Super-enhancer RNA m6A promotes local chromatin accessibility and oncogene transcription in pancreatic ductal adenocarcinoma

Nat Genet. 2023 Dec;55(12):2224-2234. doi: 10.1038/s41588-023-01568-8. Epub 2023 Nov 13.

Abstract

The biological functions of noncoding RNA N6-methyladenosine (m6A) modification remain poorly understood. In the present study, we depict the landscape of super-enhancer RNA (seRNA) m6A modification in pancreatic ductal adenocarcinoma (PDAC) and reveal a regulatory axis of m6A seRNA, H3K4me3 modification, chromatin accessibility and oncogene transcription. We demonstrate the cofilin family protein CFL1, overexpressed in PDAC, as a METTL3 cofactor that helps seRNA m6A methylation formation. The increased seRNA m6As are recognized by the reader YTHDC2, which recruits H3K4 methyltransferase MLL1 to promote H3K4me3 modification cotranscriptionally. Super-enhancers with a high level of H3K4me3 augment chromatin accessibility and facilitate oncogene transcription. Collectively, these results shed light on a CFL1-METTL3-seRNA m6A-YTHDC2/MLL1 axis that plays a role in the epigenetic regulation of local chromatin state and gene expression, which strengthens our knowledge about the functions of super-enhancers and their transcripts.

MeSH terms

  • Carcinoma, Pancreatic Ductal* / genetics
  • Chromatin / genetics
  • Epigenesis, Genetic
  • Humans
  • Methyltransferases / genetics
  • Oncogenes / genetics
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism
  • RNA

Substances

  • Chromatin
  • RNA
  • METTL3 protein, human
  • Methyltransferases