Genomics,Multiomics

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H3K27me3 deposition over sarcomeric and cytoskeletal promoters is required for cardiomyocyte cytokinesis and wound invasion during zebrafish heart regeneration [ChIP-seq]


ABSTRACT: Deciphering the genetic and epigenetic regulation of injury-induced heart regeneration in organisms capable of robust cardiac renewal represents an attractive inroad towards regenerating the human heart. In the highly regenerative zebrafish heart, cardiomyocytes near the wound edge undergo dramatic gene expression changes concomitant with sarcomere disassembly, loss of cell-cell adhesion, and detachment from the extracellular matrix (ECM), which leaves them poised to divide and give rise to new muscle cells that colonize the wound. Using integrated high-throughput transcriptional and chromatin analyses, we identified correlations between gene expression changes and activating H3K4me3 and/or repressive H3K27me3 dynamics in cardiomyocytes following injury. Within the category of downregulated genes that gain H3K27me3, transcripts encoding sarcomere and cytoskeletal components were significantly overrepresented. To investigate a functional requirement for H3K27me3-mediated gene silencing during zebrafish heart regeneration, we generated an inducible transgenic strain expressing a mutant version of histone 3, H3.3K27M, which allowed us to inhibit H3K27me3 catalysis in cardiomyocytes during the regenerative window. Hearts composed of H3.3K27M-expressing cardiomyocytes fail to regenerate with wound edge myocardium showing heightened expression of structural genes and prominent sarcomere structures. Although cell cycle re-entry was unperturbed, cytokinesis and wound invasion were significantly compromised. Collectively, our study identifies a requirement for H3K27me3-mediated silencing of structural genes during zebrafish heart regeneration and suggests that repression of similar structural components in the border zone of the infarcted human heart might improve its regenerative capacity. Overall design: Examination of 2 different histone modifications in enriched cardiomyocyte samples from uninjured and regenerating zebrafish hearts with three biological replicates.

INSTRUMENT(S): Illumina NextSeq 500 (Danio rerio)

ORGANISM(S): Danio rerio  

SUBMITTER: Raz Ben-Yair  

PROVIDER: GSE96928 | GEO | 2019-09-17

REPOSITORIES: GEO

Dataset's files

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GSE96928_ChIP_Seq_H3K27me3.csv.gz Csv
GSE96928_ChIP_Seq_H3K4me3.csv.gz Csv
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Publications

H3K27me3-mediated silencing of structural genes is required for zebrafish heart regeneration.

Ben-Yair Raz R   Butty Vincent L VL   Busby Michele M   Qiu Yutong Y   Levine Stuart S SS   Goren Alon A   Boyer Laurie A LA   Burns C Geoffrey CG   Burns Caroline E CE  

Development (Cambridge, England) 20191009 19


Deciphering the genetic and epigenetic regulation of cardiomyocyte proliferation in organisms that are capable of robust cardiac renewal, such as zebrafish, represents an attractive inroad towards regenerating the human heart. Using integrated high-throughput transcriptional and chromatin analyses, we have identified a strong association between H3K27me3 deposition and reduced sarcomere and cytoskeletal gene expression in proliferative cardiomyocytes following cardiac injury in zebrafish. To mov  ...[more]

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