Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster
Tissue function and shape rely on the organization of the extracellular matrix (ECM) produced by the respective cells. Our understanding of the underlying molecular mechanisms is limited. Here, we show that extracellular Tweedle (Twdl) proteins in the fruit fly Drosophila melanogaster form two adjac...
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Format: | Article |
Language: | English |
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The Royal Society
2020-12-01
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Series: | Open Biology |
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Online Access: | https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.200214 |
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author | Renata Zuber Yiwen Wang Nicole Gehring Slawomir Bartoszewski Bernard Moussian |
author_facet | Renata Zuber Yiwen Wang Nicole Gehring Slawomir Bartoszewski Bernard Moussian |
author_sort | Renata Zuber |
collection | DOAJ |
description | Tissue function and shape rely on the organization of the extracellular matrix (ECM) produced by the respective cells. Our understanding of the underlying molecular mechanisms is limited. Here, we show that extracellular Tweedle (Twdl) proteins in the fruit fly Drosophila melanogaster form two adjacent two-dimensional sheets underneath the cuticle surface and above a distinct layer of dityrosinylated and probably elastic proteins enwrapping the whole body. Dominant mutations in twdl genes cause ectopic spherical aggregation of Twdl proteins that recruit dityrosinylated proteins at their periphery within lower cuticle regions. These aggregates perturb parallel ridges at the surface of epidermal cells that have been demonstrated to be crucial for body shaping. In one scenario, hence, this disorientation of epidermal ridges may explain the squatty phenotype of Twdl mutant larvae. In an alternative scenario, this phenotype may be due to the depletion of the dityrosinylated and elastic layer, and the consequent weakening of cuticle resistance against the internal hydrostatic pressure. According to Barlow's formula describing the distribution of internal pressure forces in pipes in dependence of pipe wall material properties, it follows that this reduction in turn causes lateral expansion at the expense of the antero-posterior elongation of the body. |
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id | doaj.art-6918e81ffd7e495d813b3eea28a5c42e |
institution | Directory Open Access Journal |
issn | 2046-2441 |
language | English |
last_indexed | 2024-12-16T13:25:12Z |
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spelling | doaj.art-6918e81ffd7e495d813b3eea28a5c42e2022-12-21T22:30:14ZengThe Royal SocietyOpen Biology2046-24412020-12-01101210.1098/rsob.200214200214Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogasterRenata ZuberYiwen WangNicole GehringSlawomir BartoszewskiBernard MoussianTissue function and shape rely on the organization of the extracellular matrix (ECM) produced by the respective cells. Our understanding of the underlying molecular mechanisms is limited. Here, we show that extracellular Tweedle (Twdl) proteins in the fruit fly Drosophila melanogaster form two adjacent two-dimensional sheets underneath the cuticle surface and above a distinct layer of dityrosinylated and probably elastic proteins enwrapping the whole body. Dominant mutations in twdl genes cause ectopic spherical aggregation of Twdl proteins that recruit dityrosinylated proteins at their periphery within lower cuticle regions. These aggregates perturb parallel ridges at the surface of epidermal cells that have been demonstrated to be crucial for body shaping. In one scenario, hence, this disorientation of epidermal ridges may explain the squatty phenotype of Twdl mutant larvae. In an alternative scenario, this phenotype may be due to the depletion of the dityrosinylated and elastic layer, and the consequent weakening of cuticle resistance against the internal hydrostatic pressure. According to Barlow's formula describing the distribution of internal pressure forces in pipes in dependence of pipe wall material properties, it follows that this reduction in turn causes lateral expansion at the expense of the antero-posterior elongation of the body.https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.200214drosophilaecmcuticlebody shapeepidermis |
spellingShingle | Renata Zuber Yiwen Wang Nicole Gehring Slawomir Bartoszewski Bernard Moussian Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster Open Biology drosophila ecm cuticle body shape epidermis |
title | Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster |
title_full | Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster |
title_fullStr | Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster |
title_full_unstemmed | Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster |
title_short | Tweedle proteins form extracellular two-dimensional structures defining body and cell shape in Drosophila melanogaster |
title_sort | tweedle proteins form extracellular two dimensional structures defining body and cell shape in drosophila melanogaster |
topic | drosophila ecm cuticle body shape epidermis |
url | https://royalsocietypublishing.org/doi/pdf/10.1098/rsob.200214 |
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