Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers

Usery, Rebecca D.; Enoki, Thais A.; Wickramasinghe, Sanjula P.; Weiner, Michael D.; Tsai, Wen-Chyan; Kim, Mary B.; Wang, Shu; Torng, Thomas; Ackerman, David G.; Heberle, Frederick A.; Katsaras, John; Feigenson, Gerald W.

doi:10.1016/j.bpj.2017.02.033

Cited by 84 publications

(125 citation statements)

References 65 publications

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“…Thus, this lipid is expected to partition to the L o /L d phase boundary and to act as a linactant. However, the line activity of POPC has not been observed 29,30 . Therefore, the hybrid nature of the molecule is not a prerequisite for the line activity.…”

mentioning

confidence: 98%

Elastic deformations mediate interaction of the raft boundary with membrane inclusions leading to their effective lateral sorting

Pinigin

Kondrashov

Jiménez-Munguía

et al. 2020

Sci Rep

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Liquid-ordered lipid domains represent a lateral inhomogeneity in cellular membranes. these domains have elastic and physicochemical properties different from those of the surrounding membrane. in particular, their thickness exceeds that of the disordered membrane. thus, elastic deformations arise at the domain boundary in order to compensate for the thickness mismatch. in equilibrium, the deformations lead to an incomplete register of monolayer ordered domains: the elastic energy is minimal if domains in opposing monolayers lie on the top of each other, and their boundaries are laterally shifted by about 3 nm. This configuration introduces a region, composed of one ordered and one disordered monolayers, with an intermediate bilayer thickness. Besides, a jump in a local monolayer curvature takes place in this intermediate region, concentrating here most of the elastic stress. This region can participate in a lateral sorting of membrane inclusions by offering them an optimal bilayer thickness and local curvature conditions. In the present study, we consider the sorting of deformable lipid inclusions, undeformable peripheral and deeply incorporated peptide inclusions, and undeformable transmembrane inclusions of different molecular geometry. With rare exceptions, all types of inclusions have an affinity to the ordered domain boundary as compared to the bulk phases. the optimal lateral distribution of inclusions allows relaxing the elastic stress at the boundary of domains.Cellular membranes are laterally heterogeneous 1-3 . Many membrane proteins are believed to function properly only inside lipid-protein domains, also referred to as rafts 4-7 . Proteins in these domains are surrounded by a more or less thick lipid shell [8][9][10][11] . In model purely lipidic systems it is demonstrated that lipids can form similar domains, in which they are in a liquid-ordered (L o ) phase state, while the surrounding membrane is liquid-disordered (L d ) [12][13][14][15] . Ordered domains are usually bilayer, i.e. exist in both membrane leaflets at the same lateral position [14][15][16][17] . Such transbilayer coupling could be driven by elastic deformations arising at the domain boundary and by membrane thermal fluctuations 18-21 . The mechanism of this coupling is not specific to the exact lipid composition of the domain: only the higher ordering of lipids with respect to the surrounding membrane is important [22][23][24] . A bilayer structure of rafts is believed to be a key property in providing raft-dependent signal transduction across the plasma membrane 4,5 . There are increasing evidences that a raft interior itself may be laterally inhomogeneous: some molecules may prefer its boundary region rather than its bulk part. In particular, the fusion peptide of the human immunodeficiency virus (HIV) gp41 protein functions with the highest efficiency only in the presence of the L o /L d phase boundary in the target membrane 25,26 . In addition, the HIV receptor CCR5 preferentially localizes at the domain boundary 26 . It means t...

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mentioning

confidence: 98%

Elastic deformations mediate interaction of the raft boundary with membrane inclusions leading to their effective lateral sorting

Pinigin

Kondrashov

Jiménez-Munguía

et al. 2020

Sci Rep

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“…In this respect, thicker Lo phases are known to have higher bending rigidities that Ld phases. For example, measured ratios are κ Lo /κ Ld 5 in reference [62] and 4 in reference [63], a range of values confirmed in more recent studies measuring ratios up to 10 [32,33]. Membrane stability requires that −2 < κ G /κ < 0 (see, e.g., [64]).…”

Section: In Thermodynamic Equilibriummentioning

confidence: 60%

“…In the strong segregation limit, the typical values of λ are measured to be on the order of a few pN [25,33,105,106,107].…”

Section: Strong Segregation Limitmentioning

confidence: 99%

“…To confirm the decisive role played by line tension in the coexistence region below the demixing temperature on GUVs, a very recent work by Feigenson and coworkers [33] explored a large variety of 4-component mixtures of the (high-T m PC or sphingomyelin)/low-T m PC(s)/cholesterol type. In particular, the bSM/DOPC/POPC/cholesterol mixture of [29], as just mentioned above, is also included in this study and does display mesophases on GUVs, thus confirming our previous statement.…”

