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Rat and mouse imprintomes (allele-specific transcriptomes)

ABSTRACT: The rat is a widely used model for human physiology and psychology. However, due to their longer gestation periods and husbandry costs relative to mice, as well as the availability of superior molecular techniques to manipulate the mouse genome, relatively few genome-wide studies have been conducted in the rat. As such, a comprehensive analysis of genomic imprinting, which impacts complex traits such as growth and behaviour, has yet to be conducted in the rat. Towards this end, we systematically profiled embryonic and extra-embryonic tissue gene expression and DNA methylation with allele-specific resolution. We identified 14 embryonic and 26 extra-embryonic imprinted genes in the rat. Comparative analyses with mouse revealed that orthologous imprinted gene expression and associated canonical DNA methylation imprints are conserved in the embryo proper of the Muridae family. However, only 3 paternally expressed imprinted genes in the extra-embryonic embryo are conserved in Muridae, all of which are associated with non-canonical H3K27me3 imprints. The discovery of 8 novel candidate non-canonical imprinted genes unique to the rat is consistent with more rapid evolution of extra-embryonic imprinting. Cross-species analysis of novel rat imprinted genes with mouse and human revealed multiple mechanisms by which species-specific imprinted expression may be established, including H3K27me3 deposition in the oocyte, the birth of ZFP57 binding motifs and the insertion of endogenous retroviral promoters. Thus, characterization of the rat imprintome provides insights into the conservation of imprinted gene expression and the etiology of species-specific imprinting.

ORGANISM(S): Mus musculus Rattus norvegicus

PROVIDER: GSE185574 | GEO | 2023/01/19

REPOSITORIES: GEO

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Rat and mouse imprintomes (allele-specific DNA methylomes)

Project description:The rat is a widely used model for human physiology and psychology. However, due to their longer gestation periods and husbandry costs relative to mice, as well as the availability of superior molecular techniques to manipulate the mouse genome, relatively few genome-wide studies have been conducted in the rat. As such, a comprehensive analysis of genomic imprinting, which impacts complex traits such as growth and behaviour, has yet to be conducted in the rat. Towards this end, we systematically profiled embryonic and extra-embryonic tissue gene expression and DNA methylation with allele-specific resolution. We identified 14 embryonic and 26 extra-embryonic imprinted genes in the rat. Comparative analyses with mouse revealed that orthologous imprinted gene expression and associated canonical DNA methylation imprints are conserved in the embryo proper of the Muridae family. However, only 3 paternally expressed imprinted genes in the extra-embryonic embryo are conserved in Muridae, all of which are associated with non-canonical H3K27me3 imprints. The discovery of 8 novel candidate non-canonical imprinted genes unique to the rat is consistent with more rapid evolution of extra-embryonic imprinting. Cross-species analysis of novel rat imprinted genes with mouse and human revealed multiple mechanisms by which species-specific imprinted expression may be established, including H3K27me3 deposition in the oocyte, the birth of ZFP57 binding motifs and the insertion of endogenous retroviral promoters. Thus, characterization of the rat imprintome provides insights into the conservation of imprinted gene expression and the etiology of species-specific imprinting.

2023-01-19 | GSE186492 | GEO

Rat oocyte epigenomes

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Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues [RNA-Seq]

Project description:Background: Genomic imprinting is an epigenetic phenomenon that allows a subset of genes to be expressed mono-allelically based on parent-of-origin, and is typically regulated by differential DNA methylation inherited from gametes. Imprinting is pervasive in murine extra-embryonic lineages and, uniquely, the imprinting of several genes has been found to be conferred non-canonically through maternally-inherited repressive histone modification H3K27me3. However, the underlying regulatory mechanisms of non-canonical imprinting in post-implantation development remain unexplored. Results: We identify imprinted regions in post-implantation epiblast and extra-embryonic ectoderm (ExE) by assaying allelic histone modifications (H3K4me3, H3K36me3, H3K27me3), gene expression and DNA methylation in reciprocal C57BL/6 and CAST hybrid embryos. We distinguish loci with DNA methylation- dependent (canonical) and independent (non-canonical) imprinting by assaying hybrid embryos with ablated maternally-inherited DNA methylation. We find that non-canonical imprints are localized to endogenous retrovirus-K (ERVK) long terminal repeats (LTRs), which act as imprinted promoters specifically in extra-embryonic lineages. Transcribed ERVK LTRs are CpG-rich and located in close proximity to gene promoters, and imprinting status is determined by their epigenetic patterning in the oocyte. Finally, we show that oocyte-derived H3K27me3 associates with non-canonical imprints is not maintained beyond pre-implantation development, and is replaced by secondary imprinted DNA methylation on the maternal allele in post-implantation ExE, while being completely silenced by bi-allelic DNA methylation in epiblast. Conclusions: This study reveals distinct epigenetic mechanisms regulating non-canonical imprinted gene expression between embryonic and extra-embryonic development, and identifies an integral role for ERVK LTR repetitive elements.

