Regulatory signatures of liver regeneration distilled by integrative analysis of mRNA, histone methylation, and proteomics

J Biol Chem. 2017 May 12;292(19):8019-8037. doi: 10.1074/jbc.M116.774547. Epub 2017 Mar 16.

Abstract

The capacity of the liver to regenerate is likely to be encoded as a plasticity of molecular networks within the liver. By applying a combination of comprehensive analyses of the epigenome, transcriptome, and proteome, we herein depict the molecular landscape of liver regeneration. We demonstrated that histone H3 Lys-4 was trimethylated at the promoter regions of many loci, among which only a fraction, including cell-cycle-related genes, were transcriptionally up-regulated. A cistrome analysis guided by the histone methylation patterns and the transcriptome identified FOXM1 as the key transcription factor promoting liver regeneration, which was confirmed in vitro using a hepatocarcinoma cell line. The promoter regions of cell-cycle-related genes and Foxm1 acquired higher levels of trimethylated histone H3 Lys-4, suggesting that epigenetic regulations of these key regulatory genes define quiescence and regeneration of the liver cells. A quantitative proteome analysis of the regenerating liver revealed that conditional protein degradation also mediated regeneration-specific protein expression. These sets of informational resources should be useful for further investigations of liver regeneration.

Keywords: functional genomics; histone methylation; proteomics; regeneration; transcriptomics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Animals
  • Carcinoma, Hepatocellular / metabolism
  • Cell Line, Tumor
  • Cell Proliferation
  • Epigenesis, Genetic
  • Forkhead Box Protein M1 / metabolism
  • Gene Expression Regulation*
  • Histones / chemistry*
  • Liver / metabolism*
  • Liver Neoplasms / metabolism
  • Liver Regeneration*
  • Lysine / chemistry
  • Male
  • Methylation
  • Mice
  • Mice, Inbred C57BL
  • Promoter Regions, Genetic
  • Proteome / metabolism
  • RNA, Messenger / metabolism*
  • Transcriptome

Substances

  • Forkhead Box Protein M1
  • Foxm1 protein, mouse
  • Histones
  • Proteome
  • RNA, Messenger
  • Lysine