Section: Effect Of Volume Constraintmentioning

confidence: 99%

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A rationale for mesoscopic domain formation in biomembranes

Destainville

Manghi

Cornet

2018

Preprint

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Cell plasma membranes display a dramatically rich structural complexity characterized by functional sub-wavelength domains with specific lipid and protein composition. Under favorable experimental conditions, patterned morphologies can also be observed in vitro on model systems such as supported membranes or lipid vesicles. Lipid mixtures separating in liquid-ordered and liquid-disordered phases below a demixing temperature play a pivotal role in this context. Protein-protein and protein-lipid interactions also contribute to membrane shaping by promoting small domains or clusters. Such phase separations displaying characteristic length-scales falling in-between the nanoscopic, molecular scale on the one hand and the macroscopic scale on the other hand, are named mesophases in soft condensed matter physics. In this review, we propose a classification of the diverse mechanisms leading to mesophase separation in biomembranes. We distinguish between mechanisms relying upon equilibrium thermodynamics and those involving out-of-equilibrium mechanisms, notably active membrane recycling. In equilibrium, we especially focus on the many mechanisms that dwell on an up-down symmetry breaking between the upper and lower bilayer leaflets. Symmetry breaking is an ubiquitous mechanism in condensed matter physics at the heart of several important phenomena. In the present case, it can be either spontaneous (domain buckling) or explicit, i.e., due to an external cause (global or local vesicle bending properties). Whenever possible, theoretical predictions and simulation results are confronted to experiments on model systems or living cells, which enables us to identify the most realistic mechanisms from a biological perspective.

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“…Over the past 15 years, many investigations have focused on ternary mixtures of Chol with one high and one low melting temperature (T m ) lipid species. (16) Multiple points on phase diagrams of lipid bilayer phase separations resulting from mixtures of saturated lipids, unsaturated lipids, and cholesterol have been observed using fluorescence spectroscopy, (17,18,(27)(28)(29)(30)(31)(32)(33)(34)(19)(20)(21)(22)(23)(24)(25)(26) x-ray scattering, (20,(35)(36)(37)(38)(39)(40) atomic force microscopy (AFM), (18,37,41,42) NMR, (24,30,32,43,44)interferometric scattering, (45) and Raman spectroscopy, (46,47) allowing us to achieve a general concept of ternary lipid mixture phase diagrams.…”

Section: Tous(2)mentioning

confidence: 99%

Regimes of Complex Lipid Bilayer Phases Induced by Cholesterol Concentration in MD Simulation

Pantelopulos

Straub

2018

Preprint

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Cholesterol is essential to the formation of phase separated lipid domains in membranes. Lipid domains can exist in different thermodynamic phases depending on the molecular composition, and play significant roles in determining structure and function of membrane proteins. We investigate the role of cholesterol in the structure and dynamics of ternary lipid mixtures displaying phase separation using Molecular Dynamics simulations, employing a physiologically-relevant span of cholesterol concentration. We find that cholesterol can induce formation of three regimes of phase behavior, I) miscible liquid disordered bulk, II) phase separated, domain registered coexistence of liquid disordered and liquid ordered and domains, and III) phase separated, domain-antiregistered coexistence of liquid-disordered and newly-identified nanoscopic gel domains composed of cholesterol threads we name "cholesterolic gel" domains. These findings are validated and discussed in the context of current experimental knowledge, models of cholesterol spatial distributions, and models of ternary lipid mixture phase separation.These collected observations substantially enhance our understanding of the role of Chol in complex phase behavior in ternary lipid mixtures and provide a framework for exploring structure and dynamics of domain formation in future computational, theoretical, and experimental investigations. ASSOCIATED CONTENT Supporting InformationSee supporting information for illustrative demonstrations of order parameters mix , ) , and f , explanation and illustraton of 50% miscibility mapping to mix , and visualizations of f and | f | in all systems. Additionally, order parameters measured for transleaflet clusters and illustrative demonstration of the clustering approach used is supplied.

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Line Tension Controls Liquid-Disordered + Liquid-Ordered Domain Size Transition in Lipid Bilayers

Cited by 84 publications

References 65 publications

Elastic deformations mediate interaction of the raft boundary with membrane inclusions leading to their effective lateral sorting

Elastic deformations mediate interaction of the raft boundary with membrane inclusions leading to their effective lateral sorting

A rationale for mesoscopic domain formation in biomembranes

Regimes of Complex Lipid Bilayer Phases Induced by Cholesterol Concentration in MD Simulation

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