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      Lipidomic and biophysical homeostasis of mammalian membranes counteracts dietary lipid perturbations to maintain cellular fitness

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          Abstract

          Proper membrane physiology requires maintenance of biophysical properties, which must be buffered from external perturbations. While homeostatic adaptation of membrane fluidity to temperature variation is a ubiquitous feature of ectothermic organisms, such responsive membrane adaptation to external inputs has not been directly observed in mammals. Here, we report that challenging mammalian membranes by dietary lipids leads to robust lipidomic remodeling to preserve membrane physical properties. Specifically, exogenous polyunsaturated fatty acids are rapidly incorporated into membrane lipids, inducing a reduction in membrane packing. These effects are rapidly compensated both in culture and in vivo by lipidome-wide remodeling, most notably upregulation of saturated lipids and cholesterol, resulting in recovery of membrane packing and permeability. Abrogation of this response results in cytotoxicity when membrane homeostasis is challenged by dietary lipids. These results reveal an essential mammalian mechanism for membrane homeostasis wherein lipidome remodeling in response to dietary lipid inputs preserves functional membrane phenotypes.

          Abstract

          Proper membrane physiology requires maintenance of a narrow range of physicochemical properties, which must be buffered from external perturbations. Here, authors report lipidomic remodeling to preserve membrane physical properties upon exogenous polyunsaturated fatty acids exposure.

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          Most cited references57

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          Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?

          J R Hazel (1995)
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            Membrane fluidity and its roles in the perception of environmental signals.

            Poikilothermic organisms are exposed to frequent changes in environmental conditions and their survival depends on their ability to acclimate to such changes. Changes in ambient temperature and osmolarity cause fluctuations in the fluidity of cell membranes. Such fluctuations are considered to be critical to the initiation of the regulatory reactions that ultimately lead to acclimation. The mechanisms responsible for the perception of changes in membrane fluidity have not been fully characterized. However, the analysis of genome-wide gene expression using DNA microarrays has provided a powerful new approach to studies of the contribution of membrane fluidity to gene expression and to the identification of environmental sensors. In this review, we focus on the mechanisms that regulate membrane fluidity, on putative sensors that perceive changes in membrane fluidity, and on the subsequent expression of genes that ensures acclimation to a new set of environmental conditions.
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              Elucidating membrane structure and protein behavior using giant plasma membrane vesicles.

              The observation of phase separation in intact plasma membranes isolated from live cells is a breakthrough for research into eukaryotic membrane lateral heterogeneity, specifically in the context of membrane rafts. These observations are made in giant plasma membrane vesicles (GPMVs), which can be isolated by chemical vesiculants from a variety of cell types and microscopically observed using basic reagents and equipment available in any cell biology laboratory. Microscopic phase separation is detectable by fluorescent labeling, followed by cooling of the membranes below their miscibility phase transition temperature. This protocol describes the methods to prepare and isolate the vesicles, equipment to observe them under temperature-controlled conditions and three examples of fluorescence analysis: (i) fluorescence spectroscopy with an environment-sensitive dye (laurdan); (ii) two-photon microscopy of the same dye; and (iii) quantitative confocal microscopy to determine component partitioning between raft and nonraft phases. GPMV preparation and isolation, including fluorescent labeling and observation, can be accomplished within 4 h.
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                Author and article information

                Contributors
                kandice.r.levental@uth.tmc.edu
                ilya.levental@uth.tmc.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                12 March 2020
                12 March 2020
                2020
                : 11
                : 1339
                Affiliations
                [1 ]ISNI 0000 0000 9206 2401, GRID grid.267308.8, Department of Integrative Biology & Pharmacology, University of Texas Health Science Center at Houston, ; Houston, TX USA
                [2 ]ISNI 0000 0004 4687 2082, GRID grid.264756.4, Program in Integrative Nutrition & Complex Diseases and Department of Nutrition, , Texas A&M University, ; College Station, TX USA
                [3 ]ISNI 0000 0001 2167 7588, GRID grid.11749.3a, Department of Medical Biochemistry & Molecular Biology, Medical Faculty, , Saarland University, ; Homburg, Germany
                Author information
                http://orcid.org/0000-0002-2234-3683
                http://orcid.org/0000-0002-0283-3490
                http://orcid.org/0000-0002-1206-9545
                Article
                15203
                10.1038/s41467-020-15203-1
                7067841
                32165635
                47bbcf09-c556-4fd8-8bbf-fc435e74474a
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 1 June 2018
                : 21 February 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000057, U.S. Department of Health & Human Services | NIH | National Institute of General Medical Sciences (NIGMS);
                Award ID: GM114282, GM124072, GM120351
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001663, Volkswagen Foundation (VolkswagenStiftung);
                Award ID: 93091
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100000854, Human Frontier Science Program (HFSP);
                Award ID: RGP0059/2019
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2020

                Uncategorized
                biophysical chemistry,lipidomics,lipids,membrane biophysics,cell biology
                Uncategorized
                biophysical chemistry, lipidomics, lipids, membrane biophysics, cell biology

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