1. Cell Biology
  2. Developmental Biology
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Dpp controls growth and patterning in Drosophila wing precursors through distinct modes of action

  1. Pablo Sanchez Bosch
  2. Ruta Ziukaite
  3. Cyrille Alexandre
  4. Konrad Basler
  5. Jean-Paul B Vincent  Is a corresponding author
  1. University of Zurich, Switzerland
  2. The Francis Crick Institute, United Kingdom
  3. Institute of Molecular Life Sciences, Switzerland
Research Article
  • Cited 24
  • Views 2,889
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Cite this article as: eLife 2017;6:e22546 doi: 10.7554/eLife.22546

Abstract

Dpp, a member of the BMP family, is a morphogen that specifies positional information in Drosophila wing precursors. In this tissue, Dpp expressed along the anterior-posterior boundary forms a concentration gradient that controls the expression domains of target genes, which in turn specify the position of wing veins. Dpp also promotes growth in this tissue. The relationship between the spatio-temporal profile of Dpp signalling and growth has been the subject of debate, which has intensified recently with the suggestion that the stripe of Dpp is dispensable for growth. With two independent conditional alleles of dpp we find that the stripe of Dpp is essential for wing growth. We then show that this requirement, but not patterning, can be fulfilled by uniform, low level, Dpp expression. Thus, the stripe of Dpp ensures that signalling remains above a pro-growth threshold, while at the same time generating a gradient that patterns cell fates.

Article and author information

Author details

  1. Pablo Sanchez Bosch

    Institute of Molecular Life Sciences, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0574-4530
  2. Ruta Ziukaite

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Cyrille Alexandre

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Konrad Basler

    University of Zurich, Institute of Molecular Life Sciences, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  5. Jean-Paul B Vincent

    The Francis Crick Institute, London, United Kingdom
    For correspondence
    jp.vincent@crick.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2305-5744

Funding

Medical Research Council (FC001204)

  • Jean-Paul B Vincent

European Research Council (WNTEXPORT 294523)

  • Jean-Paul B Vincent

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Unknown)

  • Konrad Basler

Wellcome (PhD Studentship 105382/Z/14/Z)

  • Ruta Ziukaite

Wellcome (FC001204)

  • Jean-Paul B Vincent

Cancer Research UK (FC001204)

  • Jean-Paul B Vincent

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

Reviewing Editor

  1. Utpal Banerjee, University of California, Los Angeles, United States

Publication history

  1. Received: October 21, 2016
  2. Accepted: June 4, 2017
  3. Accepted Manuscript published: July 4, 2017 (version 1)
  4. Version of Record published: August 17, 2017 (version 2)

Copyright

© 2017, Sanchez Bosch 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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Further reading

    1. Cell Biology
    2. Developmental Biology
    Shinya Matsuda, Markus Affolter
    Short Report Updated

    The Dpp morphogen gradient derived from the anterior stripe of cells is thought to control growth and patterning of the Drosophila wing disc. However, the spatial-temporal requirement of dpp for growth and patterning remained largely unknown. Recently, two studies re-addressed this question. By generating a conditional null allele, one study proposed that the dpp stripe is critical for patterning but not for growth (Akiyama and Gibson, 2015). In contrast, using a membrane-anchored nanobody to trap Dpp, the other study proposed that Dpp dispersal from the stripe is required for patterning and also for medial wing disc growth, at least in the posterior compartment (Harmansa et al., 2015). Thus, growth control by the Dpp morphogen gradient remains under debate. Here, by removing dpp from the stripe at different time points, we show that the dpp stripe source is indeed required for wing disc growth, also during third instar larval stages.

    1. Cell Biology
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    Stefano Perni, Kurt Beam
    Research Article Updated

    Junctions between the endoplasmic reticulum and plasma membrane that are induced by the neuronal junctophilins are of demonstrated importance, but their molecular architecture is still poorly understood and challenging to address in neurons. This is due to the small size of the junctions and the multiple isoforms of candidate junctional proteins in different brain areas. Using colocalization of tagged proteins expressed in tsA201 cells, and electrophysiology, we compared the interactions of JPH3 and JPH4 with different calcium channels. We found that JPH3 and JPH4 caused junctional accumulation of all the tested high-voltage-activated CaV isoforms, but not a low-voltage-activated CaV. Also, JPH3 and JPH4 noticeably modify CaV2.1 and CaV2.2 inactivation rate. RyR3 moderately colocalized at junctions with JPH4, whereas RyR1 and RyR2 did not. By contrast, RyR1 and RyR3 strongly colocalized with JPH3, and RyR2 moderately. Likely contributing to this difference, JPH3 binds to cytoplasmic domain constructs of RyR1 and RyR3, but not of RyR2.