Wild-type p53-induced phosphatase 1 (Wip1) forestalls cellular premature senescence at physiological oxygen levels by regulating DNA damage response signaling during DNA replication

Cell Cycle. 2014;13(6):1015-29. doi: 10.4161/cc.27920. Epub 2014 Jan 31.

Abstract

Wip1 (protein phosphatase Mg(2+)/Mn(2+)-dependent 1D, Ppm1d) is a nuclear serine/threonine protein phosphatase that is induced by p53 following the activation of DNA damage response (DDR) signaling. Ppm1d(-/-) mouse embryonic fibroblasts (MEFs) exhibit premature senescence under conventional culture conditions; however, little is known regarding the role of Wip1 in regulating cellular senescence. In this study, we found that even at a representative physiological concentration of 3% O2, Ppm1d(-/-) MEFs underwent premature cellular senescence that depended on the functional activation of p53. Interestingly, Ppm1d(-/-) MEFs showed increased H2AX phosphorylation levels without increased levels of reactive oxygen species (ROS) or DNA base damage compared with wild-type (Wt) MEFs, suggesting a decreased threshold for DDR activation or sustained DDR activation during recovery. Notably, the increased H2AX phosphorylation levels observed in Ppm1d(-/-) MEFs were primarily associated with S-phase cells and predominantly dependent on the activation of ATM. Moreover, these same phenotypes were observed when Wt and Ppm1d(-/-) MEFs were either transiently or chronically exposed to low levels of agents that induce replication-mediated double-stranded breaks. These findings suggest that Wip1 prevents the induction of cellular senescence at physiological oxygen levels by attenuating DDR signaling in response to endogenous double-stranded breaks that form during DNA replication.

Keywords: ATM; DNA damage response; Wip1; camptothecin; cellular senescence; p53.

Publication types

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

MeSH terms

  • Aging, Premature / genetics
  • Aging, Premature / metabolism*
  • Animals
  • Cells, Cultured
  • DNA Damage / physiology*
  • DNA Replication / physiology*
  • Histones / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Oxygen / metabolism*
  • Phosphoprotein Phosphatases / metabolism*
  • Phosphorylation
  • Protein Phosphatase 2C
  • Reactive Oxygen Species / metabolism
  • S Phase / physiology
  • Signal Transduction
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • Histones
  • Reactive Oxygen Species
  • Tumor Suppressor Protein p53
  • Phosphoprotein Phosphatases
  • Ppm1d protein, mouse
  • Protein Phosphatase 2C
  • Oxygen