Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences

Here, biophysical properties of membranes enriched in three metabolically related sterols are analyzed both in vitro and in vivo. Unlike cholesterol and ergosterol, the common metabolic precursor zymosterol is unable to induce the formation of a liquid ordered (lo) phase in model lipid membranes and...

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Main Authors: Alena Khmelinskaia, Joaquim M. T. Marquês, André E. P. Bastos, Catarina A. C. Antunes, Andreia Bento-Oliveira, Silvia Scolari, Gerson M. da S. Lobo, Rui Malhó, Andreas Herrmann, H. Susana Marinho, Rodrigo F. M. de Almeida
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/article/10.3389/fcell.2020.00337/full
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author Alena Khmelinskaia
Joaquim M. T. Marquês
André E. P. Bastos
Catarina A. C. Antunes
Andreia Bento-Oliveira
Silvia Scolari
Gerson M. da S. Lobo
Rui Malhó
Andreas Herrmann
H. Susana Marinho
Rodrigo F. M. de Almeida
author_facet Alena Khmelinskaia
Joaquim M. T. Marquês
André E. P. Bastos
Catarina A. C. Antunes
Andreia Bento-Oliveira
Silvia Scolari
Gerson M. da S. Lobo
Rui Malhó
Andreas Herrmann
H. Susana Marinho
Rodrigo F. M. de Almeida
author_sort Alena Khmelinskaia
collection DOAJ
description Here, biophysical properties of membranes enriched in three metabolically related sterols are analyzed both in vitro and in vivo. Unlike cholesterol and ergosterol, the common metabolic precursor zymosterol is unable to induce the formation of a liquid ordered (lo) phase in model lipid membranes and can easily accommodate in a gel phase. As a result, Zym has a marginal ability to modulate the passive membrane permeability of lipid vesicles with different compositions, contrary to cholesterol and ergosterol. Using fluorescence-lifetime imaging microscopy of an aminostyryl dye in living mammalian and yeast cells we established a close parallel between sterol-dependent membrane biophysical properties in vivo and in vitro. This approach unraveled fundamental differences in yeast and mammalian plasma membrane organization. It is often suggested that, in eukaryotes, areas that are sterol-enriched are also rich in sphingolipids, constituting highly ordered membrane regions. Our results support that while cholesterol is able to interact with saturated lipids, ergosterol seems to interact preferentially with monounsaturated phosphatidylcholines. Taken together, we show that different eukaryotic kingdoms developed unique solutions for the formation of a sterol-rich plasma membrane, a common evolutionary trait that accounts for sterol structural diversity.
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spelling doaj.art-95aeb875e7f246adb6ef6ca11a2788fa2022-12-22T00:08:40ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-06-01810.3389/fcell.2020.00337531452Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational DifferencesAlena Khmelinskaia0Joaquim M. T. Marquês1André E. P. Bastos2Catarina A. C. Antunes3Andreia Bento-Oliveira4Silvia Scolari5Gerson M. da S. Lobo6Rui Malhó7Andreas Herrmann8H. Susana Marinho9Rodrigo F. M. de Almeida10Centro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalDepartment of Biology, Molecular Biophysics, Humboldt-Universität zu Berlin, Berlin, GermanyCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalFaculdade de Ciências, BioISI, Universidade de Lisboa, Lisbon, PortugalDepartment of Biology, Molecular Biophysics, Humboldt-Universität zu Berlin, Berlin, GermanyCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalCentro de Química Estrutural, Faculdade de Ciências, Universidade de Lisboa, Lisbon, PortugalHere, biophysical properties of membranes enriched in three metabolically related sterols are analyzed both in vitro and in vivo. Unlike cholesterol and ergosterol, the common metabolic precursor zymosterol is unable to induce the formation of a liquid ordered (lo) phase in model lipid membranes and can easily accommodate in a gel phase. As a result, Zym has a marginal ability to modulate the passive membrane permeability of lipid vesicles with different compositions, contrary to cholesterol and ergosterol. Using fluorescence-lifetime imaging microscopy of an aminostyryl dye in living mammalian and yeast cells we established a close parallel between sterol-dependent membrane biophysical properties in vivo and in vitro. This approach unraveled fundamental differences in yeast and mammalian plasma membrane organization. It is often suggested that, in eukaryotes, areas that are sterol-enriched are also rich in sphingolipids, constituting highly ordered membrane regions. Our results support that while cholesterol is able to interact with saturated lipids, ergosterol seems to interact preferentially with monounsaturated phosphatidylcholines. Taken together, we show that different eukaryotic kingdoms developed unique solutions for the formation of a sterol-rich plasma membrane, a common evolutionary trait that accounts for sterol structural diversity.https://www.frontiersin.org/article/10.3389/fcell.2020.00337/fullergosterolcholesterolzymosterolfluorescence lifetime imaging microscopyfluorescence spectroscopyplasma membrane
spellingShingle Alena Khmelinskaia
Joaquim M. T. Marquês
André E. P. Bastos
Catarina A. C. Antunes
Andreia Bento-Oliveira
Silvia Scolari
Gerson M. da S. Lobo
Rui Malhó
Andreas Herrmann
H. Susana Marinho
Rodrigo F. M. de Almeida
Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
Frontiers in Cell and Developmental Biology
ergosterol
cholesterol
zymosterol
fluorescence lifetime imaging microscopy
fluorescence spectroscopy
plasma membrane
title Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
title_full Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
title_fullStr Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
title_full_unstemmed Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
title_short Liquid-Ordered Phase Formation by Mammalian and Yeast Sterols: A Common Feature With Organizational Differences
title_sort liquid ordered phase formation by mammalian and yeast sterols a common feature with organizational differences
topic ergosterol
cholesterol
zymosterol
fluorescence lifetime imaging microscopy
fluorescence spectroscopy
plasma membrane
url https://www.frontiersin.org/article/10.3389/fcell.2020.00337/full
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