Bending rigidity of charged lipid bilayer membranes

Faizi, Hammad A.; Frey, Shelli L.; Steinkühler, Jan; Dimova, Rumiana; Vlahovska, Petia M.

doi:10.1039/c9sm00772e

Cited by 109 publications

(119 citation statements)

References 57 publications

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“…The predictive power of the proposed mechanism relies on the ability to independently control interlamellar forces and bending rigidity, a requirement that is likely not strictly met in any real experiment. In some cases, the different influences reinforce each other: for example, it is well established that adding charged lipid to neutral bilayers increases lamellar separation which in turn reduces bilayer adhesion (14), and there is evidence that charged lipid can also increase membrane bending rigidity (15,16). Both of these factors favor unilamellarity, consistent with experimental observations reported here.…”

Section: Statement Of Significancesupporting

confidence: 86%

“…For example, the addition of monovalent salt has been shown to reduce attractive van der Waals forces in neutral bilayers (17,18), but also decrease interbilayer separation (and thereby increase adhesion) in charged bilayers through screening effects (the Debye length decreases by three orders of magnitude between pure water and physiological salt concentration). Moreover, NaCl has been shown to increase the bending rigidity of POPC multilayers (19) but decrease the bending rigidity of POPC giant unilamellar vesicles (16). Divalent cations are even more complicated due to their ability to tightly bind acidic headgroups (20).…”

Section: Statement Of Significancementioning

confidence: 99%

See 1 more Smart Citation

On the mechanism of bilayer separation by extrusion; or, why your large unilamellar vesicles are not really unilamellar

Scott

Skinkle

Kelley

et al. 2019

Preprint

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Extrusion through porous filters is a widely used method for preparing biomimetic model membranes. Of primary importance in this approach is the efficient production of single bilayer (unilamellar) vesicles that eliminate the influence of interlamellar interactions and strictly define the bilayer surface area available to external reagents such as proteins. Sub-microscopic vesicles produced using extrusion are widely assumed to be unilamellar, and large deviations from this assumption would dramatically impact interpretations from many model membrane experiments. Using three probe-free methods—small-angle X-ray and neutron scattering (SAXS and SANS) and cryogenic electron microscopy (cryoEM)—we report unambiguous evidence of extensive multilamellarity in extruded vesicles composed of neutral phosphatidylcholine lipids, including for the common case of neutral lipids dispersed in physiological buffer and extruded through 100 nm diameter pores. In such preparations, only ~35% of lipids are externally accessible, and this fraction is highly dependent on preparation conditions. Charged lipids promote unilamellarity, as does decreasing solvent ionic strength, indicating the importance of electrostatic interactions in determining the lamellarity of extruded vesicles. Smaller extrusion pore sizes also robustly increase the fraction of unilamellar vesicles, suggesting a role for membrane bending. Taken together, these observations suggest a mechanistic model for extrusion, wherein formation of unilamellar vesicles involves competition between bilayer bending and adhesion energies. The findings presented here have wide-ranging implications for the design and interpretation of model membrane studies, especially ensemble-averaged observations relying on the assumption of unilamellarity.STATEMENT OF SIGNIFICANCEExtruded vesicles are a ubiquitous tool in membrane research. It is widely presumed that extrusion produces unilamellar (i.e., single bilayer) vesicles, an assumption that is often crucial for data analysis and interpretation. Using X-ray and neutron scattering and cryogenic electron microscopy, we show that a substantial amount of lipid remains inaccessible after extrusion due to an abundance of multilamellar vesicles (MLVs). While this is a general phenomenon for neutral lipids, MLV contamination can be reduced by several complementary approaches such as including charged lipids in the mixture, reducing the ionic strength of the aqueous medium, and reducing the extrusion pore size. These observations together suggest a mechanism by which extrusion strips MLVs of their layers.

