Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling.
Skeletal condensation occurs when specified mesenchyme cells self-organize over several days to form a distinctive cartilage template. Here, we determine how and when specified mesenchyme cells integrate mechanical and molecular information from their environment, forming cartilage condensations in...
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doaj-026be808c1b14747a01dddb2e3192b042020-11-25T00:44:19ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01108e013470210.1371/journal.pone.0134702Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling.Poulomi RaySusan C ChapmanSkeletal condensation occurs when specified mesenchyme cells self-organize over several days to form a distinctive cartilage template. Here, we determine how and when specified mesenchyme cells integrate mechanical and molecular information from their environment, forming cartilage condensations in the pharyngeal arches of chick embryos. By disrupting cytoskeletal reorganization, we demonstrate that dynamic cell shape changes drive condensation and modulate the response of the condensing cells to Fibroblast Growth Factor (FGF), Bone Morphogenetic Protein (BMP) and Transforming Growth Factor beta (TGF-β) signaling pathways. Rho Kinase (ROCK)-driven actomyosin contractions and Myosin II-generated differential cell cortex tension regulate these cell shape changes. Disruption of the condensation process inhibits the differentiation of the mesenchyme cells into chondrocytes, demonstrating that condensation regulates the fate of the mesenchyme cells. We also find that dorsal and ventral condensations undergo distinct cell shape changes. BMP signaling is instructive for dorsal condensation-specific cell shape changes. Moreover, condensations exhibit ventral characteristics in the absence of BMP signaling, suggesting that in the pharyngeal arches ventral morphology is the ground pattern. Overall, this study characterizes the interplay between cytoskeletal dynamics and molecular signaling in a self-organizing system during tissue morphogenesis.http://europepmc.org/articles/PMC4523177?pdf=render |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Poulomi Ray Susan C Chapman |
spellingShingle |
Poulomi Ray Susan C Chapman Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. PLoS ONE |
author_facet |
Poulomi Ray Susan C Chapman |
author_sort |
Poulomi Ray |
title |
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. |
title_short |
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. |
title_full |
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. |
title_fullStr |
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. |
title_full_unstemmed |
Cytoskeletal Reorganization Drives Mesenchymal Condensation and Regulates Downstream Molecular Signaling. |
title_sort |
cytoskeletal reorganization drives mesenchymal condensation and regulates downstream molecular signaling. |
publisher |
Public Library of Science (PLoS) |
series |
PLoS ONE |
issn |
1932-6203 |
publishDate |
2015-01-01 |
description |
Skeletal condensation occurs when specified mesenchyme cells self-organize over several days to form a distinctive cartilage template. Here, we determine how and when specified mesenchyme cells integrate mechanical and molecular information from their environment, forming cartilage condensations in the pharyngeal arches of chick embryos. By disrupting cytoskeletal reorganization, we demonstrate that dynamic cell shape changes drive condensation and modulate the response of the condensing cells to Fibroblast Growth Factor (FGF), Bone Morphogenetic Protein (BMP) and Transforming Growth Factor beta (TGF-β) signaling pathways. Rho Kinase (ROCK)-driven actomyosin contractions and Myosin II-generated differential cell cortex tension regulate these cell shape changes. Disruption of the condensation process inhibits the differentiation of the mesenchyme cells into chondrocytes, demonstrating that condensation regulates the fate of the mesenchyme cells. We also find that dorsal and ventral condensations undergo distinct cell shape changes. BMP signaling is instructive for dorsal condensation-specific cell shape changes. Moreover, condensations exhibit ventral characteristics in the absence of BMP signaling, suggesting that in the pharyngeal arches ventral morphology is the ground pattern. Overall, this study characterizes the interplay between cytoskeletal dynamics and molecular signaling in a self-organizing system during tissue morphogenesis. |
url |
http://europepmc.org/articles/PMC4523177?pdf=render |
work_keys_str_mv |
AT poulomiray cytoskeletalreorganizationdrivesmesenchymalcondensationandregulatesdownstreammolecularsignaling AT susancchapman cytoskeletalreorganizationdrivesmesenchymalcondensationandregulatesdownstreammolecularsignaling |
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