Phase Behavior of Lipid Bilayers under Tension

Uline, Mark J.; Schick, M.; Szleifer, Igal

doi:10.1016/j.bpj.2011.12.050

Cited by 50 publications

(72 citation statements)

References 17 publications

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“…Ursell et al (13) observed a repulsion of domains in deflated GUVs, caused by the induction of membrane curvature between the l o domains. In the case of PSMs, the rather large lateral membrane tension of about 1 mN·m −1 (23,24,32) prevents the induction of a 3D structure in the center of the PSM, although it does not significantly alter phase separation (33,34). This trait allows the l o domains to merge, leading to only one mobile domain in each PSM.…”

Section: Resultsmentioning

confidence: 99%

Size and mobility of lipid domains tuned by geometrical constraints

Schütte

Mey

Enderlein

et al. 2017

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

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In the plasma membrane of eukaryotic cells, proteins and lipids are organized in clusters, the latter ones often called lipid domains or "lipid rafts." Recent findings highlight the dynamic nature of such domains and the key role of membrane geometry and spatial boundaries. In this study, we used porous substrates with different pore radii to address precisely the extent of the geometric constraint, permitting us to modulate and investigate the size and mobility of lipid domains in phase-separated continuous pore-spanning membranes (PSMs). Fluorescence video microscopy revealed two types of liquid-ordered (l o ) domains in the freestanding parts of the PSMs: (i) immobile domains that were attached to the pore rims and (ii) mobile, round-shaped l o domains within the center of the PSMs. Analysis of the diffusion of the mobile l o domains by video microscopy and particle tracking showed that the domains' mobility is slowed down by orders of magnitude compared with the unrestricted case. We attribute the reduced mobility to the geometric confinement of the PSM, because the drag force is increased substantially due to hydrodynamic effects generated by the presence of these boundaries. Our system can serve as an experimental test bed for diffusion of 2D objects in confined geometry. The impact of hydrodynamics on the mobility of enclosed lipid domains can have great implications for the formation and lateral transport of signaling platforms. diffusion | hydrodynamics | lipid rafts | membrane dynamics | pore-spanning membranes T he plasma membrane of eukaryotic cells compartmentalizes into lipid domains that enable the selective recruitment of specific proteins (1, 2). These domains are an important feature for regulating biological functions such as apical sorting, protein trafficking, and the clustering of proteins during signaling. The most prominent concept for membrane organization, the lipid raft theory, relates lipid phase separation [driven by interactions between cholesterol (chol), sphingolipids, and saturated phospholipids] to membrane protein partitioning and regulation (2, 3). Lipid domains such as rafts are difficult to observe in biological membranes due to their small size and dynamic nature (4). To understand the phase separation phenomena and the dynamics of lipid domains, the phase behavior of giant plasma membrane-derived vesicles (5, 6) as well as ternary model membranes containing two phospholipid species and chol have been investigated extensively in the last decade. In these model membranes, lipid phase separation between liquid-ordered (l o ) and liquid-disordered (l d ) phases is readily observed at low temperature (7-9). These raft-like domains grow several micrometers in size in giant unilamellar vesicles (GUVs) (7), while their mobility is preserved, whereas lipid domains in supported lipid bilayers are smaller but are largely immobile and do not form energy-minimized round shapes (10). Explanations for the size difference of lipid domains in native plasma membranes and model membranes ran...

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Section: Resultsmentioning

confidence: 99%

Size and mobility of lipid domains tuned by geometrical constraints

Schütte

Mey

Enderlein

et al. 2017

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

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“…Tension has also been hypothesized, but not confirmed, to influence the shapes of solid domains (25). Relevant to the current focus on the thermodynamic role of tension, tension was shown reduce the liquid-liquid coexistence temperature only slightly (a fraction of a Celsius degree for each 0.1 mN/m in tension) in cholesterol-containing phospholipid vesicles (26,27). …”

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confidence: 84%

Large effect of membrane tension on the fluid–solid phase transitions of two-component phosphatidylcholine vesicles

