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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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 |
work_keys_str_mv |
AT juliasauerwald matrixmetalloproteinase1modulatesinvasivebehavioroftrachealbranchesduringentryintodrosophilaflightmuscles AT wilkobacker matrixmetalloproteinase1modulatesinvasivebehavioroftrachealbranchesduringentryintodrosophilaflightmuscles AT tillmatzat matrixmetalloproteinase1modulatesinvasivebehavioroftrachealbranchesduringentryintodrosophilaflightmuscles AT frankschnorrer matrixmetalloproteinase1modulatesinvasivebehavioroftrachealbranchesduringentryintodrosophilaflightmuscles AT stefanluschnig matrixmetalloproteinase1modulatesinvasivebehavioroftrachealbranchesduringentryintodrosophilaflightmuscles |
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1721458909621780480 |