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Ronin governs early heart development by controlling core gene programs

ABSTRACT: Ronin (THAP11), an idiosyncratic DNA-binding protein that evolved from a primordial DNA transposon by molecular domestication, recognizes a hyperconserved promoter sequence through which it controls a variety of developmentally and metabolically essential genes in pluripotent stem cells. However, it remains unclear whether Ronin or related THAP proteins perform similar functions elsewhere in development. Here, we present evidence indicating that Ronin performs a novel function within the nascent heart as it arises from the mesoderm and forms a four-chambered organ. We show that Ronin is vital for cardiogenesis during midgestation through its control of a core set of critical genes. The activity of Ronin coincided with the recruitment of its cofactor, Hcf-1, and the elevation of H3K4me3 levels at specific target genes, suggesting the involvement of an epigenetic mechanism. On the strength of these findings, we propose that Ronin activity during cardiogenesis may offer a template that could be used to understand how important gene programs are sustained across different cell types within a developing organ, such as the heart.

ORGANISM(S): Mus musculus

PROVIDER: GSE103959 | GEO | 2017/09/19

SECONDARY ACCESSION(S): PRJNA407786

REPOSITORIES: GEO

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Project description:Analysis of transcriptional regulation in human cells has implicated a large number of promoter-specific DNA-binding proteins that regulate transcription via diverse mechanisms. In some cases, these DNA-sequence-specific factors associate with intermediaries that orchestrate interactions with the chromatin-modifying enzymes. One such intermediary is HCF-1 (host-cell factor-1; HCFC1). HCF-1, first identified for its involvement in herpes-simplex virus transcription and subsequently shown to be an important cell-cycle regulator, has a poorly defined role in genome-wide transcriptional regulation. We show here, by chromatin immunoprecipitation followed by high-throughput sequence analysis (ChIP-seq), that HCF-1 is a major transcriptional start site associated factor, whose promoter association correlates positively with transcriptional activity. Thus, in HeLa cells HCF-1 is observed on 5400 generally active CpG-island promoters. Examination of the DNA sequences underlying the HCF-1-binding sites revealed three sequence motifs associated with the binding of (i) ZNF143 and Ronin/THAP11, (ii) GABP, and (iii) YY1 sequence-specific transcription factors. Subsequent ChIP-seq analysis of these four transcription factors revealed a large co-association of HCF-1 with these four transcription factors at approximately 90% of HCF-1-bound promoters. These studies suggest that a relatively small number of transcription factors -- some (ZNF143 and Ronin/THAP11) in novel combinations -- play a major role in HeLa-cell transcriptional regulation in association with HCF-1. This experiment includes the sequencing data of material obtained from chromatin immunoprecipitation using antibodies against HCFC1(antibodies against the C-subunit and the N-subunit), PolII(antibody against the RPB2 subunit), H3K36ME3 and H3K4Me3 histone modifications, ZNF143, THAP11, GABPalpha and YY1. It also includes control data of the Input material. All of them were done using HeLa cycling cells.

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Ronin governs early heart development by controlling core gene programs

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