Chen¹,

Santore

2013

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

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Model phospholipid membranes and vesicles have long provided insight into the nature of confined materials and membranes while also providing a platform for drug delivery. The rich thermodynamic behavior and interesting domain shapes in these membranes have previously been mapped in extensive studies that vary temperature and composition; however, the thermodynamic impact of tension on bilayers has been restricted to recent reports of subtly reduced fluidfluid transition temperatures. In two-component phosphatidylcholine unilamellar vesicles [1,2-dioleoyl-sn-glycero-3-phosphocholine (DOPC)/1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC)], we report a dramatic influence of tension on the fluid-solid transition and resulting phases: At fixed composition, systematic variations in tension produce differently shaped solid domains (striped or irregular hexagons), shift fluid-solid transition temperatures, and produce a triple-point-like intersection of coexistence curves at elevated tensions, about 3 mN/m for 30% DOPC/70% DPPC. Tension therefore represents a potential switch of microstructure in responsive engineered materials; it is an important morphology-determining variable in confined systems, and, in biological membranes, it may provide a means to regulate dynamic structure.ripple tilt bilayer | phase diagram | domain morphology | biomimetic membrane | phase separation P hospholipid vesicles, capsular lamellar assemblies of phospholipid amphiphiles, are model systems that have advanced our perceptions of material surfaces and thin films, facilitated drug delivery technologies, and anchored the understanding of biological membranes to fundamental physics. Extensive studies of phase transitions in phospholipid bilayers and vesicles have focused almost exclusively on temperature and composition, revealing complex phase behavior (1-6) and beautiful patterns in the domain shapes within vesicle membranes (4, 6, 7). Tension has been mostly neglected as a thermodynamic variable and is unspecified in phase diagrams of vesicle membranes, although in analogous studies of phospholipid monolayers, surface pressure is known to drive transitions between gas-like layers, liquid fluids, and ordered crystals, which are sometimes polymorphic (8-10). Besides its fundamental thermodynamic importance, membrane tension may be biologically important, because stresses on cells can dominate their interactions (11-14) and fates (15). Indeed, tension has been proposed to regulate the dynamic structure of the cellular surface, for instance through coupling with curvature (16) or by clustering proteins in "rafts" (17, 18).Used as a mechanical variable, tension can stretch or bend uniform bilayers (19,20). In multicomponent vesicles containing coexisting fluid domains, coupling of line tension with membrane bending determines vesicle shapes and drives budding transitions (21-24). Tension has also been hypothesized, but not confirmed, to influence the shapes of solid domains (25). Relevant to the current focus on the thermodynamic role of t...

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“…The effect of surface pressure (or negative surface tension) is an effective increase in the melting transition temperature by a factor P Δ A melt /Δ H melt °, which will slow down the melting rate. 43 We can approximate a pressure-dependent melting rate by substituting T m from eq B1 with a pressure-dependent transition temperature T m ( P ):

- \frac{d A_{gel}}{d t} = C L_{bnd} true(T - T_{normalm} true(1 + \frac{P Δ A_{melt}}{Δ H_{melt}^{normalo}} true) true)

The overall dynamics of melting will then depend on the balance of pressure building up through the area increase associated with melting and the rate of pressure relaxation through changes in vesicle shape and volume, which are implicitly included in the relaxation rate Γ, which would be expected to depend on pressure but may depend on the structural state of the vesicle as well. If we can treat surface relaxation as negligible on the melting time scale, (Γ = 0) then these two equations yield an exponential decay in the gel-phase area until the surface pressure effect on T m halts further melting:

- \frac{Δ A_{gel} (t)}{A_{tot}} = \frac{Δ H^{normalo}}{χ_{melt} κ Δ A} true(\frac{T}{T_{normalm} (0)} - 1 true) true(1 - exp true(- \frac{C L_{bnd}}{A_{tot}} \frac{χ_{melt} κ Δ A}{Δ H^{normalo}} T_{normalm} (0) t true) true)

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confidence: 99%

Dynamics of the Gel to Fluid Phase Transformation in Unilamellar DPPC Vesicles

Nagarajan

Schuler

et al. 2012

J. Phys. Chem. B

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The dynamics of the gel to fluid phase transformation in 100 nm large unilamellar vesicles (LUV) of 1,2-dipalmitoyl(d62)-sn-glycero-3-phosphocholine (d62-DPPC), has been studied by laser-induced temperature-jump initiation coupled with time-resolved infrared spectroscopy and by MD simulations. The infrared transients that characterize the temperature dependent phase transformation are complex, extending from the nanosecond to the millisecond time scales. An initial fast (submicrosecond) component can be modeled by partial melting of the gel domains, initiated at pre-existing defects at the edges of the faceted structure of the gel phase. Molecular dynamics simulations support the model of fast melting from edge defects. The extent of melting during the fast phase is limited by the area expansion on melting, which leads to a surface pressure that raises the effective melting temperature. Subsequent melting is observed to follow highly stretched exponential kinetics, consistent with collective relaxation of the surface pressure through a hierarchy of surface undulations with different relaxation times. The slowest step is water diffusion through the bilayer to allow the vesicle volume to grow along with its expanded surface area. The results demonstrate that the dominant relaxation in the gel to fluid phase transformation in response to a large T-jump perturbation (compared to the transition width) is fast (submicrosecond), which has important practical and fundamental consequences.

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Phase Behavior of Lipid Bilayers under Tension

Cited by 50 publications

References 17 publications

Size and mobility of lipid domains tuned by geometrical constraints

Size and mobility of lipid domains tuned by geometrical constraints

Large effect of membrane tension on the fluid–solid phase transitions of two-component phosphatidylcholine vesicles

Dynamics of the Gel to Fluid Phase Transformation in Unilamellar DPPC Vesicles

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