Extensive Bilayer Perforation Coupled with the Phase Transition Region of an Anionic Phospholipid

Riske, Karin A.; Amáral, L. Q.; Lamy, M. Teresa

doi:10.1021/la9012137

Cited by 43 publications

(96 citation statements)

References 35 publications

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“…The fact that during equilibration the vesicle radius as well as the pore sizes were relaxed (as in the twogradient calculations discussed above) proves once again that under the specified conditions the pores in the vesicles are thermodynamically stable. It also serves as a proof of principle that vesicles with many pores can exist and that it is very well imaginable that indeed the "disappearing" vesicles observed by Riske et al 8 were undergoing a phase transition from a closed state to a porous one.…”

Section: Poresmentioning

confidence: 85%

“…11 are used and displayed here as a set of polynomial fits to those data (Eqs. [8][9][10][11][12][13][14][15][16].…”

Section: Theorymentioning

confidence: 99%

“…18, 21, and 22. However, there are other scenarios dramatically exemplified by the phosphatidylglycerol (PG) bilayers studied by Riske et al 8 The general thermodynamic scenarios are basically known. 20,23 When the edge energy is sufficiently positive, thermodynamically stable edges do not exist and pores only form when the bilayers are under tension.…”

Section: Introductionmentioning

confidence: 99%

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On the edge energy of lipid membranes and the thermodynamic stability of pores

Pera

Kleijn

Leermakers

2015

The Journal of Chemical Physics

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To perform its barrier function, the lipid bilayer membrane requires a robust resistance against pore formation. Using a self-consistent field (SCF) theory and a molecularly detailed model for membranes composed of charged or zwitterionic lipids, it is possible to predict structural, mechanical, and thermodynamical parameters for relevant lipid bilayer membranes. We argue that the edge energy in membranes is a function of the spontaneous lipid monolayer curvature, the mean bending modulus, and the membrane thickness. An analytical Helfrich-like model suggests that most bilayers should have a positive edge energy. This means that there is a natural resistance against pore formation. Edge energies evaluated explicitly in a two-gradient SCF model are consistent with this. Remarkably, the edge energy can become negative for phosphatidylglycerol (e.g., dioleoylphosphoglycerol) bilayers at a sufficiently low ionic strength. Such bilayers become unstable against the formation of pores or the formation of lipid disks. In the weakly curved limit, we study the curvature dependence of the edge energy and evaluate the preferred edge curvature and the edge bending modulus. The latter is always positive, and the former increases with increasing ionic strength. These results point to a small window of ionic strengths for which stable pores can form as too low ionic strengths give rise to lipid disks. Higher order curvature terms are necessary to accurately predict relevant pore sizes in bilayers. The electric double layer overlap across a small pore widens the window of ionic strengths for which pores are stable.

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Section: Poresmentioning

confidence: 85%

“…11 are used and displayed here as a set of polynomial fits to those data (Eqs. [8][9][10][11][12][13][14][15][16].…”

Section: Theorymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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On the edge energy of lipid membranes and the thermodynamic stability of pores

Pera

Kleijn

Leermakers

2015

The Journal of Chemical Physics

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“…Our conclusion is that agarose vesicles should not be employed for instance when extracting membrane properties from vesicle deformation (4,35), pore formation by membrane active molecules (8,42,43), protein-induced membrane curvature (44)(45)(46), initial steps in membrane solubilization by detergents (47,48), and vesicle reshaping during changes in the phase state of the bilayer (7,49). On the other hand, studies focusing on membrane properties such as lateral mobility of membrane components and phase separation, or membrane protein reconstitution might still profit from the use of agarose-GUVs.…”

Section: Discussionmentioning

confidence: 99%

Giant Unilamellar Vesicles Formed by Hybrid Films of Agarose and Lipids Display Altered Mechanical Properties

