Effect of membrane tension on the physical properties of DOPC lipid bilayer membrane

Reddy, A. Srinivas; Warshaviak, Dora Toledo; Chachisvilis, Mirianas

doi:10.1016/j.bbamem.2012.05.006

Cited by 110 publications

(96 citation statements)

References 96 publications

(132 reference statements)

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“…1. The resulting area expansion coefficients for DPhPC (K A = 222 ± 14 mN/m; mean ± SD for n = 8 ramps from two GUVs) and DOPC (K A = 199 ± 48 mN/m; mean ± SD for n = 6 ramps from two GUVs) are comparable to the area expansion coefficients measured by micropipette aspiration (265 ± 18 mN/m for DOPC) (37), and in excellent agreement with the reported area and thickness changes from molecular dynamics simulations (effective K A = 220 mN/m for DOPC) (38). Thus, the whole-GUV method allows membrane tension to be varied from the lowest physiologically relevant levels right up to the lysis tension of the membrane while simultaneously controlling the membrane voltage and measuring the membrane current, which has allowed us to confirm the predicted relationship between membrane capacitance and tension directly (Eq.…”

Section: Resultssupporting

confidence: 73%

Whole-GUV patch-clamping

Garten

Mosgaard

Bornschlögl

et al. 2016

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

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Studying how the membrane modulates ion channel and transporter activity is challenging because cells actively regulate membrane properties, whereas existing in vitro systems have limitations, such as residual solvent and unphysiologically high membrane tension. Cell-sized giant unilamellar vesicles (GUVs) would be ideal for in vitro electrophysiology, but efforts to measure the membrane current of intact GUVs have been unsuccessful. In this work, two challenges for obtaining the "whole-GUV" patch-clamp configuration were identified and resolved. First, unless the patch pipette and GUV pressures are precisely matched in the GUV-attached configuration, breaking the patch membrane also ruptures the GUV. Second, GUVs shrink irreversibly because the membrane/glass adhesion creating the high-resistance seal (>1 GΩ) continuously pulls membrane into the pipette. In contrast, for cell-derived giant plasma membrane vesicles (GPMVs), breaking the patch membrane allows the GPMV contents to passivate the pipette surface, thereby dynamically blocking membrane spreading in the whole-GMPV mode. To mimic this dynamic passivation mechanism, beta-casein was encapsulated into GUVs, yielding a stable, high-resistance, whole-GUV configuration for a range of membrane compositions. Specific membrane capacitance measurements confirmed that the membranes were truly solvent-free and that membrane tension could be controlled over a physiological range. Finally, the potential for ion transport studies was tested using the model ion channel, gramicidin, and voltage-clamp fluorometry measurements were performed with a voltage-dependent fluorophore/ quencher pair. Whole-GUV patch-clamping allows ion transport and other voltage-dependent processes to be studied while controlling membrane composition, tension, and shape. giant unilamellar vesicle | patch clamp | electrophysiology | biomimetic system | lipid-glass interaction

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Section: Resultssupporting

confidence: 73%

Whole-GUV patch-clamping

Garten

Mosgaard

Bornschlögl

et al. 2016

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

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“…Under the above concentration conditions, Dr eq /r 0 for GUVs with a radius of 10 mm is 6.2 Â 10 À3 , which is 13 times larger than that for LUVs with a radius of 100 nm (¼ 4.9 Â 10 À4 ), and hence, s eq osm for the GUV is 13 times larger than s eq osm for the LUV. To validate this theory on the radius dependence of s eq osm , we measured a change in a physical property of lipid membranes induced by P. It was recently reported that the membrane stretching due to lateral tension increases the fluidity of lipid membranes (45,46) and the diffusion coefficient of lipid molecules (45)(46)(47). To monitor the fluidity of the membranes, we used generalized emission polarization value (GP) of Laurdan in membranes, because it is generally considered that with an increase in fluidity of lipid membranes the interaction of water molecules with a Laurdan molecule in the membrane interface increases, which causes the GP value to decrease (48,49).…”

Section: Discussionmentioning

confidence: 99%

“…DOPC-GUVs were prepared by natural swelling in water (MilliQ) containing sucrose as follows (27). DOPC in chloroform (1.0 mM, 200 mL) in a small glass bottle (5 mL) was dried by N 2 gas to produce a thin, homogeneous lipid film; then, residual chloroform in the film was removed by placing the bottle in a vacuum desiccator connected to a rotary vacuum pump for >12 h. MilliQ water (20 mL) was added and the bottle was sealed and incubated in [45][46][47] C water for 8 min (prehydration). Then, 1.0 mL of 100.0 mM sucrose in MilliQ was added gently, and the bottle was resealed and incubated in an incubator at 37 C for 2 h to produce a GUV suspension.…”

