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Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape.

ABSTRACT: A fundamental feature of cellular plasma membranes (PMs) is an asymmetric lipid distribution between the bilayer leaflets. However, neither the detailed, comprehensive compositions of individual PM leaflets nor how these contribute to structural membrane asymmetries have been defined. We report the distinct lipidomes and biophysical properties of both monolayers in living mammalian PMs. Phospholipid unsaturation is dramatically asymmetric, with the cytoplasmic leaflet being approximately twofold more unsaturated than the exoplasmic leaflet. Atomistic simulations and spectroscopy of leaflet-selective fluorescent probes reveal that the outer PM leaflet is more packed and less diffusive than the inner leaflet, with this biophysical asymmetry maintained in the endocytic system. The structural asymmetry of the PM is reflected in the asymmetric structures of protein transmembrane domains. These structural asymmetries are conserved throughout Eukaryota, suggesting fundamental cellular design principles.

SUBMITTER: Lorent JH

PROVIDER: S-EPMC7246138 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape.

Lorent J H JH Levental K R KR Ganesan L L Rivera-Longsworth G G Sezgin E E Doktorova M M Lyman E E Levental I I

Nature chemical biology 20200504 6

A fundamental feature of cellular plasma membranes (PMs) is an asymmetric lipid distribution between the bilayer leaflets. However, neither the detailed, comprehensive compositions of individual PM leaflets nor how these contribute to structural membrane asymmetries have been defined. We report the distinct lipidomes and biophysical properties of both monolayers in living mammalian PMs. Phospholipid unsaturation is dramatically asymmetric, with the cytoplasmic leaflet being approximately twofold ...[more]

PMID: 32367017

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Project description:Biological membranes are composed of lipid bilayers that are often asymmetric with regards to the lipid composition and/or aqueous solvent they separate. Studying lipid asymmetry both experimentally and computationally is challenging. Molecular dynamics simulations of lipid bilayers with asymmetry are difficult due to finite system sizes and time scales accessible to simulations. Due to the very slow flip-flop rate for phospholipids, one must first choose how many lipids are on each side of the bilayer, but the resulting bilayer may be unstable (or metastable) due to differing tensile and compressive forces between leaflets. Here we use molecular dynamics simulations to investigate a number of different asymmetric membrane systems, both with atomistic and coarse-grained models. Asymmetries studied include differences in number of lipids, lipid composition (unsaturated and saturated tails and different headgroups), and chemical gradients between the aqueous phases. Extensive analysis of the bilayers' properties such as area per lipid, density, and lateral pressure profiles are used to characterize bilayer asymmetry. We also address how cholesterol (which flip-flops relatively quickly) influences membrane asymmetries. Our results show how each leaflet is influenced by the other and can mitigate the structural changes to the bilayer overall structure. Cholesterol can respond to changes in bilayer asymmetry to alleviate some of the effect on the bilayer structure, but that will alter its leaflet distribution, which in turn affects its chemical potential. Ionic imbalances are shown to have a modest change in bilayer structure, despite large changes in the electrostatic potential. Bilayer asymmetry can also induce a modest electrostatic potential across the membrane. Our results highlight the importance of membrane asymmetry on bilayer properties, the influence of lipid headgroups, tails and cholesterol on asymmetry, and the ability of lipids to adapt to different environments.

Dataset Information

Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape.

Publications

Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape.

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