Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
- University of Münster, Germany
- 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.
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All data generated or analysed during this study are included in the manuscript and supporting files.
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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.
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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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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