1. Cell Biology
  2. Developmental Biology
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Radially-patterned cell behaviours during tube budding from an epithelium

  1. Yara E Sanchez-Corrales
  2. Guy B Blanchard  Is a corresponding author
  3. Katja Röper  Is a corresponding author
  1. University of Cambridge, United Kingdom
Research Article
  • Cited 19
  • Views 3,167
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Cite this article as: eLife 2018;7:e35717 doi: 10.7554/eLife.35717
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Abstract

The budding of tubular organs from flat epithelial sheets is a vital morphogenetic process. Cell behaviours that drive such processes are only starting to be unraveled. Using live-imaging and novel morphometric methods we show that in addition to apical constriction, radially-oriented directional intercalation of cells plays a major contribution to early stages of invagination of the salivary gland tube in the Drosophila embryo. Extending analyses in 3D, we find that near the pit of invagination, isotropic apical constriction leads to strong cell-wedging. Further from the pit cells interleave circumferentially, suggesting apically-driven behaviours. Supporting this, junctional myosin is enriched in, and neighbour exchanges are biased towards the circumferential orientation. In a mutant failing pit specification, neither are biased due to an inactive pit. Thus, tube budding involves radially-patterned pools of apical myosin, medial as well as junctional, and radially-patterned 3D-cell behaviours, with a close mechanical interplay between invagination and intercalation.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all figures.

Article and author information

Author details

  1. Yara E Sanchez-Corrales

    MRC-Laboratory of Molecular Biology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1438-1994
  2. Guy B Blanchard

    Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    gb288@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  3. Katja Röper

    MRC -Laboratory of Molecular Biology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    kroeper@mrc-lmb.cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3361-766X

Funding

Medical Research Council (U105178780)

  • Yara E Sanchez-Corrales
  • Guy B Blanchard
  • Katja Röper

Biotechnology and Biological Sciences Research Council (BB/J010278/1)

  • Guy B Blanchard

Wellcome (100329/Z/12/Z)

  • Guy B Blanchard

Isaac Newton Trust (15.23(k))

  • Guy B Blanchard

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

Reviewing Editor

  1. Stefan Luschnig

Publication history

  1. Received: February 6, 2018
  2. Accepted: July 16, 2018
  3. Accepted Manuscript published: July 17, 2018 (version 1)
  4. Accepted Manuscript updated: July 23, 2018 (version 2)
  5. Accepted Manuscript updated: July 24, 2018 (version 3)
  6. Version of Record published: August 13, 2018 (version 4)

Copyright

© 2018, Sanchez-Corrales 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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