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Section: Statement Of Significancesupporting

confidence: 86%

Section: Statement Of Significancementioning

confidence: 99%

On the mechanism of bilayer separation by extrusion; or, why your large unilamellar vesicles are not really unilamellar

Scott

Skinkle

Kelley

et al. 2019

Preprint

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“…We will incorporate fluctuating hydrodynamics into the boundary integral formulation to extract physical properties of the lipid bilayer membrane such as membrane diffusivity, bending rigidity and the surface tension. By modification of the interfacial labels, HADF can account for charged lipids and study their impact on elastic properties of bilayer [20]. Since we have immersed the particles in a zero-Reynolds flow, it is possible to study the rheological properties of micelle networks in large particle simulations [50].…”

Section: Conclusion Topological Transitions Of a Lipid Bilayer Membmentioning

confidence: 99%

Simulation of Multiscale Hydrophobic Lipid Dynamics via Efficient Integral Equation Methods

Fu¹,

Ryham²,

Klöckner³

et al. 2020

Multiscale Model. Simul.

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In this paper a mathematical model for long-range, hydrophobic attraction between amphiphilic particles is developed to quantify the macroscopic assembly and mechanics of a lipid bilayer membrane in solvents. The non-local interactions between amphiphilic particles are obtained from the first domain variation of a hydrophobicity functional, giving rise to forces and torques (between particles) that dictate the motion of both particles and the surrounding solvent. The functional minimizer (that accounts for hydrophobicity at molecular-aqueous interfaces) is a solution to a boundary value problem of the screened Laplace equation. We reformulate the boundary value problem as a second-kind integral equation (SKIE), discretize the SKIE using a Nyström discretization and 'Quadrature by Expansion' (QBX) and solve the resulting linear system iteratively using GMRES. We evaluate the required layer potentials using the 'GIGAQBX' fast algorithm, a variant of the Fast Multipole Method (FMM), yielding the required particle interactions with asymptotically optimal cost. Solving a mobility problem in Stokes flow is incorporated to obtain corresponding rigid body motion. The simulated fluid-particle systems exhibit a variety of multiscale behaviors over both time and length: Over short time scales, the numerical results show self-assembly for model lipid particles. For large system simulations, the particles form realistic configurations like micelles and bilayers. Over long time scales, the bilayer shapes emerging from the simulation appear to minimize a form of bending energy.

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“…The fluctuating amplitudes have variance dependent on the membrane bending rigidity and tension. Imaging is most commonly done by phase contrast microscopy [1,7,15,[17][18][19][20][21][22] but other methods such as confocal [23][24][25] and light sheet microscopy [26] have also been employed. The increased variety of imaging methods raises the question if they all yield the same results.…”

mentioning

confidence: 99%

“…However, comparing bending rigidity numbers obtained by different imaging techniques is only meaningful if the same system is probed. It is known that many factors such as sugars (and gravity), salt, buffers, solution asymmetry, concentration of fluorescent lipids, preparation method or type of bilayer configuration (stacked or free-floating), influence the measured mechanical properties of bilayer membranes [1,18,[27][28][29][30][31]. For example, even measurements with the same method can give wide range of values, e.g., the bending rigidity of a DOPC bilayer measured with flickering spectroscopy has been reported form 15 k B T [24] to 27 k B T [32], where k B T is the thermal energy; see Table 1 in the Supporting Information (SI) for a comprehensive list.…”

mentioning

confidence: 99%

Fluctuation spectroscopy of giant unilamellar vesicles using confocal and phase contrast microscopy

Faizi¹,

Reeves

Georgiev

et al. 2020

Preprint

Self Cite

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A widely used method to measure the bending rigidity of bilayer membranes is fluctuation spectroscopy, which analyses the thermally-driven membrane undulations of giant unilamellar vesicles recorded with either phase-contrast or confocal microscopy. Here, we analyze the fluctuations of the same vesicle using both techniques and obtain consistent values for the bending modulus. We discuss the factors that may lead to discrepancies.

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Bending rigidity of charged lipid bilayer membranes

Abstract: We experimentally study the increase of bending rigidity with charge content of bilayer membranes using GUVs made of a mixture of neutral and monovalent negatively charged lipids.

Cited by 109 publications

References 57 publications

On the mechanism of bilayer separation by extrusion; or, why your large unilamellar vesicles are not really unilamellar

On the mechanism of bilayer separation by extrusion; or, why your large unilamellar vesicles are not really unilamellar

Simulation of Multiscale Hydrophobic Lipid Dynamics via Efficient Integral Equation Methods

Fluctuation spectroscopy of giant unilamellar vesicles using confocal and phase contrast microscopy

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