4D Genome Rewiring during Oncogene-Induced and Replicative Senescence

Mol Cell. 2020 May 7;78(3):522-538.e9. doi: 10.1016/j.molcel.2020.03.007. Epub 2020 Mar 26.

Abstract

To understand the role of the extensive senescence-associated 3D genome reorganization, we generated genome-wide chromatin interaction maps, epigenome, replication-timing, whole-genome bisulfite sequencing, and gene expression profiles from cells entering replicative senescence (RS) or upon oncogene-induced senescence (OIS). We identify senescence-associated heterochromatin domains (SAHDs). Differential intra- versus inter-SAHD interactions lead to the formation of senescence-associated heterochromatin foci (SAHFs) in OIS but not in RS. This OIS-specific configuration brings active genes located in genomic regions adjacent to SAHDs in close spatial proximity and favors their expression. We also identify DNMT1 as a factor that induces SAHFs by promoting HMGA2 expression. Upon DNMT1 depletion, OIS cells transition to a 3D genome conformation akin to that of cells in replicative senescence. These data show how multi-omics and imaging can identify critical features of RS and OIS and discover determinants of acute senescence and SAHF formation.

Keywords: 3D genome architecture; DNMT1; Hi-C; chromatin compartments; gene regulation; oncogene-induced senescence; replicative senescence; senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cells, Cultured
  • Cellular Senescence / genetics*
  • Chromatin Assembly and Disassembly / genetics
  • DNA (Cytosine-5-)-Methyltransferase 1 / genetics*
  • DNA (Cytosine-5-)-Methyltransferase 1 / metabolism
  • DNA Methylation
  • Fibroblasts
  • Genome, Human*
  • Heterochromatin / genetics
  • Humans
  • In Situ Hybridization, Fluorescence
  • Oncogenes*

Substances

  • Heterochromatin
  • DNA (Cytosine-5-)-Methyltransferase 1
  • DNMT1 protein, human