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Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis.

ABSTRACT: 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.

SUBMITTER: Rosenbauer J

PROVIDER: S-EPMC7340325 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis.

Rosenbauer Jakob J Zhang Chengting C Mattes Benjamin B Reinartz Ines I Wedgwood Kyle K Schindler Simone S Sinner Claude C Scholpp Steffen S Schug Alexander A

PLoS computational biology 20200624 6

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 pl ...[more]

PMID: 32579554

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Project description:This study presents statistical analyses of gene expression during all 40 developmental stages in the teleost Fundulus heteroclitus using four biological replicates per stage. Patterns of gene expression for 7,000 genes appear to be important as they recapitulate developmental timing. Among the 45% of genes with significant expression differences between pairs of temporally adjacent stages, significant differences in gene expression vary from as few as five to more than 660. Five adjacent stages have disproportionately more significant changes in gene expression (>200 genes) relative to other stages: four to eight and eight to sixteen cell stages, onset of circulation, pre- and post-hatch, and during complete yolk absorption. The fewest differences among adjacent stages occur during gastrulation. Yet, at stage 16 (pre-mid-gastrulation), the largest number of genes has peak expression. This stage has an over-representation of genes in oxidative respiration and protein expression (ribosomes, translational genes and proteases). Unexpectedly, among all ribosomal genes, both strong positive and negative correlations occur. Similar correlated patterns of expression occur among all significant genes. These data provide statistical support for the temporal dynamics of developmental gene expression during all stages of vertebrate development. A double-loop design was used for the microarray hybridizations, where each sample is hybridized to 2 arrays using both Cy3- and Cy5-labelled fluorophores (Kerr and Churchill 2001a; Kerr and Churchill 2001b). The loop consisted of Cy3- and Cy5-labelled embryo aRNAs from 4 biological pools for each of 40 stages (S). In total, 160 biological pools were hybridized to 80 microarrays. Each array had different combinations of biological pools (Altman and Hua 2006). The double loop formed was S1M-bM-^FM-^R S2 M-bM-^FM-^R S3M-bM-^FM-^R M-bM-^@M-& S40M-bM-^FM-^R S1 and S40M-bM-^FM-^R S39M-bM-^FM-^R S38M-bM-^FM-^R M-bM-^@M-& S2M-bM-^FM-^R S1 M-bM-^FM-^R S40, where each arrow represents a separate hybridization (array) with the biological pool at the base of the arrow labeled with Cy3 and the biological pool at the head of the arrow labelled with Cy5.

Dataset Information

Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis.

Publications

Modeling of Wnt-mediated tissue patterning in vertebrate embryogenesis.

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