Enhancer switching in cell lineage priming is linked to eRNA, Brg1's AT-hook, and SWI/SNF recruitment

Mol Cell. 2024 May 16;84(10):1855-1869.e5. doi: 10.1016/j.molcel.2024.03.013. Epub 2024 Apr 8.

Abstract

RNA transcribed from enhancers, i.e., eRNA, has been suggested to directly activate transcription by recruiting transcription factors and co-activators. Although there have been specific examples of eRNA functioning in this way, it is not clear how general this may be. We find that the AT-hook of SWI/SNF preferentially binds RNA and, as part of the esBAF complex, associates with eRNA transcribed from intronic and intergenic regions. Our data suggest that SWI/SNF is globally recruited in cis by eRNA to cell-type-specific enhancers, representative of two distinct stages that mimic early mammalian development, and not at enhancers that are shared between the two stages. In this manner, SWI/SNF facilitates recruitment and/or activation of MLL3/4, p300/CBP, and Mediator to stage-specific enhancers and super-enhancers that regulate the transcription of metabolic and cell lineage priming-related genes. These findings highlight a connection between ATP-dependent chromatin remodeling and eRNA in cell identity and typical- and super-enhancer activation.

Keywords: Brg1/Smarca4; EpiSCs; MLL3/4; RNAPII; SWI/SNF; eRNA; enhancer; mediator (Med1); naive; p300/CBP; primed.

MeSH terms

  • Animals
  • Cell Lineage* / genetics
  • Chromatin Assembly and Disassembly
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • DNA Helicases* / genetics
  • DNA Helicases* / metabolism
  • Enhancer Elements, Genetic*
  • Humans
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • Transcription Factors* / genetics
  • Transcription Factors* / metabolism

Substances

  • Chromosomal Proteins, Non-Histone
  • DNA Helicases
  • Nuclear Proteins
  • SMARCA4 protein, human
  • Smarca4 protein, mouse
  • SWI-SNF-B chromatin-remodeling complex
  • Transcription Factors