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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Autores: Manni, Marco M., Tiberti, Marion L., Pagnotta, Sophie, Barelli, Hélène, Gautier, Romain, Antonny, Bruno
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2018
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/403747
Acceso en línea:http://hdl.handle.net/10261/403747
https://api.elsevier.com/content/abstract/scopus_id/85045657403
Access Level:acceso abierto
Palabra clave:Dynamin
Bar domain
Biochemistry
Chemical biology
Membrane curvature
Membrane deformation
Membrane fission
Membrane permeability
Molecular biophysics
Omega-3
Omega-3 omega-6 PUFAs
Omega-6
Polyunsaturated phospholipid
Structural biology
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spelling Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakageManni, Marco M.Tiberti, Marion L.Pagnotta, SophieBarelli, HélèneGautier, RomainAntonny, BrunoDynaminBar domainBiochemistryChemical biologyDynaminMembrane curvatureMembrane deformationMembrane fissionMembrane permeabilityMolecular biophysicsOmega-3Omega-3 omega-6 PUFAsOmega-6Polyunsaturated phospholipidStructural biologyPhospholipid 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.This work was supported in part by an ERC grant (268 888) and is currently supported by the Agence Nationale de la Recherche (ANR-11-LABX-0028–01) and the HPC resources of CINES under the allocations 2016-c2016077362 and 2017-A0020707362 made by GENCI. MM is supported by a postdoctoral fellowship from the Basque Government.Peer reviewedeLife Sciences PublicationsEuropean CommissionAgence Nationale de la Recherche (France)Eusko JaurlaritzaAntonny, Bruno [0000-0002-9166-8668]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252018info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/403747https://api.elsevier.com/content/abstract/scopus_id/85045657403reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/EC/H2020/268888The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.7554/eLife.34394https://doi.org/10.7554/eLife.34394Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4037472026-05-22T06:33:51Z
dc.title.none.fl_str_mv Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
title Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
spellingShingle Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
Manni, Marco M.
Dynamin
Bar domain
Biochemistry
Chemical biology
Dynamin
Membrane curvature
Membrane deformation
Membrane fission
Membrane permeability
Molecular biophysics
Omega-3
Omega-3 omega-6 PUFAs
Omega-6
Polyunsaturated phospholipid
Structural biology
title_short 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_sort Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
dc.creator.none.fl_str_mv Manni, Marco M.
Tiberti, Marion L.
Pagnotta, Sophie
Barelli, Hélène
Gautier, Romain
Antonny, Bruno
author Manni, Marco M.
author_facet Manni, Marco M.
Tiberti, Marion L.
Pagnotta, Sophie
Barelli, Hélène
Gautier, Romain
Antonny, Bruno
author_role author
author2 Tiberti, Marion L.
Pagnotta, Sophie
Barelli, Hélène
Gautier, Romain
Antonny, Bruno
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv European Commission
Agence Nationale de la Recherche (France)
Eusko Jaurlaritza
Antonny, Bruno [0000-0002-9166-8668]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Dynamin
Bar domain
Biochemistry
Chemical biology
Dynamin
Membrane curvature
Membrane deformation
Membrane fission
Membrane permeability
Molecular biophysics
Omega-3
Omega-3 omega-6 PUFAs
Omega-6
Polyunsaturated phospholipid
Structural biology
topic Dynamin
Bar domain
Biochemistry
Chemical biology
Dynamin
Membrane curvature
Membrane deformation
Membrane fission
Membrane permeability
Molecular biophysics
Omega-3
Omega-3 omega-6 PUFAs
Omega-6
Polyunsaturated phospholipid
Structural biology
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.
publishDate 2018
dc.date.none.fl_str_mv 2018
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/403747
https://api.elsevier.com/content/abstract/scopus_id/85045657403
url http://hdl.handle.net/10261/403747
https://api.elsevier.com/content/abstract/scopus_id/85045657403
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/EC/H2020/268888
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI https://doi.org/10.7554/eLife.34394
https://doi.org/10.7554/eLife.34394

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications
publisher.none.fl_str_mv eLife Sciences Publications
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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