Transient Hysteresis in CDK4/6 Activity Underlies Passage of the Restriction Point in G1

Mol Cell. 2019 Nov 21;76(4):562-573.e4. doi: 10.1016/j.molcel.2019.08.020. Epub 2019 Sep 19.

Abstract

Cells escape the need for mitogens at a restriction point several hours before entering S phase. The restriction point has been proposed to result from CDK4/6 initiating partial Rb phosphorylation to trigger a bistable switch whereby cyclin E-CDK2 and Rb mutually reinforce each other to induce Rb hyperphosphorylation. Here, using single-cell analysis, we unexpectedly found that cyclin E/A-CDK activity can only maintain Rb hyperphosphorylation starting at the onset of S phase and that CDK4/6 activity, but not cyclin E/A-CDK activity, is required to hyperphosphorylate Rb throughout G1 phase. Mitogen removal in G1 results in a gradual loss of CDK4/6 activity with a high likelihood of cells sustaining Rb hyperphosphorylation until S phase, at which point cyclin E/A-CDK activity takes over. Thus, it is short-term memory, or transient hysteresis, in CDK4/6 activity following mitogen removal that sustains Rb hyperphosphorylation, demonstrating a probabilistic rather than an irreversible molecular mechanism underlying the restriction point.

Keywords: CDK; E2F; bistability; cell cycle; cyclin; hysteresis; restriction point; retinoblastoma.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cell Proliferation*
  • Cyclin-Dependent Kinase 4 / metabolism*
  • Cyclin-Dependent Kinase 6 / metabolism*
  • Dose-Response Relationship, Drug
  • Epithelial Cells / drug effects*
  • Epithelial Cells / enzymology
  • Fibroblasts / drug effects
  • Fibroblasts / enzymology
  • G1 Phase Cell Cycle Checkpoints*
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / enzymology
  • Humans
  • Mice
  • Mitogens / pharmacology*
  • Models, Biological
  • Phosphorylation
  • Retinoblastoma Binding Proteins / metabolism
  • Signal Transduction
  • Time Factors
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Mitogens
  • RB1 protein, human
  • Retinoblastoma Binding Proteins
  • Ubiquitin-Protein Ligases
  • CDK4 protein, human
  • CDK6 protein, human
  • Cyclin-Dependent Kinase 4
  • Cyclin-Dependent Kinase 6