Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles

  1. Julia Sauerwald
  2. Wilko Backer
  3. Till Matzat
  4. Frank Schnorrer
  5. Stefan Luschnig  Is a corresponding author
  1. University of Münster, Germany
  2. Aix Marseille University, France

Abstract

Tubular networks like the vasculature extend branches throughout animal bodies, but how developing vessels interact with and invade tissues is not well understood. We investigated the underlying mechanisms using the developing tracheal tube network of Drosophila indirect flight muscles (IFMs) as a model. Live imaging revealed that tracheal sprouts invade IFMs directionally with growth-cone-like structures at branch tips. Ramification inside IFMs proceeds until tracheal branches fill the myotube. However, individual tracheal cells occupy largely separate territories, possibly mediated by cell-cell repulsion. Matrix metalloproteinase 1 (MMP1) is required in tracheal cells for normal invasion speed and for the dynamic organization of growth-cone-like branch tips. MMP1 remodels the CollagenIV-containing matrix around branch tips, which show differential matrix composition with low CollagenIV levels, while Laminin is present along tracheal branches. Thus, tracheal-derived MMP1 sustains branch invasion by modulating the dynamic behavior of sprouting branches as well as properties of the surrounding matrix.

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. Julia Sauerwald

    Institute of Zoophysiology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Wilko Backer

    Institute of Zoophysiology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Till Matzat

    Institute of Zoophysiology, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Frank Schnorrer

    Aix Marseille University, Marseille, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9518-7263
  5. Stefan Luschnig

    Institute of Zoophysiology, University of Münster, Münster, Germany
    For correspondence
    luschnig@uni-muenster.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0634-3368

Funding

Boehringer Ingelheim Fonds (Fellowship)

  • Julia Sauerwald

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (SNF 31003A_141093_1)

  • Julia Sauerwald
  • Till Matzat
  • Stefan Luschnig

Deutsche Forschungsgemeinschaft (Cluster of Excellence)

  • Julia Sauerwald
  • Wilko Backer
  • Till Matzat
  • Stefan Luschnig

European Molecular Biology Organization (Young Investigator Programme)

  • Frank Schnorrer

H2020 European Research Council (310939)

  • Frank Schnorrer

Centre National de la Recherche Scientifique

  • Frank Schnorrer

Excellence Initiative Aix-Marseille University AMIDEX (ANR-11-IDEX-0001-02)

  • Frank Schnorrer

LabEX-INFORM (ANR-11-LABX-0054)

  • Frank Schnorrer

Bettencourt Foundation

  • Frank Schnorrer

Deutsche Forschungsgemeinschaft (CRC 1348)

  • Stefan Luschnig

Deutsche Forschungsgemeinschaft (CRC 1009)

  • Stefan Luschnig

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

Reviewing Editor

  1. K VijayRaghavan, National Centre for Biological Sciences, Tata Institute of Fundamental Research, India

Version history

  1. Received: May 28, 2019
  2. Accepted: October 1, 2019
  3. Accepted Manuscript published: October 2, 2019 (version 1)
  4. Version of Record published: October 16, 2019 (version 2)

Copyright

© 2019, Sauerwald 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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  1. Julia Sauerwald
  2. Wilko Backer
  3. Till Matzat
  4. Frank Schnorrer
  5. Stefan Luschnig
(2019)
Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
eLife 8:e48857.
https://doi.org/10.7554/eLife.48857

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https://doi.org/10.7554/eLife.48857

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