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An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [ChIP-Seq]

ABSTRACT: Head regeneration in Hydra requires the transformation of gastric tissue into a head organizer that produces a head activator and a head inhibitor. Here we report the decipherment of a long-standing question in developmental biology, the identification of the transcription factor Sp5 as a key head inhibitory component. We show that Sp5 has an apical to basal graded expression pattern in intact Hydra, its expression is induced upon Wnt/β-catenin signaling activation and when knocked-down triggers the formation of multiple heads and axes in homeostatic and regenerative conditions. Our data indicate that Sp5 acts in a feed-forward loop to robustly regulate its own expression and that Sp5 prevents head formation by repressing the Wnt3 promoter. This Sp5 mediated Wnt antagonism is conserved and was invented early in metazoan evolution to set up axial patterning.

ORGANISM(S): Homo sapiens

PROVIDER: GSE121316 | GEO | 2019/01/18

REPOSITORIES: GEO

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An evolutionary conserved Sp5-Wnt3 regulatory module contributes to restrict head organizer activity in Hydra

2019-03-01 | GSE110277 | GEO

An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [RNA-Seq]

Project description:Head regeneration in Hydra requires the transformation of gastric tissue into a head organizer that produces a head activator and a head inhibitor. Here we report the decipherment of a long-standing question in developmental biology, the identification of the transcription factor Sp5 as a key head inhibitory component. We show that Sp5 has an apical to basal graded expression pattern in intact Hydra, its expression is induced upon Wnt/β-catenin signaling activation and when knocked-down triggers the formation of multiple heads and axes in homeostatic and regenerative conditions. Our data indicate that Sp5 acts in a feed-forward loop to robustly regulate its own expression and that Sp5 prevents head formation by repressing the Wnt3 promoter. This Sp5 mediated Wnt antagonism is conserved and was invented early in metazoan evolution to set up axial patterning. To gain insights on the evolution of the transcriptional properties of the Sp5 gene, we analyzed the capacity of the hydra Sp5 and zebrafish Sp5a paralogs to bind to cis-regulatory elements of the contitutively active human genome and to regulate the expression of the corresponding target genes. To this end, we transfected HEK293 cells with plasmids encoding for either hySp5 or zfSp5a proteins and we performed ChIPseq and RNAseq experiments to analyze their genomic occupancies and the changes in the transcriptional profiles induced upon transfection.

2019-01-18 | GSE121317 | GEO

An evolutionary conserved Sp5-Wnt3 regulatory module contributes to restrict head organizer activity in Hydra

Project description:An evolutionary conserved Sp5-Wnt3 regulatory module contributes to restrict head organizer activity in Hydra

| PRJNA433362 | ENA

An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra

Project description:An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra

| PRJNA497058 | ENA

An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [RNA-Seq]

Project description:An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [RNA-Seq]

| PRJNA497062 | ENA

An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [ChIP-Seq]

Project description:An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra [ChIP-Seq]

| PRJNA497061 | ENA

An evolutionarily-conserved Wnt3/?-catenin/Sp5 feedback loop restricts head organizer activity in Hydra.

Project description:Polyps of the cnidarian Hydra maintain their adult anatomy through two developmental organizers, the head organizer located apically and the foot organizer basally. The head organizer is made of two antagonistic cross-reacting components, an activator, driving apical differentiation and an inhibitor, preventing ectopic head formation. Here we characterize the head inhibitor by comparing planarian genes down-regulated when ?-catenin is silenced to Hydra genes displaying a graded apical-to-basal expression and an up-regulation during head regeneration. We identify Sp5 as a transcription factor that fulfills the head inhibitor properties: leading to a robust multiheaded phenotype when knocked-down in Hydra, acting as a transcriptional repressor of Wnt3 and positively regulated by Wnt/?-catenin signaling. Hydra and zebrafish Sp5 repress Wnt3 promoter activity while Hydra Sp5 also activates its own expression, likely via ?-catenin/TCF interaction. This work identifies Sp5 as a potent feedback loop inhibitor of Wnt/?-catenin signaling, a function conserved across eumetazoan evolution.

