Regulation of Cdc2/cyclin B activation in Xenopus egg extracts via inhibitory phosphorylation of Cdc25C phosphatase by Ca(2+)/calmodulin-dependent protein [corrected] kinase II

Mol Biol Cell. 2003 Oct;14(10):4003-14. doi: 10.1091/mbc.e03-02-0061. Epub 2003 Jul 11.

Abstract

Activation of Cdc2/cyclin B kinase and entry into mitosis requires dephosphorylation of inhibitory sites on Cdc2 by Cdc25 phosphatase. In vertebrates, Cdc25C is inhibited by phosphorylation at a single site targeted by the checkpoint kinases Chk1 and Cds1/Chk2 in response to DNA damage or replication arrest. In Xenopus early embryos, the inhibitory site on Cdc25C (S287) is also phosphorylated by a distinct protein kinase that may determine the intrinsic timing of the cell cycle. We show that S287-kinase activity is repressed in extracts of unfertilized Xenopus eggs arrested in M phase but is rapidly stimulated upon release into interphase by addition of Ca2+, which mimics fertilization. S287-kinase activity is not dependent on cyclin B degradation or inactivation of Cdc2/cyclin B kinase, indicating a direct mechanism of activation by Ca2+. Indeed, inhibitor studies identify the predominant S287-kinase as Ca2+/calmodulin-dependent protein kinase II (CaMKII). CaMKII phosphorylates Cdc25C efficiently on S287 in vitro and, like Chk1, is inhibited by 7-hydroxystaurosporine (UCN-01) and debromohymenialdisine, compounds that abrogate G2 arrest in somatic cells. CaMKII delays Cdc2/cyclin B activation via phosphorylation of Cdc25C at S287 in egg extracts, indicating that this pathway regulates the timing of mitosis during the early embryonic cell cycle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Azepines / pharmacology
  • CDC2-CDC28 Kinases / metabolism*
  • Calcium / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases / metabolism*
  • Cell Cycle Proteins / metabolism*
  • Checkpoint Kinase 1
  • Checkpoint Kinase 2
  • Cloning, Molecular
  • Cyclin B / metabolism*
  • DNA Damage
  • DNA Replication
  • Female
  • G2 Phase / physiology
  • Interphase
  • Mitosis
  • Models, Molecular
  • Molecular Sequence Data
  • Oocytes / enzymology*
  • Phosphorylation
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases / metabolism
  • Protein Structure, Tertiary
  • Pyrroles / pharmacology
  • Staurosporine / analogs & derivatives*
  • Staurosporine / pharmacology
  • Xenopus Proteins
  • Xenopus laevis
  • cdc25 Phosphatases / metabolism*

Substances

  • Azepines
  • Cell Cycle Proteins
  • Cyclin B
  • Pyrroles
  • Xenopus Proteins
  • debromohymenialdisine
  • 7-hydroxystaurosporine
  • Protein Kinases
  • Checkpoint Kinase 2
  • Checkpoint Kinase 1
  • Chek1 protein, Xenopus
  • Protein Serine-Threonine Kinases
  • Calcium-Calmodulin-Dependent Protein Kinase Type 2
  • Calcium-Calmodulin-Dependent Protein Kinases
  • CDC2-CDC28 Kinases
  • cdc25 Phosphatases
  • Staurosporine
  • Calcium