Section: Methodsmentioning

confidence: 99%

Experimental Estimation of Membrane Tension Induced by Osmotic Pressure

Shibly

Ghatak

Karal

et al. 2016

Biophysical Journal

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Osmotic pressure (P) induces the stretching of plasma membranes of cells or lipid membranes of vesicles, which plays various roles in physiological functions. However, there have been no experimental estimations of the membrane tension of vesicles upon exposure to P. In this report, we estimated experimentally the lateral tension of the membranes of giant unilamellar vesicles (GUVs) when they were transferred into a hypotonic solution. First, we investigated the effect of P on the rate constant, k p , of constant-tension (s ex )-induced rupture of dioleoylphosphatidylcholine (DOPC)-GUVs using the method developed by us recently. We obtained the s ex dependence of k p in GUVs under P and by comparing this result with that in the absence of P, we estimated the tension of the membrane due to P at the swelling equilibrium, s eq osm . Next, we measured the volume change of DOPC-GUVs under small P. The experimentally obtained values of s eq osm and the volume change agreed with their theoretical values within the limits of the experimental errors. Finally, we investigated the characteristics of the P-induced pore formation in GUVs. The s eq osm corresponding to the threshold P at which pore formation is induced is similar to the threshold tension of the s ex -induced rupture. The time course of the radius change of GUVs in the P-induced pore formation depends on the total membrane tension, s t ; for small s t , the radius increased with time to an equilibrium one, which remained constant for a long time until pore formation, but for large s t , the radius increased with time and pore formation occurred before the swelling equilibrium was reached. Based on these results, we discussed the s eq osm and the P-induced pore formation in lipid membranes.

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“…From the response to osmotic pressure, the material constants are then evaluated for the membrane deformation. Such structural measures can also be used to experimentally validate molecular dynamics (MD) simulations [81, 82] of lipid systems and biomembranes [53, 54, 83]. The molecular force fields encapsulate the data obtained with different experimental techniques [84].…”

Section: Implications Of Membrane Deformation Due To Osmotic Stressmentioning

confidence: 99%

Elastic deformation and area per lipid of membranes: Atomistic view from solid-state deuterium NMR spectroscopy

Kinnun

Mallikarjunaiah

Petrache

et al. 2015

Biochimica et Biophysica Acta (BBA) - Biomembranes

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This article reviews the application of solid-state 2H nuclear magnetic resonance (NMR) spectroscopy for investigating the deformation of lipid bilayers at the atomistic level. For liquid-crystalline membranes, the average structure is manifested by the segmental order parameters (SCD) of the lipids. Solid-state 2H NMR yields observables directly related to the stress field of the lipid bilayer. The extent to which lipid bilayers are deformed by osmotic pressure is integral to how lipid-protein interactions affect membrane functions. Calculations of the average area per lipid and related structural properties are pertinent to bilayer remodeling and molecular dynamics (MD) simulations of membranes. To establish structural quantities, such as area per lipid and volumetric bilayer thickness, a mean-torque analysis of 2H NMR order parameters is applied. Osmotic stress is introduced by adding polymer solutions or by gravimetric dehydration, which are thermodynamically equivalent. Solid-state NMR studies of lipids under osmotic stress probe membrane interactions involving collective bilayer undulations, order-director fluctuations, and lipid molecular protrusions. Removal of water yields a reduction of the mean area per lipid, with a corresponding increase in volumetric bilayer thickness, by up to 20% in the liquid-crystalline state. Hydrophobic mismatch can shift protein states involving mechanosensation, transport, and molecular recognition by G-protein–coupled receptors. Measurements of the order parameters versus osmotic pressure yield the elastic area compressibility modulus and the corresponding bilayer thickness at an atomistic level. Solid-state 2H NMR thus reveals how membrane deformation can affect protein conformational changes within the stress field of the lipid bilayer.

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Effect of membrane tension on the physical properties of DOPC lipid bilayer membrane

Cited by 110 publications

References 96 publications

Whole-GUV patch-clamping

Whole-GUV patch-clamping

Experimental Estimation of Membrane Tension Induced by Osmotic Pressure

Elastic deformation and area per lipid of membranes: Atomistic view from solid-state deuterium NMR spectroscopy

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