Sphingomyelin metabolism controls the shape and function of the Golgi cisternae

  1. Felix Campelo  Is a corresponding author
  2. Josse van Galen
  3. Gabriele Turacchio
  4. Seetharaman Parashuraman
  5. Michael M Kozlov
  6. María García-Parajo
  7. Vivek Malhotra  Is a corresponding author
  1. The Barcelona Institute of Science and Technology, Spain
  2. National Research Council of Italy, Italy
  3. Tel Aviv University, Israel

Abstract

The flat Golgi cisterna is a highly conserved feature of eukaryotic cells, but how is this morphology achieved and is it related to its function in cargo sorting and export? A physical model of cisterna morphology led us to propose that sphingomyelin (SM) metabolism at the trans-Golgi membranes in mammalian cells essentially controls the structural features of a Golgi cisterna by regulating its association to curvature-generating proteins. An experimental test of this hypothesis revealed that affecting SM homeostasis converted flat cisternae into highly curled membranes with a concomitant dissociation of membrane curvature-generating proteins. These data lend support to our hypothesis that SM metabolism controls the structural organization of a Golgi cisterna. Together with our previously presented role of SM in controlling the location of proteins involved in glycosylation and vesicle formation, our data reveal the significance of SM metabolism in the structural organization and function of Golgi cisternae.

Article and author information

Author details

  1. Felix Campelo

    ICFO - The Institute of Photonic Sciences, The Barcelona Institute of Science and Technology, Barcelona, Spain
    For correspondence
    felix.campelo@icfo.eu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0786-9548
  2. Josse van Galen

    Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    No competing interests declared.
  3. Gabriele Turacchio

    Institute of Protein Biochemistry, National Research Council of Italy, Naples, Italy
    Competing interests
    No competing interests declared.
  4. Seetharaman Parashuraman

    Institute of Protein Biochemistry, National Research Council of Italy, Naples, Italy
    Competing interests
    No competing interests declared.
  5. Michael M Kozlov

    Department of Physiology and Pharmacology, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    Michael M Kozlov, Reviewing editor, eLife.
  6. María García-Parajo

    ICFO - The Institute of Photonic Sciences, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    No competing interests declared.
  7. Vivek Malhotra

    Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    For correspondence
    vivek.malhotra@crg.eu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6198-7943

Funding

Ministerio de Economía y Competitividad (Severo Ochoa Programme SEV-2015-240522)

  • Felix Campelo
  • María García-Parajo

H2020 European Research Council (Advanced Grant 268692)

  • Vivek Malhotra

Ministerio de Economía y Competitividad (Severo Ochoa Programme SEV-2012-0208)

  • Vivek Malhotra

Ministerio de Economía y Competitividad (BFU2015-73288-JIN AEI/FED)

  • Felix Campelo
  • María García-Parajo

Fundación Cellex

  • Felix Campelo
  • María García-Parajo

Human Frontier Science Program (GA RGP0027/2012)

  • María García-Parajo

European Commission (FP7-NANO-VISTA GA 288263)

  • María García-Parajo

Institució Catalana de Recerca i Estudis Avançats

  • María García-Parajo
  • Vivek Malhotra

Israel Science Foundation (758/11)

  • Michael M Kozlov

Ministerio de Economía y Competitividad (Plan Nacional FIS2014-56107-R)

  • María García-Parajo

Ministerio de Economía y Competitividad (Plan Nacional BFU2013-44188-P)

  • Vivek Malhotra

Ministerio de Economía y Competitividad (Consolider CSD2009-00016)

  • Vivek Malhotra

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 23, 2016
  2. Accepted: May 4, 2017
  3. Accepted Manuscript published: May 13, 2017 (version 1)
  4. Version of Record published: June 7, 2017 (version 2)

Copyright

© 2017, Campelo 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. Felix Campelo
  2. Josse van Galen
  3. Gabriele Turacchio
  4. Seetharaman Parashuraman
  5. Michael M Kozlov
  6. María García-Parajo
  7. Vivek Malhotra
(2017)
Sphingomyelin metabolism controls the shape and function of the Golgi cisternae
eLife 6:e24603.
https://doi.org/10.7554/eLife.24603

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