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PLoS genetics2015; 11(8); e1005442; doi: 10.1371/journal.pgen.1005442

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

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.
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Publication Date: 2015-08-04 PubMed ID: 26241857PubMed Central: PMC4524645DOI: 10.1371/journal.pgen.1005442Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research looked into the evolution and early development of gene body DNA methylation patterns in the placentas of different mammals. The findings show that the majority of mammalian placentas, as well as the opossum extraembryonic membrane, have globally lower levels of methylation compared to somatic tissues. Higher methylation was found over the bodies of genes involved in certain cellular processes, and was associated with higher gene expression across all species examined.

Objective of Research

  • The research primarily aims to investigate the DNA methylation patterns and transcriptional regulatory programs across a range of mammalian placentas – including human, rhesus macaque, squirrel monkey, mouse, dog, horse, and cow – and in the opossum’s extraembryonic membrane.
  • The study also sought to identify the conservation of these methylation patterns from an evolutionary perspective.

Methylation Levels

  • The results revealed that, similar to humans, mammalian placentas and opossum extraembryonic membrane exhibit lower overall methylation levels compared to somatic (non-reproductive) tissues.
  • The research also found significant levels of methylation within the gene bodies, a conserved feature across all mammalian placentas examined, regardless of other differences in methylation patterns or level of absolute methylation.

Gene Body Methylation

  • The researchers observed higher levels of methylation over the bodies of specific genes. These genes were involved in key cellular processes such as mitosis (cell division), vesicle-mediated transport (transporting substances within a cell), protein phosphorylation (a process that activates or deactivates many protein enzymes), and chromatin modification (altering the structure of chromatin, which comprises cell’s genetic material).
  • In all mammals, the study found an association between higher methylation and increased gene expression (the process by which information from a gene is used to synthesize a functional gene product).

Comparison with Oocytes and Preimplantation Embryos

  • Moreover, DNA methylation analysis was conducted on oocytes and preimplantation embryos, revealing a conserved pattern of gene body methylation that is similar to that found in the placenta.
  • Intriguingly, although PMD/HMDs (partially methylated domains and highly methylated domains) were observed in mouse and cow oocytes as well as mouse early embryos, they were not observed in the placentas of these species.
  • The researchers suggest that PMD/HMDs might be a characteristic of early preimplantation methylation patterns, which become lost during placental development across some species and following the implantation of the embryo.

Cite This Article

APA
Schroeder DI, Jayashankar K, Douglas KC, Thirkill TL, York D, Dickinson PJ, Williams LE, Samollow PB, Ross PJ, Bannasch DL, Douglas GC, LaSalle JM. (2015). Early Developmental and Evolutionary Origins of Gene Body DNA Methylation Patterns in Mammalian Placentas. PLoS Genet, 11(8), e1005442. https://doi.org/10.1371/journal.pgen.1005442

Publication

PLoS genetics
ISSN: 1553-7404
NlmUniqueID: 101239074
Country: United States
Language: English
Volume: 11
Issue: 8
Pages: e1005442
PII: e1005442

Researcher Affiliations

Schroeder, Diane I
  • Department of Medical Microbiology and Immunology, The University of California Davis School of Medicine, Davis, California, United States of America; University of California Davis Genome Center, University of California Davis, Davis, California, United States of America; University of California Davis MIND Institute, University of California Davis, Sacramento, California, United States of America.
Jayashankar, Kartika
  • Department of Population Health and Reproduction, UC Davis School of Veterinary Medicine, Davis, California, United States of America.
Douglas, Kory C
  • Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas, United States of America.
Thirkill, Twanda L
  • Department of Cell Biology and Human Anatomy, University of California Davis School of Medicine, Davis, California, United States of America.
York, Daniel
  • Department of Surgical and Radiological Sciences, University of California School of Veterinary Medicine, Davis, California, United States of America.
Dickinson, Pete J
  • Department of Surgical and Radiological Sciences, University of California School of Veterinary Medicine, Davis, California, United States of America.
Williams, Lawrence E
  • Department of Veterinary Sciences, University of Texas MD Anderson Cancer Center, Bastrop, Texas, United States of America.
Samollow, Paul B
  • Department of Veterinary Integrative Biosciences, Texas A&M University, College Station, Texas, United States of America.
Ross, Pablo J
  • Department of Animal Science, University of California Davis, Davis, California, United States of America.
Bannasch, Danika L
  • Department of Population Health and Reproduction, UC Davis School of Veterinary Medicine, Davis, California, United States of America.
Douglas, Gordon C
  • Department of Cell Biology and Human Anatomy, University of California Davis School of Medicine, Davis, California, United States of America.
LaSalle, Janine M
  • Department of Medical Microbiology and Immunology, The University of California Davis School of Medicine, Davis, California, United States of America; University of California Davis Genome Center, University of California Davis, Davis, California, United States of America; University of California Davis MIND Institute, University of California Davis, Sacramento, California, United States of America.

MeSH Terms

  • Animals
  • Cattle
  • Cells, Cultured
  • DNA Methylation
  • Dogs
  • Epigenesis, Genetic
  • Evolution, Molecular
  • Female
  • Horses
  • Macaca mulatta
  • Mice
  • Oocytes / physiology
  • Open Reading Frames
  • Opossums
  • Placenta / physiology
  • Pregnancy
  • Saimiri
  • Species Specificity
  • Transcription, Genetic

Grant Funding

  • R01ES021707 / NIEHS NIH HHS
  • P01 ES011269 / NIEHS NIH HHS
  • P40 OD010938 / NIH HHS
  • R01 HD070044 / NICHD NIH HHS
  • S10RR029668 / NCRR NIH HHS
  • R01NS081913 / NINDS NIH HHS
  • S10RR027303 / NCRR NIH HHS
  • S10 RR029668 / NCRR NIH HHS
  • S10 RR027303 / NCRR NIH HHS
  • R24 RR014214 / NCRR NIH HHS
  • R01 ES021707 / NIEHS NIH HHS
  • 8P40OD010938 / NIH HHS
  • R01 NS081913 / NINDS NIH HHS

Conflict of Interest Statement

The authors have declared that no competing interests exist.

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