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Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer.

ABSTRACT: Polarized Wnt signaling along the primary body axis is a conserved property of axial patterning in bilaterians and prebilaterians, and depends on localized sources of Wnt ligands. However, the mechanisms governing the localized Wnt expression that emerged early in evolution are poorly understood. Here we find in the cnidarian Hydra that two functionally distinct cis-regulatory elements control the head organizer-associated Hydra Wnt3 (HyWnt3). An autoregulatory element, which mediates direct inputs of Wnt/β-catenin signaling, highly activates HyWnt3 transcription in the head region. In contrast, a repressor element is necessary and sufficient to restrict the activity of the autoregulatory element, thereby allowing the organizer-specific expression. Our results reveal that a combination of autoregulation and repression is crucial for establishing a Wnt-expressing organizing center in a basal metazoan. We suggest that this transcriptional control is an evolutionarily old strategy in the formation of Wnt signaling centers and metazoan axial patterning.

SUBMITTER: Nakamura Y

PROVIDER: S-EPMC3107325 | biostudies-literature | 2011 May

REPOSITORIES: biostudies-literature

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Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer.

Nakamura Yukio Y Tsiairis Charisios D CD Özbek Suat S Holstein Thomas W TW

Proceedings of the National Academy of Sciences of the United States of America 20110516 22

Polarized Wnt signaling along the primary body axis is a conserved property of axial patterning in bilaterians and prebilaterians, and depends on localized sources of Wnt ligands. However, the mechanisms governing the localized Wnt expression that emerged early in evolution are poorly understood. Here we find in the cnidarian Hydra that two functionally distinct cis-regulatory elements control the head organizer-associated Hydra Wnt3 (HyWnt3). An autoregulatory element, which mediates direct inp ...[more]

PMID: 21576458

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Project description:BACKGROUND:Axis patterning during development is accompanied by large-scale gene expression changes. These are brought about by changes in the histone modifications leading to dynamic alterations in chromatin architecture. The cis regulatory DNA elements also play an important role towards modulating gene expression in a context-dependent manner. Hydra belongs to the phylum Cnidaria where the first asymmetry in the body plan was observed and the oral-aboral axis originated. Wnt signaling has been shown to determine the head organizer function in the basal metazoan Hydra. RESULTS:To gain insights into the evolution of cis regulatory elements and associated chromatin signatures, we ectopically activated the Wnt signaling pathway in Hydra and monitored the genome-wide alterations in key histone modifications. Motif analysis of putative intergenic enhancer elements from Hydra revealed the conservation of bilaterian cis regulatory elements that play critical roles in development. Differentially regulated enhancer elements were identified upon ectopic activation of Wnt signaling and found to regulate many head organizer specific genes. Enhancer activity of many of the identified cis regulatory elements was confirmed by luciferase reporter assay. Quantitative chromatin immunoprecipitation analysis upon activation of Wnt signaling further confirmed the enrichment of H3K27ac on the enhancer elements of Hv_Wnt5a, Hv_Wnt11 and head organizer genes Hv_Bra1, CnGsc and Hv_Pitx1. Additionally, perturbation of the putative H3K27me3 eraser activity using a specific inhibitor affected the ectopic activation of Wnt signaling indicating the importance of the dynamic changes in the H3K27 modifications towards regulation of the genes involved in the head organizer activity. CONCLUSIONS:The activation-associated histone marks H3K4me3, H3K27ac and H3K9ac mark chromatin in a similar manner as seen in bilaterians. We identified intergenic cis regulatory elements which harbor sites for key transcription factors involved in developmental processes. Differentially regulated enhancers exhibited motifs for many zinc-finger, T-box and ETS related TFs whose homologs have a head specific expression in Hydra and could be a part of the pioneer TF network in the patterning of the head. The ability to differentially modify the H3K27 residue is critical for the patterning of Hydra axis revealing a dynamic acetylation/methylation switch to regulate gene expression and chromatin architecture.

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Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer.

Publications

Autoregulatory and repressive inputs localize Hydra Wnt3 to the head organizer.

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