2019-09-19 | GSE124215 | GEO

Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues [Bisulfite-Seq]

2019-09-19 | GSE124213 | GEO

Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues [ChIP-Seq]

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The conservation and divergence of epigenitic reprogramming during mammalian early development

Project description:To explore how parental epigenetic information is transmitted to the next generation across mammals, we systematically investigated the epigenomes of oocytes and early embryos among human, bovine, porcine, rat, and mouse. This unprecedented dataset revealed strikingly diverse, species-specific innovation of epigenetic transition. In oocytes, DNA methylation is restricted to active gene bodies in rodents, allowing methylation of maternal imprints but not intergenic paternal imprints. Strikingly, hypermethylation also occurs in non-transcribed regions in porcine and bovine, where paternal imprints instead reside in hypomethylated, megabase-long “CpG continents (CGCs)”. Despite the presence of H3K4me3 and H3K27me3 domains in non-human oocytes, only rodent H3K27me3 survives beyond genome activation, supporting H3K27me3-mediated imprinting. Coincidently, regulatory elements are segregated away from H3K27me3 domains, the ectopic invasion of which leads to aberrant embryonic transcription. Finally, human does not fully resemble any of the rest species. Hence, mammals invent diverse epigenetic inheritance and reprogramming which center around a delicate balance in establishing imprints while protecting other regulatory regions.

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Imprinted expression is different in visceral yolk sac and cystic embryoid body endoderm

Project description:Genomic imprinting is an epigenetic phenomenon resulting in parent-of-origin mono-allelic expression of a small subset of mammalian genes. Imprinted genes have been categorized into two groups: multi lineage (ML) imprinted genes that can show imprinted expression in both embryonic and extra-embryonic lineages, and genes that show extra-embryonic lineage (EXEL) specific imprinted expression restricted to tissues like the placenta and visceral yolk sac (VYS) endoderm. Many genes showing EXEL imprinted expression are silenced by lncRNAs that act over long distances. Thus the analysis of this form of gene silencing is likely to be pivotal for understanding new mechanisms of long range gene silencing by lncRNAs. It has been reported that ES cells differentiated into cystic embryoid bodies (cystic EBs) contain VYS endoderm and here we investigate if cystic EBs could serve as an in vitro model for the analysis of EXEL imprinted expression. Unexpectedly we found that cystic EBs lack EXEL imprinted expression, while retaining normal imprinted expression of ML genes. This shows that cystic EBs do not model VYS imprinted expression and also argues against previous claims that cystic EBs contain VYS endoderm. We further characterized cystic EBs by performing RNA-seq and whole genome bisulphite sequencing. By comparison to various embryonic tissues we found that cystic EBs more resemble embryonic liver, which contains definitive endoderm, than the extra-embryonic endoderm of the VYS. Examination of gene and retrotranssposone expression and DNA methylation in extraembryonic, embryonic tissues and ES cell diferentiated as cystic EBs

2015-07-22 | E-GEOD-56276 | biostudies-arrayexpress

Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues

Project description:Endogenous retroviral insertions drive non-canonical imprinting in extra-embryonic tissues

| PRJNA510996 | ENA

Imprinted expression is different in visceral yolk sac and cystic embryoid body endoderm

2015-07-22 | GSE56276 | GEO

Non-canonical imprinting ensures embryonic development and restrains placental overgrowth

Project description:Genomic imprinting regulates parental origin-dependent mono-allelic gene expression. It is mediated by either germline differential methylation of DNA (canonical imprinting) or oocyte-derived H3K27me3 (non-canonical imprinting) in mice. Depletion of Eed, an essential component of Polycomb repressive complex 2, results in genome-wide loss of H3K27me3 in oocytes, which causes loss of non-canonical imprinting (LOI) in embryos. Although Eed maternal KO (matKO) embryos show partial lethality after implantation, it is unknown whether LOI itself contributes to the developmental phenotypes of these embryos, which makes it unclear whether non-canonical imprinting is developmentally relevant. Here, by combinatorial matKO of Xist, a non-canonical imprinted gene whose LOI causes aberrant transient maternal X chromosome inactivation (XCI) at preimplantation, we show that prevention of the transient maternal XCI greatly restores the development of Eed matKO embryos. Moreover, we find that the placentae of Eed matKO embryos are remarkably enlarged in a manner independent of Xist LOI. Heterozygous deletion screening of individual autosomal non-canonical imprinted genes suggests that LOI of the Sfmbt2 miRNA cluster-chromosome 2 miRNA cluster (C2MC), solute carrier family 38 member 4 (Slc38a4), and Gm32885 contributes to the placental enlargement. Taken together, our study provides evidence that Xist imprinting sustains embryonic development and autosomal non-canonical imprinting restrains placental overgrowth.

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