Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae

  1. Galina V Beznoussenko
  2. Seetharaman Parashuraman
  3. Riccardo Rizzo
  4. Roman Polishchuk
  5. Oliviano Martella
  6. Daniele Di Giandomenico
  7. Aurora Fusella
  8. Alexander Spaar
  9. Michele Sallese
  10. Maria Grazia Capestrano
  11. Margit Pavelka
  12. Matthijn R Vos
  13. Yuri GM Rikers
  14. Volkhard Helms
  15. Alexandre A Mironov
  16. Alberto Luini  Is a corresponding author
  1. Fondazione IFOM, Italy
  2. Consiglio Nazionale Delle Ricerche (CNR-IBP), Italy
  3. Telethon Institute for Genetics and Medicine (TIGEM), Italy
  4. Consorzio Mario Negri Sud, Italy
  5. Center for Anatomy and Cell Biology, Medical University of Vienna, Austria
  6. FEI Company, Netherlands
  7. Saarland University, Germany

Abstract

The mechanism of transport through the Golgi complex is not completely understood, insofar as no single transport mechanism appears to account for all of the observations. Here, we compare the transport of soluble secretory proteins (albumin and α1-antitrypsin) with that of supramolecular cargoes (e.g., procollagen) that are proposed to traverse the Golgi by compartment progression-maturation. We show that these soluble proteins traverse the Golgi much faster than procollagen while moving through the same stack. Moreover, we present kinetic and morphological observations that indicate that albumin transport occurs by diffusion via intercisternal continuities. These data provide evidence that this transport mechanism that applies to a major class of secretory proteins and indicate the co-existence of multiple intra-Golgi trafficking modes.

Article and author information

Author details

  1. Galina V Beznoussenko

    Fondazione IFOM, Milan, Italy
    Competing interests
    The authors declare that no competing interests exist.
  2. Seetharaman Parashuraman

    Consiglio Nazionale Delle Ricerche (CNR-IBP), Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
  3. Riccardo Rizzo

    Consiglio Nazionale Delle Ricerche (CNR-IBP), Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Roman Polishchuk

    Telethon Institute for Genetics and Medicine (TIGEM), Naples, Italy
    Competing interests
    The authors declare that no competing interests exist.
  5. Oliviano Martella

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniele Di Giandomenico

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  7. Aurora Fusella

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  8. Alexander Spaar

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  9. Michele Sallese

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  10. Maria Grazia Capestrano

    Consorzio Mario Negri Sud, Santa Maria Imbaro, Italy
    Competing interests
    The authors declare that no competing interests exist.
  11. Margit Pavelka

    Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  12. Matthijn R Vos

    FEI Company, Eindhoven, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Yuri GM Rikers

    FEI Company, Eindhoven, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  14. Volkhard Helms

    Saarland University, Saarbruecken, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Alexandre A Mironov

    Fondazione IFOM, Milan, Italy
    Competing interests
    The authors declare that no competing interests exist.
  16. Alberto Luini

    Consiglio Nazionale Delle Ricerche (CNR-IBP), Naples, Italy
    For correspondence
    luini@tigem.it
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Suzanne R Pfeffer, Stanford University, United States

Version history

  1. Received: December 4, 2013
  2. Accepted: May 25, 2014
  3. Accepted Manuscript published: May 27, 2014 (version 1)
  4. Version of Record published: June 25, 2014 (version 2)

Copyright

© 2014, Beznoussenko 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.

Metrics

  • 5,843
    views
  • 540
    downloads
  • 69
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Galina V Beznoussenko
  2. Seetharaman Parashuraman
  3. Riccardo Rizzo
  4. Roman Polishchuk
  5. Oliviano Martella
  6. Daniele Di Giandomenico
  7. Aurora Fusella
  8. Alexander Spaar
  9. Michele Sallese
  10. Maria Grazia Capestrano
  11. Margit Pavelka
  12. Matthijn R Vos
  13. Yuri GM Rikers
  14. Volkhard Helms
  15. Alexandre A Mironov
  16. Alberto Luini
(2014)
Transport of soluble proteins through the Golgi occurs by diffusion via continuities across cisternae
eLife 3:e02009.
https://doi.org/10.7554/eLife.02009

Share this article

https://doi.org/10.7554/eLife.02009

Further reading

    1. Cancer Biology
    2. Cell Biology
    Ian Lorimer
    Insight

    Establishing a zebrafish model of a deadly type of brain tumor highlights the role of the immune system in the early stages of the disease.

    1. Cell Biology
    2. Neuroscience
    Jaebin Kim, Edwin Bustamante ... Scott H Soderling
    Research Article

    One of the most extensively studied members of the Ras superfamily of small GTPases, Rac1 is an intracellular signal transducer that remodels actin and phosphorylation signaling networks. Previous studies have shown that Rac1-mediated signaling is associated with hippocampal-dependent working memory and longer-term forms of learning and memory and that Rac1 can modulate forms of both pre- and postsynaptic plasticity. How these different cognitive functions and forms of plasticity mediated by Rac1 are linked, however, is unclear. Here, we show that spatial working memory in mice is selectively impaired following the expression of a genetically encoded Rac1 inhibitor at presynaptic terminals, while longer-term cognitive processes are affected by Rac1 inhibition at postsynaptic sites. To investigate the regulatory mechanisms of this presynaptic process, we leveraged new advances in mass spectrometry to identify the proteomic and post-translational landscape of presynaptic Rac1 signaling. We identified serine/threonine kinases and phosphorylated cytoskeletal signaling and synaptic vesicle proteins enriched with active Rac1. The phosphorylated sites in these proteins are at positions likely to have regulatory effects on synaptic vesicles. Consistent with this, we also report changes in the distribution and morphology of synaptic vesicles and in postsynaptic ultrastructure following presynaptic Rac1 inhibition. Overall, this study reveals a previously unrecognized presynaptic role of Rac1 signaling in cognitive processes and provides insights into its potential regulatory mechanisms.