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

Abstract

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.

Article and author information

Author details

  1. Marco M Manni

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Marion L Tiberti

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Sophie Pagnotta

    Centre Commun de Microscopie Appliquée, Université Côte d'Azur, Nice, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Hélène Barelli

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Romain Gautier

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Bruno Antonny

    CNRS, Institut de Pharmacologie Moléculaire et Cellulaire, Université Côte d'Azur, Valbonne, France
    For correspondence
    antonny@ipmc.cnrs.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9166-8668

Funding

Agence Nationale de la Recherche (ANR-11-LABX-0028-01)

  • Bruno Antonny

European Commission (ERC advanced grant 268888)

  • Bruno Antonny

Eusko Jaurlaritza (Post-doctoral fellowship)

  • Marco M Manni

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Patricia Bassereau, Institut Curie, France

Publication history

  1. Received: December 15, 2017
  2. Accepted: March 14, 2018
  3. Accepted Manuscript published: March 15, 2018 (version 1)
  4. Version of Record published: April 17, 2018 (version 2)
  5. Version of Record updated: April 24, 2018 (version 3)

Copyright

© 2018, Manni et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Marco M Manni
  2. Marion L Tiberti
  3. Sophie Pagnotta
  4. Hélène Barelli
  5. Romain Gautier
  6. Bruno Antonny
(2018)
Acyl chain asymmetry and polyunsaturation of brain phospholipids facilitate membrane vesiculation without leakage
eLife 7:e34394.
https://doi.org/10.7554/eLife.34394

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