Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
06 2020
Historique:
received: 19 09 2019
accepted: 14 05 2020
revised: 07 07 2020
pubmed: 25 6 2020
medline: 25 8 2020
entrez: 25 6 2020
Statut: epublish

Résumé

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.

Identifiants

pubmed: 32579554
doi: 10.1371/journal.pcbi.1007417
pii: PCOMPBIOL-D-19-01606
pmc: PMC7340325
doi:

Substances chimiques

Wnt Proteins 0
beta Catenin 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1007417

Subventions

Organisme : Medical Research Council
ID : MR/S007970/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT105618MA
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P01478X/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/S016295/1
Pays : United Kingdom

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Jakob Rosenbauer (J)

John von Neumann Institute for Computing, Jülich Supercomputer Centre, Forschungszentrum Jülich, Jülich, Germany.

Chengting Zhang (C)

Living Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.

Benjamin Mattes (B)

Living Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.

Ines Reinartz (I)

Steinbuch Centre for Computing, Karlsruhe Institute for Technology, Karlsruhe, Germany.
Department of Physics, Karlsruhe Institute of Technology, Karlsruhe, Germany.

Kyle Wedgwood (K)

Living Systems Institute, Centre for Biomedical Modelling and Analysis, College of Engineering, Mathematics, and Physical Sciences, University of Exeter, Exeter, United Kingdom.

Simone Schindler (S)

Living Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.

Claude Sinner (C)

Steinbuch Centre for Computing, Karlsruhe Institute for Technology, Karlsruhe, Germany.
Department of Physics, Karlsruhe Institute of Technology, Karlsruhe, Germany.

Steffen Scholpp (S)

Living Systems Institute, School of Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter, United Kingdom.

Alexander Schug (A)

John von Neumann Institute for Computing, Jülich Supercomputer Centre, Forschungszentrum Jülich, Jülich, Germany.
Faculty of Biology, University of Duisburg-Essen, Essen, Germany.

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Classifications MeSH