Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression and senescence in primary cells

J Biol Chem. 2011 Sep 23;286(38):33061-9. doi: 10.1074/jbc.M111.257667. Epub 2011 Jul 11.

Abstract

Sustained expression of the histone demethylase, KDM2B (Ndy1/FBXL10/JHDM1B), bypasses cellular senescence in primary mouse embryonic fibroblasts (MEFs). Here, we show that KDM2B is a conserved regulator of lifespan in multiple primary cell types and defines a program in which this chromatin-modifying enzyme counteracts the senescence-associated down-regulation of the EZH2 histone methyltransferase. Senescence in MEFs epigenetically silences KDM2B and induces the tumor suppressor miRNAs let-7b and miR-101, which target EZH2. Forced expression of KDM2B promotes immortalization by silencing these miRNAs through locus-specific histone H3 K36me2 demethylation, leading to EZH2 up-regulation. Overexpression of let-7b down-regulates EZH2, induces premature senescence, and counteracts immortalization of MEFs driven by KDM2B. The KDM2B-let-7-EZH2 pathway also contributes to the proliferation of immortal Ink4a/Arf null fibroblasts suggesting that, beyond its anti-senescence role in primary cells, this histone-modifying enzyme functions more broadly in the regulation of cellular proliferation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-Ribosylation Factors / metabolism
  • Animals
  • Cell Cycle*
  • Cell Proliferation
  • Cells, Cultured
  • Cellular Senescence*
  • Conserved Sequence / genetics
  • Cyclin-Dependent Kinase Inhibitor p16 / deficiency
  • Cyclin-Dependent Kinase Inhibitor p16 / metabolism
  • Enhancer of Zeste Homolog 2 Protein
  • Epigenesis, Genetic
  • F-Box Proteins / metabolism*
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • Histone-Lysine N-Methyltransferase / metabolism*
  • Jumonji Domain-Containing Histone Demethylases / metabolism*
  • Lysine / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / metabolism*
  • Polycomb Repressive Complex 2
  • Signal Transduction*
  • Substrate Specificity
  • Up-Regulation / genetics

Substances

  • Cyclin-Dependent Kinase Inhibitor p16
  • F-Box Proteins
  • MicroRNAs
  • mirnlet7 microRNA, mouse
  • Jumonji Domain-Containing Histone Demethylases
  • Kdm2b protein, mouse
  • Enhancer of Zeste Homolog 2 Protein
  • Ezh2 protein, mouse
  • Histone-Lysine N-Methyltransferase
  • Polycomb Repressive Complex 2
  • ADP-Ribosylation Factors
  • Lysine