cytoskeleton is tightly attached to the lipid bilayer from the cytoplasmic side. However, under certain pathological conditions, e.g., in sickle cell disease, the cytoskeleton may become dissociated from the lipid bilayer (1). Although the biomechanics of the two-component erythrocyte membrane have been studied extensively for decades (2), the mechanical properties of the interactions between the lipid bilayer and the cytoskeleton (such as elastic stiffness, viscous friction, and strength) via the pinning connections of transmembrane proteins are still largely unknown. This is at least in part ascribed to the fact that it is difficult to measure these interactions directly from experiments, because the length scale of these connections is too small compared with the chara...

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“…Numerous works were devoted to the study of tether growth from various cells, namely red blood cells (RBCs) (5,6,8,22), neuronal growth cones (NGCs) (10,12), outer hair cells (OHCs) (23). In the vast majority of cases, experiments were aimed at measuring the static force to derive the static adhesion energy, W 0 .…”

Section: Proposed Reinterpretation Of Experimental Resultsmentioning

confidence: 99%

“…Membranous tails also are observed to be left by migrating cells in culture dishes (3). Tethers can be extracted from synthetic vesicles or living cells by the application of an external point force [using a fluid drag (4,5) or pipette-tweezer system (6,7)]. In the case of living cells, where the lipidic membrane is coupled to a cytoskeleton, tethers can be used as membrane sensors to measure the membrane-cytoskeleton adhesion energy W 0 (8)(9)(10)(11)(12).…”

mentioning

confidence: 99%

Hydrodynamic narrowing of tubes extruded from cells

Brochard-Wyart

Borghi

Cuvelier

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

122

156

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We discuss the pulling force f required to extrude a lipid tube from a living cell as a function of the extrusion velocity L . The main feature is membrane friction on the cytoskeleton. As recently observed for neutrophils, the tether force exhibits a ''shear thinning'' response over a large range of pulling velocities, which was previously interpreted by assuming viscoelastic flows of the sliding membrane. Here, we propose an alternative explanation based on purely Newtonian flow: The diameter of the tether decreases concomitantly with the increase of the membrane tension in the lipid tube. The pulling force is found to vary as L 1/3 , which is consistent with reported experimental data for various types of cells.cytoskeleton ͉ dynamics ͉ membrane tethers M any cellular processes [such as intracellular trafficking (1) or intercellular organelle transport (2)] involve the formation of thin tubular structures known as tethers. Membranous tails also are observed to be left by migrating cells in culture dishes (3). Tethers can be extracted from synthetic vesicles or living cells by the application of an external point force [using a fluid drag (4, 5) or pipette-tweezer system (6, 7)]. In the case of living cells, where the lipidic membrane is coupled to a cytoskeleton, tethers can be used as membrane sensors to measure the membrane-cytoskeleton adhesion energy W 0 (8-12).Our aim here is to describe the formation of a tether and to derive the required pulling force as a function of the extrusion velocity. Pulling a tube from a cell membrane implies a surface flow of lipid from the cell body to the tether through the membranecytoskeleton binders. This viscous drag gives rise to an increase of the membrane tension in the tube and a decrease of its radius. Statics of ExtrusionWe follow the thermodynamic analysis of tether formation proposed by Waugh and coworkers (7,13,14), Evans and Yeung (15), and Derényi and coworkers (16) for lipidic bilayers and extended to cell membranes by Sheetz and coworkers (10, 12). As shown in Fig. 1, the cell is usually held by micropipette suction (pressure Ϫ⌬P) that sets the membrane tension of the cell : 2 Ӎ R p ⌬P, where R p is the radius of the micropipette. The length of the tongue in the pipette is L p . Another case of experimental interest is found when cells are spread onto an adhesive surface, which ensures that the membrane tension remains weak or constant during the time course of the experiment. The tube is then either extruded by pulling out a small bead adhering to the membrane via micromanipulation if the cell is firmly adhered or, more simply, by applying a hydrodynamic flow over the cell in case of a discrete and sparse adhesion site. The length of the tube is L, the membrane tension of the tube is t , and its radius is r t . We want to relate r t and t to , the tension of the cell body, and to W 0 , the adhesion energy of the membrane to the cytoskeleton. The pulling force f 0 is deduced from the following four equations. The distribution of areas:2 r t dL ϭ 2 R p dL p...

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Measurement of the Elastic Modulus for Red Cell Membrane Using a Fluid Mechanical Technique

Cited by 293 publications

References 7 publications

Force measurements with the atomic force microscope: Technique, interpretation and applications

Force measurements with the atomic force microscope: Technique, interpretation and applications

Lipid bilayer and cytoskeletal interactions in a red blood cell

Hydrodynamic narrowing of tubes extruded from cells

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