Dephosphorylation of p53 Ser 392 Enhances Trimethylation of Histone H3 Lys 9 via SUV39h1 Stabilization in CK2 Downregulation-Mediated Senescence

Mol Cells. 2019 Nov 30;42(11):773-782. doi: 10.14348/molcells.2019.0018.

Abstract

Cellular senescence is an irreversible form of cell cycle arrest. Senescent cells have a unique gene expression profile that is frequently accompanied by senescence-associated heterochromatic foci (SAHFs). Protein kinase CK2 (CK2) downregulation can induce trimethylation of histone H3 Lys 9 (H3K9me3) and SAHFs formation by activating SUV39h1. Here, we present evidence that the PI3K-AKTmTOR-reactive oxygen species-p53 pathway is necessary for CK2 downregulation-mediated H3K9me3 and SAHFs formation. CK2 downregulation promotes SUV39h1 stability by inhibiting its proteasomal degradation in a p53dependent manner. Moreover, the dephosphorylation status of Ser 392 on p53, a possible CK2 target site, enhances the nuclear import and subsequent stabilization of SUV39h1 by inhibiting the interactions between p53, MDM2, and SUV39h1. Furthermore, p21Cip1/WAF1 is required for CK2 downregulation-mediated H3K9me3, and dephosphorylation of Ser 392 on p53 is important for efficient transcription of p21Cip1/WAF1. Taken together, these results suggest that CK2 downregulation induces dephosphorylation of Ser 392 on p53, which subsequently increases the stability of SUV39h1 and the expression of p21Cip1/WAF1, leading to H3K9me3 and SAHFs formation.

Keywords: CK2; H3K9me3; SAHFs; SUV39h1; p53.

MeSH terms

  • Casein Kinase II / genetics
  • Casein Kinase II / metabolism*
  • Cell Line, Tumor
  • Cellular Senescence*
  • Cyclin-Dependent Kinase Inhibitor p21 / genetics
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism
  • Down-Regulation
  • HCT116 Cells
  • Heterochromatin / genetics
  • Histones / metabolism*
  • Humans
  • Lysine / metabolism
  • MCF-7 Cells
  • Methylation
  • Methyltransferases / metabolism*
  • Phosphorylation
  • Protein Stability
  • RNA Interference
  • Repressor Proteins / metabolism*
  • Serine / metabolism
  • Signal Transduction / genetics
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • CDKN1A protein, human
  • Cyclin-Dependent Kinase Inhibitor p21
  • Heterochromatin
  • Histones
  • Repressor Proteins
  • Tumor Suppressor Protein p53
  • Serine
  • SUV39H1 protein, human
  • Methyltransferases
  • Casein Kinase II
  • Lysine