Tiling Histone H3 Lysine 4 and 27 Methylation in Zebrafish Using High-Density Microarrays

Lindeman, Leif C.; Reiner, Andrew H.; Mathavan, Sinnakaruppan; Aleström, Peter; Collas, Philippe

doi:10.1371/journal.pone.0015651

Cited by 29 publications

(27 citation statements)

References 34 publications

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“…By contrast, nearly half of the RefSeq genes with the lowest or no expression were not marked at all and just 45% were marked by H3K4me3. These results suggest a direct correlation between binding of H3K4me3 or concordant binding of both H3K4me1 and H3K4me3 with levels of gene expression in the developing zebrafish embryo and are consistent with recent studies showing a similar correlation in a zebrafish cell line (Lindeman et al, 2010). …”

Section: Resultssupporting

confidence: 92%

Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites

Aday

Zhu

Lakshmanan

et al. 2011

Developmental Biology

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An organism’s genome sequence serves as a blueprint for the proteins and regulatory RNAs essential for cellular function. The genome also harbors cis-acting non-coding sequences that control gene expression and are essential to coordinate regulatory programs during embryonic development. However, the genome sequence is largely identical between cell types within a multi-cellular organism indicating that factors such as DNA accessibility and chromatin structure play a crucial role in governing cell-specific gene expression. Recent studies have identified particular chromatin modifications that define functionally distinct cis regulatory elements. Among these are forms of histone 3 that are mono- or tri-methylated at lysine 4 (H3K4me1 or H3K4me3, respectively), which bind preferentially to promoter and enhancer elements in the mammalian genome. In this work, we investigated whether these modified histones could similarly identify cis regulatory elements within the zebrafish genome. By applying chromatin immunoprecipitation followed by deep sequencing, we find that H3K4me1 and H3K4me3 are enriched at transcriptional start sites in the genome of the developing zebrafish embryo and that this association correlates with gene expression. We further find that these modifications associate with distal non-coding conserved elements, including known active enhancers. Finally, we demonstrate that it is possible to utilize H3K4me1 and H3K4me3 binding profiles in combination with available expression data to computationally identify relevant cis regulatory sequences flanking syn-expressed genes in the developing embryo. Taken together, our results indicate that H3K4me1 and H3K4me3 generally mark cis regulatory elements within the zebrafish genome and indicate that further characterization of the zebrafish using this approach will prove valuable in defining transcriptional networks in this model system.

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Section: Resultssupporting

confidence: 92%

Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites

Aday

Zhu

Lakshmanan

et al. 2011

Developmental Biology

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“…Methylation was assessed by methylated DNA immunoprecipitation (MeDIP) and hybridization to microarrays tiling 15 kb upstream and 5 kb downstream of the transcription start site (TSS) of 12,697 zebrafish RefSeq genes [18]. Comparisons of log 2 MeDIP/input ratios show robust correlation (R > 0.95) between MeDIP replicates and thus high MeDIP-chip reproducibility from early stage embryos (Additional file 1).…”

Section: Resultsmentioning

confidence: 99%

Developmental features of DNA methylation during activation of the embryonic zebrafish genome

et al. 2012

Self Cite

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BackgroundZygotic genome activation (ZGA) occurs at the mid-blastula transition (MBT) in zebrafish and is a period of extensive chromatin remodeling. Genome-scale gametic demethylation and remethylation occurs after fertilization, during blastula stages, but how ZGA relates to promoter DNA methylation states is unknown. Using methylated DNA immunoprecipitation coupled to high-density microarray hybridization, we characterize genome-wide promoter DNA methylation dynamics before, during and after ZGA onset, in relation to changes in post-translational histone modifications and gene expression.ResultsWe show methylation of thousands of promoters before ZGA and additional methylation after ZGA, finding more dynamic methylation -1 to 0 kb upstream of the transcription start site than downstream. The MBT is marked by differential methylation of high and low CpG promoters, and we identify hypomethylated promoters that are mostly CG-rich and remain hypomethylated through the MBT. Hypomethylated regions constitute a platform for H3K4me3, whereas H3K9me3 preferentially associates with methylated regions. H3K27me3 associates with either methylation state depending on its coincidence with H3K4me3 or H3K9me3. Cohorts of genes differentially expressed through the MBT period display distinct promoter methylation patterns related to CG content rather than transcriptional fate. Lastly, although a significant proportion of genes methylated in sperm are unmethylated in embryos, over 90% of genes methylated in embryos are also methylated in sperm.ConclusionsOur results suggest a pre-patterning of developmental gene expression potential by a combination of DNA hypomethylation and H3K4 trimethylation on CG-rich promoters, and are consistent with a transmission of DNA methylation states from gametes to early embryos.

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“…The epigenetic landscape in zebrafish embryos had been widely studied by microarray analysis [189,190,191]. Zebrafish embryos first develop from messenger RNAs (mRNAs) and proteins stored in the egg without ongoing transcription [192,193].…”

Section: Epigenetic Effects Of Ionizing Radiation In Zebrafishmentioning

confidence: 99%

Zebrafish as an In Vivo Model to Assess Epigenetic Effects of Ionizing Radiation

Kong

Cheng

2016

IJMS

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Exposure to ionizing radiations (IRs) is ubiquitous in our environment and can be categorized into “targeted” effects and “non-targeted” effects. In addition to inducing deoxyribonucleic acid (DNA) damage, IR exposure leads to epigenetic alterations that do not alter DNA sequence. Using an appropriate model to study the biological effects of radiation is crucial to better understand IR responses as well as to develop new strategies to alleviate exposure to IR. Zebrafish, Danio rerio, is a scientific model organism that has yielded scientific advances in several fields and recent studies show the usefulness of this vertebrate model in radiation biology. This review briefly describes both “targeted” and “non-targeted” effects, describes the findings in radiation biology using zebrafish as a model and highlights the potential of zebrafish to assess the epigenetic effects of IR, including DNA methylation, histone modifications and miRNA expression. Other in vivo models are included to compare observations made with zebrafish, or to illustrate the feasibility of in vivo models when the use of zebrafish was unavailable. Finally, tools to study epigenetic modifications in zebrafish, including changes in genome-wide DNA methylation, histone modifications and miRNA expression, are also described in this review.

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Tiling Histone H3 Lysine 4 and 27 Methylation in Zebrafish Using High-Density Microarrays

Cited by 29 publications

References 34 publications

Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites

Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites

Developmental features of DNA methylation during activation of the embryonic zebrafish genome

Zebrafish as an In Vivo Model to Assess Epigenetic Effects of Ionizing Radiation

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