A Cds1-mediated checkpoint protects the MBF activator Rep2 from ubiquitination by anaphase-promoting complex/cyclosome-Ste9 at S-phase arrest in fission yeast

Mol Cell Biol. 2009 Sep;29(18):4959-70. doi: 10.1128/MCB.00562-09. Epub 2009 Jul 13.

Abstract

Transcription of the MluI cell cycle box (MCB) motif-containing genes at G(1) phase is regulated by the MCB-binding factors (MBF) (also called DSC1) in Schizosaccharomyces pombe. Upon S-phase arrest, the MBF transcriptional activity is induced through the accumulation of the MBF activator Rep2. In this study, we show that the turnover of Rep2 is attributable to ubiquitin-mediated proteolysis. Levels of Rep2 oscillate during the cell cycle, with a peak at G(1) phase, coincident with the MBF activity. Furthermore, we show that Rep2 ubiquitination requires the function of the E3 ligase anaphase-promoting complex/cyclosome (APC/C). Ste9 can be phosphorylated by the checkpoint kinase Cds1 in vitro, and its inhibition/phosphorylation at S-phase arrest is dependent on the function of Cds1. Our data indicate that the Cds1-dependent stabilization of Rep2 is achieved through the inhibition/phosphorylation of APC/C-Ste9 at the onset of S-phase arrest. Stabilization of Rep2 is important for stimulating transcription of the MBF-dependent genes to ensure a sufficient supply of proteins essential for cell recovery from S-phase arrest. We propose that oscillation of Rep2 plays a role in regulation of periodic transcription of the MBF-dependent genes during cell cycle progression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Anaphase-Promoting Complex-Cyclosome
  • Cell Cycle Proteins / metabolism*
  • Checkpoint Kinase 2
  • DNA-Binding Proteins / metabolism
  • G1 Phase / drug effects
  • Hydroxyurea / pharmacology
  • Mutation / genetics
  • Phosphorylation / drug effects
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Binding / drug effects
  • Protein Processing, Post-Translational / drug effects
  • Protein Serine-Threonine Kinases / metabolism*
  • Protein Stability / drug effects
  • S Phase* / drug effects
  • Schizosaccharomyces / cytology*
  • Schizosaccharomyces / drug effects
  • Schizosaccharomyces / enzymology*
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces pombe Proteins / chemistry
  • Schizosaccharomyces pombe Proteins / metabolism*
  • Trans-Activators / chemistry
  • Trans-Activators / metabolism*
  • Transcription, Genetic / drug effects
  • Ubiquitin-Protein Ligase Complexes / metabolism*
  • Ubiquitination / drug effects

Substances

  • Cell Cycle Proteins
  • DNA-Binding Proteins
  • Rep2 protein, S pombe
  • Schizosaccharomyces pombe Proteins
  • Trans-Activators
  • res2 protein, S pombe
  • srw1 protein, S pombe
  • Ubiquitin-Protein Ligase Complexes
  • Anaphase-Promoting Complex-Cyclosome
  • Checkpoint Kinase 2
  • Cds1 protein, S pombe
  • Protein Serine-Threonine Kinases
  • Proteasome Endopeptidase Complex
  • Hydroxyurea