Chemical genomics reveals histone deacetylases are required for core regulatory transcription

Nat Commun. 2019 Jul 8;10(1):3004. doi: 10.1038/s41467-019-11046-7.

Abstract

Identity determining transcription factors (TFs), or core regulatory (CR) TFs, are governed by cell-type specific super enhancers (SEs). Drugs to selectively inhibit CR circuitry are of high interest for cancer treatment. In alveolar rhabdomyosarcoma, PAX3-FOXO1 activates SEs to induce the expression of other CR TFs, providing a model system for studying cancer cell addiction to CR transcription. Using chemical genetics, the systematic screening of chemical matter for a biological outcome, here we report on a screen for epigenetic chemical probes able to distinguish between SE-driven transcription and constitutive transcription. We find that chemical probes along the acetylation-axis, and not the methylation-axis, selectively disrupt CR transcription. Additionally, we find that histone deacetylases (HDACs) are essential for CR TF transcription. We further dissect the contribution of HDAC isoforms using selective inhibitors, including the newly developed selective HDAC3 inhibitor LW3. We show HDAC1/2/3 are the co-essential isoforms that when co-inhibited halt CR transcription, making CR TF sites hyper-accessible and disrupting chromatin looping.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation / drug effects
  • Cell Line, Tumor
  • Chromatin / drug effects
  • Chromatin / metabolism
  • Enhancer Elements, Genetic / drug effects*
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Genomics / methods
  • High-Throughput Nucleotide Sequencing
  • High-Throughput Screening Assays
  • Histone Deacetylase Inhibitors / chemistry
  • Histone Deacetylase Inhibitors / pharmacology*
  • Histone Deacetylases / chemistry
  • Histone Deacetylases / metabolism*
  • Humans
  • Molecular Dynamics Simulation
  • Molecular Probes / chemistry
  • Molecular Probes / pharmacology
  • Oncogene Proteins, Fusion / genetics
  • Paired Box Transcription Factors / genetics
  • Primary Cell Culture
  • Protein Isoforms / antagonists & inhibitors
  • Protein Isoforms / chemistry
  • Protein Isoforms / metabolism
  • Rhabdomyosarcoma / genetics*
  • Rhabdomyosarcoma / pathology
  • Sequence Analysis, RNA
  • Transcription, Genetic / drug effects

Substances

  • Chromatin
  • Histone Deacetylase Inhibitors
  • Molecular Probes
  • Oncogene Proteins, Fusion
  • PAX3-FOXO1A fusion protein, human
  • Paired Box Transcription Factors
  • Protein Isoforms
  • Histone Deacetylases