Epo reprograms the epigenome of erythroid cells

Exp Hematol. 2017 Jul:51:47-62. doi: 10.1016/j.exphem.2017.03.004. Epub 2017 Apr 12.

Abstract

The hormone erythropoietin (Epo) is required for erythropoiesis, yet its molecular mechanism of action remains poorly understood, particularly with respect to chromatin dynamics. To investigate how Epo modulates the erythroid epigenome, we performed epigenetic profiling using an ex vivo murine cell system that undergoes synchronous erythroid maturation in response to Epo stimulation. Our findings define the repertoire of Epo-modulated enhancers, illuminating a new facet of Epo signaling. First, a large number of enhancers rapidly responded to Epo stimulation, revealing a cis-regulatory network of Epo-responsive enhancers. In contrast, most of the other identified enhancers remained in an active acetylated state during Epo signaling, suggesting that most erythroid enhancers are established at an earlier precursor stage. Second, we identified several hundred super-enhancers that were linked to key erythroid genes, such as Tal1, Bcl11a, and Mir144/451. Third, experimental and computational validation revealed that many predicted enhancer regions were occupied by TAL1 and enriched with DNA-binding motifs for GATA1, KLF1, TAL1/E-box, and STAT5. Additionally, many of these cis-regulatory regions were conserved evolutionarily and displayed correlated enhancer:promoter acetylation. Together, these findings define a cis-regulatory enhancer network for Epo signaling during erythropoiesis, and provide the framework for future studies involving the interplay of epigenetics and Epo signaling.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / biosynthesis
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Carrier Proteins / biosynthesis
  • Carrier Proteins / genetics
  • Cellular Reprogramming / physiology*
  • DNA-Binding Proteins
  • Epigenesis, Genetic / physiology*
  • Epigenomics
  • Erythroid Cells / cytology
  • Erythroid Cells / metabolism*
  • Erythropoiesis / physiology*
  • Erythropoietin / genetics
  • Erythropoietin / metabolism*
  • Female
  • GATA1 Transcription Factor / biosynthesis
  • GATA1 Transcription Factor / genetics
  • Kruppel-Like Transcription Factors / biosynthesis
  • Kruppel-Like Transcription Factors / genetics
  • Mice
  • Mice, Inbred BALB C
  • MicroRNAs / biosynthesis
  • MicroRNAs / genetics
  • Nuclear Proteins / biosynthesis
  • Nuclear Proteins / genetics
  • Proto-Oncogene Proteins / biosynthesis
  • Proto-Oncogene Proteins / genetics
  • Repressor Proteins
  • STAT5 Transcription Factor / biosynthesis
  • STAT5 Transcription Factor / genetics
  • Signal Transduction / physiology*
  • T-Cell Acute Lymphocytic Leukemia Protein 1

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Bcl11a protein, mouse
  • Carrier Proteins
  • DNA-Binding Proteins
  • GATA1 Transcription Factor
  • Gata1 protein, mouse
  • Kruppel-Like Transcription Factors
  • MIRN144 microRNA, mouse
  • MicroRNAs
  • Mirn451 microRNA, mouse
  • Nuclear Proteins
  • Proto-Oncogene Proteins
  • Repressor Proteins
  • STAT5 Transcription Factor
  • T-Cell Acute Lymphocytic Leukemia Protein 1
  • Tal1 protein, mouse
  • erythroid Kruppel-like factor
  • Erythropoietin