KrasG12D induces changes in chromatin territories that differentially impact early nuclear reprogramming in pancreatic cells

Genome Biol. 2021 Oct 14;22(1):289. doi: 10.1186/s13059-021-02498-6.

Abstract

Background: Pancreatic ductal adenocarcinoma initiation is most frequently caused by Kras mutations.

Results: Here, we apply biological, biochemical, and network biology methods to validate GEMM-derived cell models using inducible KrasG12D expression. We describe the time-dependent, chromatin remodeling program that impacts function during early oncogenic signaling. We find that the KrasG12D-induced transcriptional response is dominated by downregulated expression concordant with layers of epigenetic events. More open chromatin characterizes the ATAC-seq profile associated with a smaller group of upregulated genes and epigenetic marks. RRBS demonstrates that promoter hypermethylation does not account for the silencing of the extensive gene promoter network. Moreover, ChIP-Seq reveals that heterochromatin reorganization plays little role in this early transcriptional program. Notably, both gene activation and silencing primarily depend on the marking of genes with a combination of H3K27ac, H3K4me3, and H3K36me3. Indeed, integrated modeling of all these datasets shows that KrasG12D regulates its transcriptional program primarily through unique super-enhancers and enhancers, and marking specific gene promoters and bodies. We also report chromatin remodeling across genomic areas that, although not contributing directly to cis-gene transcription, are likely important for KrasG12D functions.

Conclusions: In summary, we report a comprehensive, time-dependent, and coordinated early epigenomic program for KrasG12D in pancreatic cells, which is mechanistically relevant to understanding chromatin remodeling events underlying transcriptional outcomes needed for the function of this oncogene.

Keywords: Epigenomics; KRAS; Pancreatic cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Line
  • Cell Nucleus / genetics
  • Cellular Reprogramming / genetics*
  • Chromatin / metabolism*
  • DNA Methylation
  • Epigenesis, Genetic*
  • Genes, ras*
  • Genome
  • Histone Code
  • Mice
  • Mice, Transgenic
  • Pancreatic Neoplasms / genetics*
  • Promoter Regions, Genetic
  • Repetitive Sequences, Nucleic Acid
  • Transcription, Genetic

Substances

  • Chromatin