Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes

Nickels, Jonathan D.; Smith, Jeremy C.; Cheng, Xiaolin

doi:10.1016/j.chemphyslip.2015.07.012

Cited by 108 publications

(117 citation statements)

References 202 publications

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“…Contributing factors to domain registration could be transmembrane proteins, lipid interdigitation, membrane curvature, line tension, cholesterol flip-flop, and electrostatic interactions (Nickels et al, 2015) of which chain interdigitation has been invoked as the major contributing factor (May, 2009) but also has been totally dismissed (Collins, 2008). A recent experimental determination of the strength of the coupling parameter that causes domain registration matches a theoretical predictions with values around 0.01 k B T /nm 2 (Putzel et al, 2011; Blosser et al, 2015), but considerably higher values have also been suggested from theoretical considerations (May, 2009).…”

Section: The Registration Of Membrane Nanodomains In the Two Leafletsmentioning

confidence: 99%

Interleaflet Coupling, Pinning, and Leaflet Asymmetry—Major Players in Plasma Membrane Nanodomain Formation

Fujimoto

Parmryd

2017

Front. Cell Dev. Biol.

111

114

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The plasma membrane has a highly asymmetric distribution of lipids and contains dynamic nanodomains many of which are liquid entities surrounded by a second, slightly different, liquid environment. Contributing to the dynamics is a continuous repartitioning of components between the two types of liquids and transient links between lipids and proteins, both to extracellular matrix and cytoplasmic components, that temporarily pin membrane constituents. This make plasma membrane nanodomains exceptionally challenging to study and much of what is known about membrane domains has been deduced from studies on model membranes at equilibrium. However, living cells are by definition not at equilibrium and lipids are distributed asymmetrically with inositol phospholipids, phosphatidylethanolamines and phosphatidylserines confined mostly to the inner leaflet and glyco- and sphingolipids to the outer leaflet. Moreover, each phospholipid group encompasses a wealth of species with different acyl chain combinations whose lateral distribution is heterogeneous. It is becoming increasingly clear that asymmetry and pinning play important roles in plasma membrane nanodomain formation and coupling between the two lipid monolayers. How asymmetry, pinning, and interdigitation contribute to the plasma membrane organization is only beginning to be unraveled and here we discuss their roles and interdependence.

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Section: The Registration Of Membrane Nanodomains In the Two Leafletsmentioning

confidence: 99%

Interleaflet Coupling, Pinning, and Leaflet Asymmetry—Major Players in Plasma Membrane Nanodomain Formation

Fujimoto

Parmryd

2017

Front. Cell Dev. Biol.

111

114

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“…The first widely accepted membrane model (2), the so-called “fluid mosaic model”, assumes that phospholipids are merely structural molecules in which membrane proteins can move freely. This passive description of the membrane lipids is increasingly challenged by recent findings (3, 4, 5, 6). Studies have shown that the membrane is a highly dynamical structure that actively supports the cell function.…”

Section: Introductionmentioning

confidence: 98%

“…Studies have shown that the membrane is a highly dynamical structure that actively supports the cell function. Phospholipids play an important role in this new understanding, for example in conferring membrane curvature (7) and actively organizing proteins complexes (6, 8). Despite these advances, our molecular-level understanding of plasma membranes is still limited, partly due to a lack of experimental results.…”

Section: Introductionmentioning

confidence: 99%

“…Solid-supported membranes are typically immersed in aqueous solution, and only a few nanometers of the solution separate the membrane from the solid support (18). This approach effectively confines the membrane in two dimensions, hence facilitating high-resolution investigations with techniques such as atomic force microscopy (19), fluorescence microscopy (20), fluorescence recovery after photobleaching (FRAP) (21), quartz crystal microbalance (22), and neutron reflectometry (6). Synthetic supported lipid bilayers (23) (SLBs) are routinely used in experimental studies, including for investigating the influence of proteins (24, 25), antibodies (26), functionalized nanoparticles (27), polymers (28), amino acids (29), and antimicrobial peptides (30) on the morphology and biophysical properties of the membrane.…”