Lira

Dimova

Riske

2014

Biophysical Journal

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Giant unilamellar vesicles (GUVs) are presumably the current most popular biomimetic membrane model. Preparation of GUVs in physiological conditions using the classical electroformation method is challenging. To circumvent these difficulties, a new method was recently reported, by which GUVs spontaneously swell from hybrid films of agarose and lipids. However, agarose is left encapsulated in the vesicles in different amounts. In this work, we thoroughly characterize the mechanical properties of these agarose-GUVs in response to electric pulses, which induce vesicle deformation and can lead to membrane poration. We show that the relaxation dynamics of deformed vesicles, both in the presence and absence of poration, is significantly slowed down for agarose-GUVs when compared to agarose-free GUVs. In the presence of poration, agarose polymers prevent complete pore closure and lead to high membrane permeability. A fraction of the vesicles were found to encapsulate agarose in the form of a gel-like meshwork. These vesicles rupture and open up after electroporation and the meshwork is expelled through a macropore. When the agarose-GUVs are heated above the melting temperature of agarose for 2 h before use, vesicle response is (partially) recovered due to substantial release of encapsulated agarose during temperature treatment. Our findings reveal potential artifactual behavior of agarose-GUVs in processes involving morphological changes in the membrane as well as poration.

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“…single-component system [37]. Within a temperature range from 25℃ to 28℃, a large number of pores were formed on GUVs consisting of DMPG (-) .…”

Section: ⅰ Introductionmentioning

confidence: 99%

Coupling between pore formation and phase separation in charged lipid membranes

et al. 2015

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We investigated the effect of charge on the membrane morphology of giant unilamellar vesicles (GUVs) composed of various mixtures containing charged lipids. We observed the membrane morphologies by fluorescent and confocal laser microscopy in lipid mixtures consisting of a neutral unsaturated lipid [dioleoylphosphatidylcholine (DOPC)], a neutral saturated lipid [dipalmitoylphosphatidylcholine (DPPC)], a charged unsaturated lipid [dioleoylphosphatidylglycerol (DOPG (-) )], a charged saturated lipid[dipalmitoylphosphatidylglycerol (DPPG (-) )], and cholesterol (Chol). In binary mixtures of neutral DOPC/DPPC and charged DOPC/DPPG (-) , spherical vesicles were formed. On the other hand, pore formation was often observed with GUVs consisting of DOPG (-) and DPPC.In a DPPC/DPPG (-) /Chol ternary mixture, pore-formed vesicles were also frequently observed. The percentage of pore-formed vesicles increased with the DPPG (-) concentration.Moreover, when the head group charges of charged lipids were screened by the addition of salt, pore-formed vesicles were suppressed in both the binary and ternary charged lipid mixtures. We discuss the mechanisms of pore formation in charged lipid mixtures and the relationship between phase separation and the membrane morphology. Finally, we reproduce the results seen in experimental systems by using coarse-grained molecular dynamics simulations. Ⅰ. INTRODUCTIONThe basic structure of a biomembrane is a lipid bilayer that is composed of various types of phospholipids. Biomembranes not only separate the inner and outer environments of living cells, but also play a role in a wide range of life-related phenomena through dynamic structural changes. In biomembranes, the components are not uniformly dispersed, and it is believed that such compositional heterogeneity emerges spontaneously. This heterogeneous structure is known as a "lipid raft" [1][2][3]. Lipid rafts, which are enriched with saturated lipids, cholesterol, or various membrane proteins, are expected to function as platforms to which proteins are attached during signal transduction and membrane trafficking [4,5].Synthetic lipid vesicles consisting of several lipid molecules are commonly used as models of biomembranes to investigate the physicochemical properties of lipid membranes. In particular, ternary lipid mixtures consisting of a saturated lipid, unsaturated lipid, and cholesterol exhibit phase separation between the saturated lipid and the cholesterol-rich phase (the liquid-ordered (Lo) phase) and the unsaturated lipid-rich phase (the liquid-disordered (Ld) phase) [6,7]. The spontaneous domain formation that results from this phase separation has attracted great attention in connection to raft formation in biomembranes.Most previous studies have investigated the primary physical properties of lipid membranes composed of electrically neutral lipids [6,8]. However, biomembranes also contain negatively charged lipids. For instance, the membranes of prokaryotes such asStaphylococcus aureus and Escherichia co...

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Extensive Bilayer Perforation Coupled with the Phase Transition Region of an Anionic Phospholipid

Cited by 43 publications

References 35 publications

On the edge energy of lipid membranes and the thermodynamic stability of pores

On the edge energy of lipid membranes and the thermodynamic stability of pores

Giant Unilamellar Vesicles Formed by Hybrid Films of Agarose and Lipids Display Altered Mechanical Properties

Coupling between pore formation and phase separation in charged lipid membranes

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