Targeted epigenetic modulation using a DNA-based histone deacetylase inhibitor enhances cardiomyogenesis in mouse embryonic stem cells

J Cell Physiol. 2021 May;236(5):3946-3962. doi: 10.1002/jcp.30140. Epub 2020 Nov 8.

Abstract

The epigenome has an essential role in orchestrating transcriptional activation and modulating key developmental processes. Previously, we developed a library of pyrrole-imidazole polyamides (PIPs) conjugated with suberoylanilide hydroxamic acid (SAHA), a histone deacetylase (HDAC) inhibitor, for the purpose of sequence-specific modification of epigenetics. Based on the gene expression profile of SAHA-PIPs and screening studies using the α-myosin heavy chain promoter-driven reporter and SAHA-PIP library, we identified that SAHA-PIP G activates cardiac-related genes. Studies in mouse ES cells showed that SAHA-PIP G could enhance the generation of spontaneous beating cells, which is consistent with upregulation of several cardiac-related genes. Moreover, ChIP-seq results confirmed that the upregulation of cardiac-related genes is highly correlated with epigenetic activation, relevant to the sequence-specific binding of SAHA-PIP G. This proof-of-concept study demonstrating the applicability of SAHA-PIP not only improves our understanding of epigenetic alterations involved in cardiomyogenesis but also provides a novel chemical-based strategy for stem cell differentiation.

Keywords: cardiomyogenesis; embryonic stem cells; epigenetic switches; histone deacetylase inhibitor; pyrrole-imidazole polyamide.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Cell Differentiation / drug effects
  • DNA / metabolism*
  • Embryoid Bodies / drug effects
  • Embryoid Bodies / metabolism
  • Endoderm / metabolism
  • Epigenesis, Genetic* / drug effects
  • HEK293 Cells
  • Histone Deacetylase Inhibitors / pharmacology*
  • Humans
  • Imidazoles / pharmacology
  • Mesoderm / metabolism
  • Mice
  • Models, Biological
  • Mouse Embryonic Stem Cells / cytology*
  • Mouse Embryonic Stem Cells / drug effects
  • Mouse Embryonic Stem Cells / metabolism
  • Myocytes, Cardiac / cytology*
  • Myocytes, Cardiac / drug effects
  • Myocytes, Cardiac / metabolism
  • Nucleotide Motifs / genetics
  • Nylons / pharmacology
  • Organogenesis*
  • Pyrroles / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcription, Genetic / drug effects

Substances

  • Biomarkers
  • Histone Deacetylase Inhibitors
  • Imidazoles
  • Nylons
  • Pyrroles
  • RNA, Messenger
  • imidazole
  • DNA