Cell cycle-dependent regulation of Greatwall kinase by protein phosphatase 1 and regulatory subunit 3B

J Biol Chem. 2017 Jun 16;292(24):10026-10034. doi: 10.1074/jbc.M117.778233. Epub 2017 Apr 26.

Abstract

Greatwall (Gwl) kinase plays an essential role in the regulation of mitotic entry and progression. Mitotic activation of Gwl requires both cyclin-dependent kinase 1 (CDK1)-dependent phosphorylation and its autophosphorylation at an evolutionarily conserved serine residue near the carboxyl terminus (Ser-883 in Xenopus). In this study we show that Gwl associates with protein phosphatase 1 (PP1), particularly PP1γ, which mediates the dephosphorylation of Gwl Ser-883. Consistent with the mitotic activation of Gwl, its association with PP1 is disrupted in mitotic cells and egg extracts. During mitotic exit, PP1-dependent dephosphorylation of Gwl Ser-883 occurs prior to dephosphorylation of other mitotic substrates; replacing endogenous Gwl with a phosphomimetic S883E mutant blocks mitotic exit. Moreover, we identified PP1 regulatory subunit 3B (PPP1R3B) as a targeting subunit that can direct PP1 activity toward Gwl. PPP1R3B bridges PP1 and Gwl association and promotes Gwl Ser-883 dephosphorylation. Consistent with the cell cycle-dependent association of Gwl and PP1, Gwl and PPP1R3B dissociate in M phase. Interestingly, up-regulation of PPP1R3B facilitates mitotic exit and blocks mitotic entry. Thus, our study suggests PPP1R3B as a new cell cycle regulator that functions by governing Gwl dephosphorylation.

Keywords: Xenopus; cell cycle; mitosis; phosphatase; phosphoprotein phosphatase 1 (PP1).

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Cell Cycle*
  • Cell Division
  • Cyclin-Dependent Kinases / metabolism
  • Enzyme Activation
  • HeLa Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / chemistry
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Mitosis
  • Mutation
  • Oocytes / cytology
  • Oocytes / enzymology
  • Oocytes / metabolism*
  • Phosphorylation
  • Protein Phosphatase 1 / chemistry
  • Protein Phosphatase 1 / genetics
  • Protein Phosphatase 1 / metabolism*
  • Protein Processing, Post-Translational*
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Subunits / chemistry
  • Protein Subunits / genetics
  • Protein Subunits / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / metabolism
  • Repressor Proteins / chemistry
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Serine / metabolism
  • Xenopus Proteins / chemistry
  • Xenopus Proteins / genetics
  • Xenopus Proteins / metabolism*
  • Xenopus laevis

Substances

  • Intracellular Signaling Peptides and Proteins
  • Protein Subunits
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Repressor Proteins
  • Xenopus Proteins
  • Serine
  • MASTL protein, Xenopus
  • Protein Serine-Threonine Kinases
  • Cyclin-Dependent Kinases
  • Protein Phosphatase 1