1. Cell Biology
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Control of endothelial cell polarity and sprouting angiogenesis by non-centrosomal microtubules

  1. Maud Martin
  2. Alexandra Veloso
  3. Jingchao Wu
  4. Eugene A Katrukha
  5. Anna Akhmanova  Is a corresponding author
  1. Utrecht University, Netherlands
  2. University of Liège, Belgium
Research Article
  • Cited 25
  • Views 5,315
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Cite this article as: eLife 2018;7:e33864 doi: 10.7554/eLife.33864

Abstract

Microtubules control different aspects of cell polarization. In cells with a radial microtubule system, a pivotal role in setting up asymmetry is attributed to the relative positioning of the centrosome and the nucleus. Here, we show that centrosome loss had no effect on the ability of endothelial cells to polarize and move in 2D and 3D environments. In contrast, non-centrosomal microtubules stabilized by the microtubule minus-end-binding protein CAMSAP2 were required for directional migration on 2D substrates and for the establishment of polarized cell morphology in soft 3D matrices. CAMSAP2 was also important for persistent endothelial cell sprouting during in vivo zebrafish vessel development. In the absence of CAMSAP2, cell polarization in 3D could be partly rescued by centrosome depletion, indicating that in these conditions the centrosome inhibited cell polarity. We propose that CAMSAP2-protected non-centrosomal microtubules are needed for establishing cell asymmetry by enabling microtubule enrichment in a single cell protrusion.

Article and author information

Author details

  1. Maud Martin

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  2. Alexandra Veloso

    Interdisciplinary Cluster for Applied Genoproteomics (GIGA-R), University of Liège, Liège, Belgium
    Competing interests
    No competing interests declared.
  3. Jingchao Wu

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  4. Eugene A Katrukha

    Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    No competing interests declared.
  5. Anna Akhmanova

    Department of Biology, Utrecht University, Utrecht, Netherlands
    For correspondence
    a.akhmanova@uu.nl
    Competing interests
    Anna Akhmanova, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9048-8614

Funding

European Research Council (Synergy 609822)

  • Anna Akhmanova

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (ALW Open Program grant 824.15.017)

  • Anna Akhmanova

Marie Sklodowska-Curie Actions (IEF fellowship)

  • Maud Martin

China Scholarship Council (PhD fellowship)

  • Jingchao Wu

Fonds De La Recherche Scientifique - FNRS (FRIA fellowship)

  • Alexandra Veloso

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

Ethics

Animal experimentation: All animal experiments were approved by the animal welfare committee of the University of Liege (protocol number 14-1556, laboratory agreement number LA 1610002).

Reviewing Editor

  1. Pekka Lappalainen, University of Helsinki, Finland

Publication history

  1. Received: November 26, 2017
  2. Accepted: March 13, 2018
  3. Accepted Manuscript published: March 16, 2018 (version 1)
  4. Version of Record published: April 13, 2018 (version 2)

Copyright

© 2018, Martin 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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