Differential adsorption of a membrane skeletal protein, spectrin, in phospholipid membranes
About: This article is published in EPL.The article was published on 2017-06-01. It has received 21 citations till now. The article focuses on the topics: Spectrin & Ankyrin.
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TL;DR: The effects of ILs on the nanoscopic dynamics and phase behaviour of a dimyristoylphosphatidylcholine membrane, a model cell membrane, as studied using neutron scattering techniques are reported.
Abstract: Ionic liquids (ILs) are potential candidates for new antimicrobials due to their tunable antibacterial and antifungal properties that are required to keep pace with the growing challenge of bacterial resistance. To a great extent their antimicrobial actions are related to the interactions of ILs with cell membranes. Here, we report the effects of ILs on the nanoscopic dynamics and phase behaviour of a dimyristoylphosphatidylcholine (DMPC) membrane, a model cell membrane, as studied using neutron scattering techniques. Two prototypical imidazolium-based ILs 1-butyl-3-methylimidazolium tetrafluoroborate (BMIM[BF4]) and 1-decyl-3-methylimidazolium tetrafluoroborate (DMIM[BF4]), which differ only in terms of the alkyl chain length of cations, have been used for the present study. Fixed Elastic Window Scan (FEWS) shows that the incorporation of ILs affects the phase behaviour of the phospholipid membrane significantly and the transition from a solid gel to a fluid phase shifts to lower temperature. This is found to be consistent with our differential scanning calorimetry measurements. DMIM[BF4], which has a longer alkyl chain cation, affects the phase behaviour more strongly in comparison to BMIM[BF4]. The pressure–area isotherms of the DMPC monolayer measured at the air–water interface show that in the presence of ILs, isotherms shift towards higher area-per lipid molecule. DMIM[BF4] is found to shift the isotherm to a greater extent compared to BMIM[BF4]. Quasielastic neutron scattering (QENS) data show that both ILs act as a plasticizer, which enhances the fluidity of the membrane. DMIM[BF4] is found to be a stronger plasticizing agent in comparison to BMIM[BF4] that has a cation with a shorter alkyl chain. The incorporation of DMIM[BF4] enhances not only the long range lateral motion but also the localised internal motion of the lipids. On the other hand, BMIM[BF4] acts weakly in comparison to DMIM[BF4] and mainly alters the localised internal motion of the lipids. Any subtle change in the dynamical properties of the membrane can profoundly affect the stability of the cell. Hence, the dominant effect of the IL with the longer chain length on the dynamics of the phospholipid membrane might be correlated with its cytotoxic activity. QENS data analysis has provided a quantitative description of the effects of the two imidazolium-based ILs on the dynamical and phase behaviour of the model cell membrane, which is essential for a detailed understanding of their action mechanism.
46 citations
Stanford University1, University of Hamburg2, University of Michigan3, University of Melbourne4, Lawrence Berkeley National Laboratory5, University of Pennsylvania6, Shanghai Jiao Tong University7, University College Dublin8, University of Kiel9, Karolinska University Hospital10, Nanjing University11, Chinese Academy of Sciences12, Ikerbasque13, European XFEL14, La Trobe University15, Ludwig Maximilian University of Munich16, Saha Institute of Nuclear Physics17, Pennsylvania State University18, German Cancer Research Center19, University of Wisconsin–Milwaukee20, Indian Institute of Science21, University of California, Los Angeles22, Hunan University23, Armenian National Academy of Sciences24
TL;DR: X-ray-based analytics are routinely applied in many fields, including physics, chemistry, materials science, and engineering as discussed by the authors, but the full potential of such techniques in the life sciences and medicine has not yet been fully exploited.
Abstract: X-ray-based analytics are routinely applied in many fields, including physics, chemistry, materials science, and engineering. The full potential of such techniques in the life sciences and medicine, however, has not yet been fully exploited. We highlight current and upcoming advances in this direction. We describe different X-ray-based methodologies (including those performed at synchrotron light sources and X-ray free-electron lasers) and their potentials for application to investigate the nano-bio interface. The discussion is predominantly guided by asking how such methods could better help to understand and to improve nanoparticle-based drug delivery, though the concepts also apply to nano-bio interactions in general. We discuss current limitations and how they might be overcome, particularly for future use in vivo.
45 citations
TL;DR: Different biophysical methods to characterize interactions between ILs and phospholipid membrane, a model biomembrane indicate that ILs interact profoundly with the lipid bilayer and modulate the structure, microscopic dynamics, and phase behavior of the membrane, which could be the fundamental cause of the observed toxicity of ILs.
Abstract: Ionic liquids (ILs) are a special class of low-temperature (typically < 100 °C) molten salts, which have huge upsurge interest in the field of chemical synthesis, catalysis, electrochemistry, pharmacology, and biotechnology, mainly due to their highly tunable nature and exceptional properties. However, practical uses of ILs are restricted mainly due to their adverse actions on organisms. Understanding interactions of ILs with biomembrane is prerequisite to assimilate the actions of these ionic compounds on the organism. Here, we review different biophysical methods to characterize interactions between ILs and phospholipid membrane, a model biomembrane. All these studies indicate that ILs interact profoundly with the lipid bilayer and modulate the structure, microscopic dynamics, and phase behavior of the membrane, which could be the fundamental cause of the observed toxicity of ILs. Effects of ILs on the membrane are found to be strongly dependent on the lipophilicity of the IL and are found to increase with the alkyl chain length of IL. This can be correlated with the observed higher toxicity of IL with the longer alkyl chain length. These informations would be useful to tune the toxicity of IL which is required in designing environment-friendly nontoxic solvents of the so-called green chemistry for various practical applications.
