A complex association between DNA methylation and gene expression in human placenta at first and third trimesters

PLoS One. 2017 Jul 13;12(7):e0181155. doi: 10.1371/journal.pone.0181155. eCollection 2017.

Abstract

The human placenta is a maternal-fetal organ essential for normal fetal development and maternal health. During pregnancy, the placenta undergoes many structural and functional changes in response to fetal needs and environmental exposures. Previous studies have demonstrated widespread epigenetic and gene expression changes from early to late pregnancy. However, on the global level, how DNA methylation changes impact on gene expression in human placenta is not yet well understood. We performed DNA methylome analysis by reduced representation bisulfite sequencing (RRBS) and gene expression analysis by RNA-Seq for both first and third trimester human placenta tissues. From first to third trimester, 199 promoters (corresponding to 189 genes) and 2,297 gene bodies were differentially methylated, with a clear dominance of hypermethylation (96.8% and 93.0% for promoters and gene bodies, respectively). A total of 2,447 genes were differentially expressed, of which 77.2% were down-regulated. Gene ontology analysis using differentially expressed genes were enriched for cell cycle and immune response functions. The correlation between DNA methylation and gene expression was non-linear and complex, depending on the genomic context (promoter or gene body) and gene expression levels. A wide range of DNA methylation and gene expression changes were observed at different gestational ages. The non-linear association between DNA methylation and gene expression indicates that epigenetic regulation of placenta development is more complex than previously envisioned.

MeSH terms

  • CpG Islands
  • DNA Methylation*
  • Epigenesis, Genetic
  • Female
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation, Developmental
  • High-Throughput Nucleotide Sequencing / methods
  • Humans
  • Placenta / chemistry*
  • Pregnancy
  • Pregnancy Trimester, First / genetics*
  • Pregnancy Trimester, Third / genetics*
  • Promoter Regions, Genetic
  • Sequence Analysis, RNA / methods

Grants and funding

This work is supported by National Health and Family Planning Commission of Zhejiang Province (CD) and the Wenzhou Medical University Startup fund (CD and SJ). The funder provided support in the form of salaries for authors [JL, SJ, CD, YCL], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.