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

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 m...

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Main Authors: Julia Sauerwald, Wilko Backer, Till Matzat, Frank Schnorrer, Stefan Luschnig
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/48857
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spelling doaj-da70e966424c4ab4984d6330309028042021-05-05T17:58:25ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.48857Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight musclesJulia Sauerwald0Wilko Backer1Till Matzat2Frank Schnorrer3https://orcid.org/0000-0002-9518-7263Stefan Luschnig4https://orcid.org/0000-0002-0634-3368Institute for Zoophysiology, University of Münster, Münster, Germany; Cluster of Excellence EXC 1003, Cells in Motion (CiM), Münster, GermanyInstitute for Zoophysiology, University of Münster, Münster, Germany; Cluster of Excellence EXC 1003, Cells in Motion (CiM), Münster, GermanyInstitute for Zoophysiology, University of Münster, Münster, Germany; Cluster of Excellence EXC 1003, Cells in Motion (CiM), Münster, GermanyAix Marseille University, CNRS, IBDM, Marseille, FranceInstitute for Zoophysiology, University of Münster, Münster, Germany; Cluster of Excellence EXC 1003, Cells in Motion (CiM), Münster, GermanyTubular 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.https://elifesciences.org/articles/48857tracheal developmentbranching morphogenesismuscle developmentmatrix metalloproteinaseflight muscletube morphogenesis
collection DOAJ
language English
format Article
sources DOAJ
author Julia Sauerwald
Wilko Backer
Till Matzat
Frank Schnorrer
Stefan Luschnig
spellingShingle Julia Sauerwald
Wilko Backer
Till Matzat
Frank Schnorrer
Stefan Luschnig
Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
eLife
tracheal development
branching morphogenesis
muscle development
matrix metalloproteinase
flight muscle
tube morphogenesis
author_facet Julia Sauerwald
Wilko Backer
Till Matzat
Frank Schnorrer
Stefan Luschnig
author_sort Julia Sauerwald
title Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
title_short Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
title_full Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
title_fullStr Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
title_full_unstemmed Matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into Drosophila flight muscles
title_sort matrix metalloproteinase 1 modulates invasive behavior of tracheal branches during entry into drosophila flight muscles
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-10-01
description 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.
topic tracheal development
branching morphogenesis
muscle development
matrix metalloproteinase
flight muscle
tube morphogenesis
url https://elifesciences.org/articles/48857
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