PCNA-Mediated Degradation of p21 Coordinates the DNA Damage Response and Cell Cycle Regulation in Individual Cells

Cell Rep. 2019 Apr 2;27(1):48-58.e7. doi: 10.1016/j.celrep.2019.03.031.

Abstract

To enable reliable cell fate decisions, mammalian cells need to adjust their responses to dynamically changing internal states by rewiring the corresponding signaling networks. Here, we combine time-lapse microscopy of endogenous fluorescent reporters with computational analysis to understand at the single-cell level how the p53-mediated DNA damage response is adjusted during cell cycle progression. Shape-based clustering revealed that the dynamics of the CDK inhibitor p21 diverges from the dynamics of its transcription factor p53 during S phase. Using mathematical modeling, we predict and experimentally validate that S phase-specific degradation of p21 by PCNA-CRL4cdt2 is sufficient to explain these heterogeneous responses. This highlights how signaling pathways and cell regulatory networks intertwine to adjust the cellular response to the individual needs of a given cell.

Keywords: PCNA; cell cycle regulation; cellular heterogeneity; genome engineering; mathematical modeling; p21; p53 signaling; shape-based clustering; single-cell analysis; time-lapse microscopy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Cell Cycle / physiology*
  • Cell Cycle Checkpoints / physiology
  • Cells, Cultured
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism*
  • DNA Damage / physiology*
  • DNA Repair / physiology
  • Female
  • HEK293 Cells
  • Humans
  • MCF-7 Cells
  • Proliferating Cell Nuclear Antigen / genetics
  • Proliferating Cell Nuclear Antigen / physiology*
  • Proteolysis*
  • Signal Transduction / genetics
  • Tumor Suppressor Protein p53 / metabolism
  • Tumor Suppressor Protein p53 / physiology

Substances

  • Cyclin-Dependent Kinase Inhibitor p21
  • Proliferating Cell Nuclear Antigen
  • TP53 protein, human
  • Tumor Suppressor Protein p53