Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage

Phospholipid membranes form cellular barriers but need to be flexible enough to divide by fission. Phospholipids generally contain a saturated fatty acid (FA) at position sn1 whereas the sn2-FA is saturated, monounsaturated or polyunsaturated. Our understanding of the impact of phospholipid unsatura...

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Main Authors: Marco M Manni, Marion L Tiberti, Sophie Pagnotta, Hélène Barelli, Romain Gautier, Bruno Antonny
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/34394
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author Marco M Manni
Marion L Tiberti
Sophie Pagnotta
Hélène Barelli
Romain Gautier
Bruno Antonny
author_facet Marco M Manni
Marion L Tiberti
Sophie Pagnotta
Hélène Barelli
Romain Gautier
Bruno Antonny
author_sort Marco M Manni
collection DOAJ
description Phospholipid membranes form cellular barriers but need to be flexible enough to divide by fission. Phospholipids generally contain a saturated fatty acid (FA) at position sn1 whereas the sn2-FA is saturated, monounsaturated or polyunsaturated. Our understanding of the impact of phospholipid unsaturation on membrane flexibility and fission is fragmentary. Here, we provide a comprehensive view of the effects of the FA profile of phospholipids on membrane vesiculation by dynamin and endophilin. Coupled to simulations, this analysis indicates that: (i) phospholipids with two polyunsaturated FAs make membranes prone to vesiculation but highly permeable; (ii) asymmetric sn1-saturated-sn2-polyunsaturated phospholipids provide a tradeoff between efficient membrane vesiculation and low membrane permeability; (iii) When incorporated into phospholipids, docosahexaenoic acid (DHA; omega-3) makes membranes more deformable than arachidonic acid (omega-6). These results suggest an explanation for the abundance of sn1-saturated-sn2-DHA phospholipids in synaptic membranes and for the importance of the omega-6/omega-3 ratio on neuronal functions.
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spelling doaj.art-e613b9af60064d0b9cb5e79e77a18c062022-12-22T02:03:16ZengeLife Sciences Publications LtdeLife2050-084X2018-03-01710.7554/eLife.34394Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakageMarco M Manni0Marion L Tiberti1Sophie Pagnotta2Hélène Barelli3Romain Gautier4Bruno Antonny5https://orcid.org/0000-0002-9166-8668Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur et CNRS, Valbonne, France; Instituto Biofisika (UPV/EHU, CSIC), Leioa, SpainInstitut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur et CNRS, Valbonne, FranceCentre Commun de Microscopie Appliquée, Université Côte d’Azur, Nice, FranceInstitut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur et CNRS, Valbonne, FranceInstitut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur et CNRS, Valbonne, FranceInstitut de Pharmacologie Moléculaire et Cellulaire, Université Côte d’Azur et CNRS, Valbonne, FrancePhospholipid membranes form cellular barriers but need to be flexible enough to divide by fission. Phospholipids generally contain a saturated fatty acid (FA) at position sn1 whereas the sn2-FA is saturated, monounsaturated or polyunsaturated. Our understanding of the impact of phospholipid unsaturation on membrane flexibility and fission is fragmentary. Here, we provide a comprehensive view of the effects of the FA profile of phospholipids on membrane vesiculation by dynamin and endophilin. Coupled to simulations, this analysis indicates that: (i) phospholipids with two polyunsaturated FAs make membranes prone to vesiculation but highly permeable; (ii) asymmetric sn1-saturated-sn2-polyunsaturated phospholipids provide a tradeoff between efficient membrane vesiculation and low membrane permeability; (iii) When incorporated into phospholipids, docosahexaenoic acid (DHA; omega-3) makes membranes more deformable than arachidonic acid (omega-6). These results suggest an explanation for the abundance of sn1-saturated-sn2-DHA phospholipids in synaptic membranes and for the importance of the omega-6/omega-3 ratio on neuronal functions.https://elifesciences.org/articles/34394polyunsaturated phospholipidDynaminmembrane curvaturemembrane fissionmembrane permeabilityomega-3 omega-6 PUFAs
spellingShingle Marco M Manni
Marion L Tiberti
Sophie Pagnotta
Hélène Barelli
Romain Gautier
Bruno Antonny
Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
eLife
polyunsaturated phospholipid
Dynamin
membrane curvature
membrane fission
membrane permeability
omega-3 omega-6 PUFAs
title Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title_full Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title_fullStr Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title_full_unstemmed Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title_short Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title_sort acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
topic polyunsaturated phospholipid
Dynamin
membrane curvature
membrane fission
membrane permeability
omega-3 omega-6 PUFAs
url https://elifesciences.org/articles/34394
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