Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas

Diane I. Schroeder, Kartika Jayashankar, Kory C. Douglas, Twanda L. Thirkill, Daniel York, Peter J Dickinson, Lawrence E. Williams, Paul B. Samollow, Pablo J. Ross, Danika L Bannasch, Gordon C Douglas, Janine M LaSalle

Research output: Contribution to journalArticle

36 Citations (Scopus)

Abstract

Over the last 20-80 million years the mammalian placenta has taken on a variety of morphologies through both divergent and convergent evolution. Recently we have shown that the human placenta genome has a unique epigenetic pattern of large partially methylated domains (PMDs) and highly methylated domains (HMDs) with gene body DNA methylation positively correlating with level of gene expression. In order to determine the evolutionary conservation of DNA methylation patterns and transcriptional regulatory programs in the placenta, we performed a genome-wide methylome (MethylC-seq) analysis of human, rhesus macaque, squirrel monkey, mouse, dog, horse, and cow placentas as well as opossum extraembryonic membrane. We found that, similar to human placenta, mammalian placentas and opossum extraembryonic membrane have globally lower levels of methylation compared to somatic tissues. Higher relative gene body methylation was the conserved feature across all mammalian placentas, despite differences in PMD/HMDs and absolute methylation levels. Specifically, higher methylation over the bodies of genes involved in mitosis, vesicle-mediated transport, protein phosphorylation, and chromatin modification was observed compared with the rest of the genome. As in human placenta, higher methylation is associated with higher gene expression and is predictive of genic location across species. Analysis of DNA methylation in oocytes and preimplantation embryos shows a conserved pattern of gene body methylation similar to the placenta. Intriguingly, mouse and cow oocytes and mouse early embryos have PMD/HMDs but their placentas do not, suggesting that PMD/HMDs are a feature of early preimplantation methylation patterns that become lost during placental development in some species and following implantation of the embryo.

Original languageEnglish (US)
Article numbere1005442
JournalPLoS Genetics
Volume11
Issue number8
DOIs
StatePublished - Aug 1 2015

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methylation
DNA methylation
DNA Methylation
placenta
Placenta
DNA
Methylation
gene
Genes
genes
Opossums
Extraembryonic Membranes
extraembryonic membranes
embryo
genome
opossums
gene expression
Oocytes
mice
embryo (animal)

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas. / Schroeder, Diane I.; Jayashankar, Kartika; Douglas, Kory C.; Thirkill, Twanda L.; York, Daniel; Dickinson, Peter J; Williams, Lawrence E.; Samollow, Paul B.; Ross, Pablo J.; Bannasch, Danika L; Douglas, Gordon C; LaSalle, Janine M.

In: PLoS Genetics, Vol. 11, No. 8, e1005442, 01.08.2015.

Research output: Contribution to journalArticle

Schroeder, Diane I. ; Jayashankar, Kartika ; Douglas, Kory C. ; Thirkill, Twanda L. ; York, Daniel ; Dickinson, Peter J ; Williams, Lawrence E. ; Samollow, Paul B. ; Ross, Pablo J. ; Bannasch, Danika L ; Douglas, Gordon C ; LaSalle, Janine M. / Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas. In: PLoS Genetics. 2015 ; Vol. 11, No. 8.
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