| S-EPMC6338789 | biostudies-literature

The Hydra magnipapillata head regeneration transcriptome

Project description:Hydra has long been studied for its remarkable ability to regenerate its head. Previous studies focusing on molecular mechanisms of axial patterning and head regeneration using a candidate gene approach have revealed a central role for the canonical Wnt pathway. We performed a global gene expression analysis during Hydra magnipapillata head regeneration using RNA-seq to identify additional genes that are transcriptionally regulated during the regeneration of the head organizer in hydra. Differential expression analysis revealed a set of 4,978 genes with significant changes during a 48-hour head regeneration time-course that includes many key genes in the Wnt, TGF-M-NM-2/BMP and MAP kinase pathways. We observed the differential regulation of several genes that are part of the epithelial-to-mesenchymal transition in bilaterians such as Snail. We assembled 806 novel putative lincRNAs with 176 of these are differentially expressed during the time course. We observed the coordinated transcriptional regulation of several factors that regulate the effective pool of free M-NM-2-catenin that together synergize to increase the amount of M-NM-2-catenin available for transcriptional regulation of downstream genes. The differential expression of Snail and some of its interacting regulators and downstream targets suggests that a partial-EMT-like response is involved in hydra head regeneration. This time-course is a valuable resource for the study of the transcriptional dynamics of head regeneration in hydra. mRNA profiling of regenerating head from 6 time points post bisection of Hydra head (H. magnipapillata), generated by deep sequencing, in duplicates, using Illumina HiSeq2500.

2014-12-13 | E-GEOD-64127 | biostudies-arrayexpress

The Hydra magnipapillata head regeneration transcriptome

Project description:Hydra has long been studied for its remarkable ability to regenerate its head. Previous studies focusing on molecular mechanisms of axial patterning and head regeneration using a candidate gene approach have revealed a central role for the canonical Wnt pathway. We performed a global gene expression analysis during Hydra magnipapillata head regeneration using RNA-seq to identify additional genes that are transcriptionally regulated during the regeneration of the head organizer in hydra. Differential expression analysis revealed a set of 4,978 genes with significant changes during a 48-hour head regeneration time-course that includes many key genes in the Wnt, TGF-β/BMP and MAP kinase pathways. We observed the differential regulation of several genes that are part of the epithelial-to-mesenchymal transition in bilaterians such as Snail. We assembled 806 novel putative lincRNAs with 176 of these are differentially expressed during the time course. We observed the coordinated transcriptional regulation of several factors that regulate the effective pool of free β-catenin that together synergize to increase the amount of β-catenin available for transcriptional regulation of downstream genes. The differential expression of Snail and some of its interacting regulators and downstream targets suggests that a partial-EMT-like response is involved in hydra head regeneration. This time-course is a valuable resource for the study of the transcriptional dynamics of head regeneration in hydra.

2014-12-13 | GSE64127 | GEO

Differential gene regulation in DAPT-treated Hydra reveals candidate direct Notch signalling targets

Project description:In Hydra, Notch inhibition causes defects in head patterning and prevents differentiation of proliferating nematocyte progenitor cells into mature nematocytes. To understand the molecular mechanisms by which the Notch pathway regulates these processes, we performed RNA-seq and identified genes that are differentially regulated in response to 48 h of treating the animals with the Notch inhibitor DAPT. To identify candidate direct regulators of Notch signalling, we profiled gene expression changes that occur during subsequent restoration of Notch activity and performed promoter analyses to identify RBPJ transcription factor-binding sites in the regulatory regions of Notch-responsive genes. Interrogating the available single-cell sequencing data set revealed the gene expression patterns of Notch-regulated Hydra genes. Through these analyses, a comprehensive picture of the molecular pathways regulated by Notch signalling in head patterning and in interstitial cell differentiation in Hydra emerged. As prime candidates for direct Notch target genes, in addition to Hydra (Hy)Hes, we suggest Sp5 and HyAlx. They rapidly recovered their expression levels after DAPT removal and possess Notch-responsive RBPJ transcription factorbinding sites in their regulatory regions

2021-09-27 | GSE184492 | GEO

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