Integrated transcriptomics and epigenomics reveal chamber-specific and species-specific characteristics of human and mouse hearts

PLoS Biol. 2021 May 18;19(5):e3001229. doi: 10.1371/journal.pbio.3001229. eCollection 2021 May.

Abstract

DNA methylation, chromatin accessibility, and gene expression represent different levels information in biological process, but a comprehensive multiomics analysis of the mammalian heart is lacking. Here, we applied nucleosome occupancy and methylome sequencing, which detected DNA methylation and chromatin accessibility simultaneously, as well as RNA-seq, for multiomics analysis of the 4 chambers of adult and fetal human hearts, and adult mouse hearts. Our results showed conserved region-specific patterns in the mammalian heart at transcriptome and DNA methylation level. Adult and fetal human hearts showed distinct features in DNA methylome, chromatin accessibility, and transcriptome. Novel long noncoding RNAs were identified in the human heart, and the gene expression profiles of major cardiovascular diseases associated genes were displayed. Furthermore, cross-species comparisons revealed human-specific and mouse-specific differentially expressed genes between the atria and ventricles. We also reported the relationship among multiomics and found there was a bell-shaped relationship between gene-body methylation and expression in the human heart. In general, our study provided comprehensive spatiotemporal and evolutionary insights into the regulation of gene expression in the heart.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chromatin / metabolism
  • CpG Islands / genetics
  • DNA / genetics
  • DNA Methylation / genetics
  • Epigenesis, Genetic / genetics
  • Epigenomics / methods
  • Gene Expression / genetics
  • Gene Expression Profiling / methods
  • Heart / growth & development*
  • Heart / physiology*
  • Heart Ventricles / growth & development
  • Heart Ventricles / metabolism
  • High-Throughput Nucleotide Sequencing / methods
  • Humans
  • Mice
  • Nucleosomes / metabolism
  • Organ Specificity / genetics
  • RNA, Long Noncoding / metabolism
  • Species Specificity
  • Transcriptome / genetics

Substances

  • Chromatin
  • Nucleosomes
  • RNA, Long Noncoding
  • DNA

Grants and funding

This work was supported by grants from the National Key R&D Program of China (2017YFA0103402 to L.W.), the CAMS Innovation Fund for Medical Sciences (CAMS-I2M, 2016-I2M-1-015 to J.W.), the National Natural Science Foundation of China (81870286 to L.S.) and the Beijing Municipal Natural Science Foundation (7181008 to L.S.). This work was also supported by the Beijing Advanced Innovation Center for Genomics at Peking University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.