Dynein-mediated transport and membrane trafficking control PAR3 polarised distribution

  1. Julie Jouette
  2. Antoine Guichet  Is a corresponding author
  3. Sandra B Claret  Is a corresponding author
  1. Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, France

Abstract

The scaffold protein PAR3 and the kinase PAR1 are essential proteins that control cell polarity. Their precise opposite localisations define plasma membrane domains with specific functions. PAR3 and PAR1 are mutually inhibited by direct or indirect phosphorylations, but their fates once phosphorylated are poorly known. Through precise spatiotemporal quantification of PAR3 localisation in the Drosophila oocyte, we identify several mechanisms responsible for its anterior cortex accumulation and its posterior exclusion. We show that PAR3 posterior plasma membrane exclusion depends on PAR1 and an endocytic mechanisms relying on RAB5 and PI(4,5)P2. In a second phase, microtubules and the dynein motor, in connection with vesicular trafficking involving RAB11 and IKK-related kinase, IKKε, are required for PAR3 transport towards the anterior cortex. Altogether our results point to a connection between membrane trafficking and dynein-mediated transport to sustain PAR3 asymmetry.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Julie Jouette

    Polarity and Morphogenesis Lab, Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Antoine Guichet

    Polarity and Morphogenesis Lab, Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, Paris, France
    For correspondence
    antoine.guichet@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
  3. Sandra B Claret

    Polarity and Morphogenesis Lab, Institut Jacques Monod, CNRS, UMR 7592, Paris Diderot University, Paris, France
    For correspondence
    sandra.claret@ijm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7167-510X

Funding

Fondation ARC pour la Recherche sur le Cancer (SLR20130607102)

  • Antoine Guichet

Ligue Contre le Cancer (RS14/75-58)

  • Antoine Guichet

Fondation ARC pour la Recherche sur le Cancer (PJA 20141201756)

  • Antoine Guichet

Fondation ARC pour la Recherche sur le Cancer (PJA 20161204931)

  • Antoine Guichet

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

Reviewing Editor

  1. Matthew Freeman, University of Oxford, United Kingdom

Version history

  1. Received: July 19, 2018
  2. Accepted: January 3, 2019
  3. Accepted Manuscript published: January 23, 2019 (version 1)
  4. Version of Record published: February 1, 2019 (version 2)
  5. Version of Record updated: February 1, 2019 (version 3)

Copyright

© 2019, Jouette 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

  • 2,235
    Page views
  • 394
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Julie Jouette
  2. Antoine Guichet
  3. Sandra B Claret
(2019)
Dynein-mediated transport and membrane trafficking control PAR3 polarised distribution
eLife 8:e40212.
https://doi.org/10.7554/eLife.40212

Share this article

https://doi.org/10.7554/eLife.40212

Further reading

    1. Cell Biology
    Kazuki Hanaoka, Kensuke Nishikawa ... Kouichi Funato
    Research Article

    Membrane contact sites (MCSs) are junctures that perform important roles including coordinating lipid metabolism. Previous studies have indicated that vacuolar fission/fusion processes are coupled with modifications in the membrane lipid composition. However, it has been still unclear whether MCS-mediated lipid metabolism controls the vacuolar morphology. Here, we report that deletion of tricalbins (Tcb1, Tcb2, and Tcb3), tethering proteins at endoplasmic reticulum (ER)–plasma membrane (PM) and ER–Golgi contact sites, alters fusion/fission dynamics and causes vacuolar fragmentation in the yeast Saccharomyces cerevisiae. In addition, we show that the sphingolipid precursor phytosphingosine (PHS) accumulates in tricalbin-deleted cells, triggering the vacuolar division. Detachment of the nucleus–vacuole junction (NVJ), an important contact site between the vacuole and the perinuclear ER, restored vacuolar morphology in both cells subjected to high exogenous PHS and Tcb3-deleted cells, supporting that PHS transport across the NVJ induces vacuole division. Thus, our results suggest that vacuolar morphology is maintained by MCSs through the metabolism of sphingolipids.

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Monica Salinas-Pena, Elena Rebollo, Albert Jordan
    Research Article

    Histone H1 participates in chromatin condensation and regulates nuclear processes. Human somatic cells may contain up to seven histone H1 variants, although their functional heterogeneity is not fully understood. Here, we have profiled the differential nuclear distribution of the somatic H1 repertoire in human cells through imaging techniques including super-resolution microscopy. H1 variants exhibit characteristic distribution patterns in both interphase and mitosis. H1.2, H1.3, and H1.5 are universally enriched at the nuclear periphery in all cell lines analyzed and co-localize with compacted DNA. H1.0 shows a less pronounced peripheral localization, with apparent variability among different cell lines. On the other hand, H1.4 and H1X are distributed throughout the nucleus, being H1X universally enriched in high-GC regions and abundant in the nucleoli. Interestingly, H1.4 and H1.0 show a more peripheral distribution in cell lines lacking H1.3 and H1.5. The differential distribution patterns of H1 suggest specific functionalities in organizing lamina-associated domains or nucleolar activity, which is further supported by a distinct response of H1X or phosphorylated H1.4 to the inhibition of ribosomal DNA transcription. Moreover, H1 variants depletion affects chromatin structure in a variant-specific manner. Concretely, H1.2 knock-down, either alone or combined, triggers a global chromatin decompaction. Overall, imaging has allowed us to distinguish H1 variants distribution beyond the segregation in two groups denoted by previous ChIP-Seq determinations. Our results support H1 variants heterogeneity and suggest that variant-specific functionality can be shared between different cell types.