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Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis

During embryogenesis, morphogens form a concentration gradient in responsive tissue, which is then translated into a spatial cellular pattern. The mechanisms by which morphogens spread through a tissue to establish such a morphogenetic field remain elusive. Here, we investigate by mutually complemen...

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Autores principales: Rosenbauer, Jakob, Zhang, Chengting, Mattes, Benjamin, Reinartz, Ines, Wedgwood, Kyle, Schindler, Simone, Sinner, Claude, Scholpp, Steffen, Schug, Alexander
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7340325/
https://www.ncbi.nlm.nih.gov/pubmed/32579554
http://dx.doi.org/10.1371/journal.pcbi.1007417
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author Rosenbauer, Jakob
Zhang, Chengting
Mattes, Benjamin
Reinartz, Ines
Wedgwood, Kyle
Schindler, Simone
Sinner, Claude
Scholpp, Steffen
Schug, Alexander
author_facet Rosenbauer, Jakob
Zhang, Chengting
Mattes, Benjamin
Reinartz, Ines
Wedgwood, Kyle
Schindler, Simone
Sinner, Claude
Scholpp, Steffen
Schug, Alexander
author_sort Rosenbauer, Jakob
collection PubMed
description During embryogenesis, morphogens form a concentration gradient in responsive tissue, which is then translated into a spatial cellular pattern. The mechanisms by which morphogens spread through a tissue to establish such a morphogenetic field remain elusive. Here, we investigate by mutually complementary simulations and in vivo experiments how Wnt morphogen transport by cytonemes differs from typically assumed diffusion-based transport for patterning of highly dynamic tissue such as the neural plate in zebrafish. Stochasticity strongly influences fate acquisition at the single cell level and results in fluctuating boundaries between pattern regions. Stable patterning can be achieved by sorting through concentration dependent cell migration and apoptosis, independent of the morphogen transport mechanism. We show that Wnt transport by cytonemes achieves distinct Wnt thresholds for the brain primordia earlier compared with diffusion-based transport. We conclude that a cytoneme-mediated morphogen transport together with directed cell sorting is a potentially favored mechanism to establish morphogen gradients in rapidly expanding developmental systems.
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spelling pubmed-73403252020-07-17 Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis Rosenbauer, Jakob Zhang, Chengting Mattes, Benjamin Reinartz, Ines Wedgwood, Kyle Schindler, Simone Sinner, Claude Scholpp, Steffen Schug, Alexander PLoS Comput Biol Research Article During embryogenesis, morphogens form a concentration gradient in responsive tissue, which is then translated into a spatial cellular pattern. The mechanisms by which morphogens spread through a tissue to establish such a morphogenetic field remain elusive. Here, we investigate by mutually complementary simulations and in vivo experiments how Wnt morphogen transport by cytonemes differs from typically assumed diffusion-based transport for patterning of highly dynamic tissue such as the neural plate in zebrafish. Stochasticity strongly influences fate acquisition at the single cell level and results in fluctuating boundaries between pattern regions. Stable patterning can be achieved by sorting through concentration dependent cell migration and apoptosis, independent of the morphogen transport mechanism. We show that Wnt transport by cytonemes achieves distinct Wnt thresholds for the brain primordia earlier compared with diffusion-based transport. We conclude that a cytoneme-mediated morphogen transport together with directed cell sorting is a potentially favored mechanism to establish morphogen gradients in rapidly expanding developmental systems. Public Library of Science 2020-06-24 /pmc/articles/PMC7340325/ /pubmed/32579554 http://dx.doi.org/10.1371/journal.pcbi.1007417 Text en © 2020 Rosenbauer et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Rosenbauer, Jakob
Zhang, Chengting
Mattes, Benjamin
Reinartz, Ines
Wedgwood, Kyle
Schindler, Simone
Sinner, Claude
Scholpp, Steffen
Schug, Alexander
Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title_full Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title_fullStr Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title_full_unstemmed Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title_short Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis
title_sort modeling of wnt-mediated tissue patterning in vertebrate embryogenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7340325/
https://www.ncbi.nlm.nih.gov/pubmed/32579554
http://dx.doi.org/10.1371/journal.pcbi.1007417
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