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...
| Autores: | , , , , , |
|---|---|
| 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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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 Sí |
| dc.rights.none.fl_str_mv |
info:eu-repo/semantics/openAccess |
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openAccess |
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application/pdf |
| dc.publisher.none.fl_str_mv |
eLife Sciences Publications |
| publisher.none.fl_str_mv |
eLife Sciences Publications |
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reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC instname:Consejo Superior de Investigaciones Científicas (CSIC) |
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Consejo Superior de Investigaciones Científicas (CSIC) |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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DIGITAL.CSIC. Repositorio Institucional del CSIC |
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15,811543 |