39 citations
TL;DR: The enthalpy and entropy calculated from temperature-dependent pressure–area isotherms of the monolayer show that the added ionic liquids bring about a disordering effect in the lipid film, and the differential scanning calorimetric measurement on a multilamellar vesicle system shows the main phase transition temperature to shift to a lower value, which indicates the dis ordering effect of the ionic liquid on lipid membrane.
Abstract: Understanding the interaction of ionic liquids with cellular membrane becomes utterly important to comprehend the activities of these liquids in living organisms. Lipid monolayer formed at the air–water interface is employed as a model system to follow this interaction by investigating important thermodynamic parameters. The penetration kinetics of the imidazolium-based ionic liquid 1-decyl-3-methylimidazolium tetrafluoroborate ([DMIM][BF4]) into the zwitterionic 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) lipid layer is found to follow the Boltzmann-like equation that reveals the characteristic time constant which is observed to be the function of initial surface pressure. The enthalpy and entropy calculated from temperature-dependent pressure–area isotherms of the monolayer show that the added ionic liquids bring about a disordering effect in the lipid film. The change in Gibbs free energy indicates that an ionic liquid with longer chain has a far greater disordering effect compared to an ionic liquid with shorter chain. The differential scanning calorimetric measurement on a multilamellar vesicle system shows the main phase transition temperature to shift to a lower value, which, again, indicates the disordering effect of the ionic liquid on lipid membrane. All these studies fundamentally point out that, when ionic liquids interact with lipid molecules, the self-assembled structure of a cellular membrane gets perturbed, which may be the mechanism of these molecules having adverse effects on living organisms.
31 citations
Cites background from "Differential adsorption of a membra..."
...The two-dimensional (2D) isothermal compressibility (Cs) can be evaluated from the same isotherms using (Giri et al. 2017a, b): Cs ¼ − 1A δA δπ T ð2Þ where A is the mean molecular area and π is the surface pressure at a given temperature (T)....
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...However, at a given temperature, the peaks are found to be broad in the presence of ILs, suggesting the effect of these ILs on the in-plane organization of the lipid molecules (Giri et al. 2017a, b)....
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TL;DR: The x-ray reflectivity studies on polymer supported lipid bilayer have shown the bilayer to shrink and correspondingly exhibit an increase in electron density, and the presence of a certain mol% of negatively charged lipid, 1,2-dipalmitoyl-rac-glycero-3-phospho-L-serine (DPPS), in DPPC mono- and bi-layers enhances the effect considerably.
29 citations
References
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TL;DR: In this article, the electron density profiles of the fully hydrated fluid phases of DMPC and dilauroylphosphatidylcholine (DLPC) were obtained at 30 degrees C.
565 citations
TL;DR: This research uses an approach representing the outer layers of bacterial and red blood cell membranes with lipid monolayers and using a combination of insertion assay, epifluorescence microscopy, and surface x-ray scattering to gain a better understanding of antimicrobial peptide's mechanism of action.
Abstract: The antimicrobial peptide protegrin-1 (PG-1) interacts with membranes in a manner that strongly depends on membrane lipid composition. In this research we use an approach representing the outer layers of bacterial and red blood cell membranes with lipid monolayers and using a combination of insertion assay, epifluorescence microscopy, and surface x-ray scattering to gain a better understanding of antimicrobial peptide's mechanism of action. We find that PG-1 inserts readily into anionic dipalmitoyl-phosphatidylglycerol, palmitoyl-oleoyl-phosphatidylglycerol, and lipid A films, but significantly less so into zwitterionic dipalmitoyl-phosphatidylcholine, palmitoyl-oleoyl-phosphatidylcholine, and dipalmitoyl-phosphatidylethanolamine monolayers under similar experimental conditions. Epifluorescence microscopy shows that the insertion of PG-1 into the lipid layer results in the disordering of lipid packing; this disordering effect is corroborated by grazing incidence x-ray diffraction data. X-ray reflectivity measurements further point to the location of the peptide in the lipid matrix. In a pathologically relevant example we show that PG-1 completely destabilizes monolayer composed of lipid A, the major component in the outer membrane of Gram-negative bacteria, which is likely to be the mechanism by which PG-1 disrupts the outer membrane, thus allowing it to reach the target inner membrane.
208 citations
79 citations
TL;DR: Shin et al. as discussed by the authors used Monte-Carlo simulation to calculate equilibrium thermodynamic properties of bilayers in the fluid (T = 340 K) or gel (t = 300 K) phases of the bilayer.
56 citations
TL;DR: This elementary system offers a means to replicate the conformational changes that occur with the cellular cytoskeleton and has great potential for fundamental biophysical studies of membrane properties and membrane-protein interactions decoupled from the underlying solid support.
Abstract: A robust and straightforward method for the preparation of lipid membranes upon dynamically responsive polymer cushions is reported. Structural characterization demonstrates that complete, well-packed membranes with tunable mobility can be constructed on the polymeric cushion. With this system, membrane conformational changes induced by cellular cytoskeleton interactions can be modeled. The membrane can be tailored to screen the cushion from changes in pH or allow rapid response to the pH environment by incorporation of protein ion channels. This elementary system offers a means to replicate the conformational changes that occur with the cellular cytoskeleton and has great potential for fundamental biophysical studies of membrane properties and membrane–protein interactions decoupled from the underlying solid support.
31 citations