Section: Introductionmentioning

confidence: 99%

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Ions Modulate Stress-Induced Nanotexture in Supported Fluid Lipid Bilayers

Piantanida

Bolt

Rozatian

et al. 2017

Biophysical Journal

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Most plasma membranes comprise a large number of different molecules including lipids and proteins. In the standard fluid mosaic model, the membrane function is effected by proteins whereas lipids are largely passive and serve solely in the membrane cohesion. Here we show, using supported 1,2-dioleoyl-sn-glycero-3-phosphocholine lipid bilayers in different saline solutions, that ions can locally induce ordering of the lipid molecules within the otherwise fluid bilayer when the latter is supported. This nanoordering exhibits a characteristic length scale of ∼20 nm, and manifests itself clearly when mechanical stress is applied to the membrane. Atomic force microscopy (AFM) measurements in aqueous solutions containing NaCl, KCl, CaCl2, and Tris buffer show that the magnitude of the effect is strongly ion-specific, with Ca2+ and Tris, respectively, promoting and reducing stress-induced nanotexturing of the membrane. The AFM results are complemented by fluorescence recovery after photobleaching experiments, which reveal an inverse correlation between the tendency for molecular nanoordering and the diffusion coefficient within the bilayer. Control AFM experiments on other lipids and at different temperatures support the hypothesis that the nanotexturing is induced by reversible, localized gel-like solidification of the membrane. These results suggest that supported fluid phospholipid bilayers are not homogenous at the nanoscale, but specific ions are able to locally alter molecular organization and mobility, and spatially modulate the membrane’s properties on a length scale of ∼20 nm. To illustrate this point, AFM was used to follow the adsorption of the membrane-penetrating antimicrobial peptide Temporin L in different solutions. The results confirm that the peptides do not absorb randomly, but follow the ion-induced spatial modulation of the membrane. Our results suggest that ionic effects have a significant impact for passively modulating the local properties of biological membranes, when in contact with a support such as the cytoskeleton.

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“…[13] Through these techniques, a vivid picture of the membrane has emerged. [14–19] Nonetheless, they have significant limitations, and fundamental questions about the ultrastructure of the membrane in vivo remain unresolved. [20]…”

Section: Introductionmentioning

confidence: 99%

The in vivo structure of biological membranes and evidence for lipid domains

et al. 2017

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Examining the fundamental structure and processes of living cells at the nanoscale poses a unique analytical challenge, as cells are dynamic, chemically diverse, and fragile. A case in point is the cell membrane, which is too small to be seen directly with optical microscopy and provides little observational contrast for other methods. As a consequence, nanoscale characterization of the membrane has been performed ex vivo or in the presence of exogenous labels used to enhance contrast and impart specificity. Here, we introduce an isotopic labeling strategy in the gram-positive bacterium Bacillus subtilis to investigate the nanoscale structure and organization of its plasma membrane in vivo. Through genetic and chemical manipulation of the organism, we labeled the cell and its membrane independently with specific amounts of hydrogen (H) and deuterium (D). These isotopes have different neutron scattering properties without altering the chemical composition of the cells. From neutron scattering spectra, we confirmed that the B. subtilis cell membrane is lamellar and determined that its average hydrophobic thickness is 24.3 ± 0.9 Ångstroms (Å). Furthermore, by creating neutron contrast within the plane of the membrane using a mixture of H- and D-fatty acids, we detected lateral features smaller than 40 nm that are consistent with the notion of lipid rafts. These experiments—performed under biologically relevant conditions—answer long-standing questions in membrane biology and illustrate a fundamentally new approach for systematic in vivo investigations of cell membrane structure.

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Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes

Cited by 108 publications

References 202 publications

Interleaflet Coupling, Pinning, and Leaflet Asymmetry—Major Players in Plasma Membrane Nanodomain Formation

Interleaflet Coupling, Pinning, and Leaflet Asymmetry—Major Players in Plasma Membrane Nanodomain Formation

Ions Modulate Stress-Induced Nanotexture in Supported Fluid Lipid Bilayers

The in vivo structure of biological membranes and evidence for lipid domains

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