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Hanna, C.W.* ; Pérez-Palacios, R.* ; Gahurova, L.* ; Schubert, M.* ; Krueger, F.* ; Biggins, L.* ; Andrews, S.* ; Colomé-Tatché, M. ; Bourc'his, D.* ; Dean, W.* ; Kelsey, G.*

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

Genome Biol. 20:225 (2019)
Publ. Version/Full Text DOI PMC
Open Access Gold
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Background: Genomic imprinting is an epigenetic phenomenon that allows a subset of genes to be expressed mono-allelically based on the 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 postimplantation 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 associated with non-canonical imprints is not maintained beyond pre-implantation development at these elements 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 the 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.
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Publication type Article: Journal article
Document type Scientific Article
Keywords Genomic Imprinting ; Histone Modifications ; Extra-embryonic ; Development ; Embryo ; H3k27me3 ; Non-canonical Imprinting ; Long Terminal Repeats (ltrs) ; Placenta ; Endogenous Retroviruses (ervs); Allelic Bivalent Chromatin; De-novo Methylation; Dna Methylation; Histone Modifications; Mammalian Development; Mouse; Placenta; Genome; Transcription; Receptor
Language english
Publication Year 2019
HGF-reported in Year 2019
ISSN (print) / ISBN 1474-760X
e-ISSN 1465-6906
Journal Genome Biology
Quellenangaben Volume: 20, Issue: 1, Pages: , Article Number: 225 Supplement: ,
Publisher BioMed Central
Publishing Place Campus, 4 Crinan St, London N1 9xw, England
Reviewing status Peer reviewed
Institute(s) Institute of Computational Biology (ICB)
POF-Topic(s) 30205 - Bioengineering and Digital Health
Research field(s) Enabling and Novel Technologies
PSP Element(s) G-554200-001
DOI 10.1186/s13059-019-1833-x
WOS ID WOS:000502825300001
Scopus ID 85074346124
PubMed ID 31665063
Erfassungsdatum 2019-11-06
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