Cyclin B3 is a dominant fast-acting cyclin that drives rapid early embryonic mitoses

J Cell Biol. 2024 Nov 4;223(11):e202308034. doi: 10.1083/jcb.202308034. Epub 2024 Aug 6.

Abstract

Mitosis in early embryos often proceeds at a rapid pace, but how this pace is achieved is not understood. Here, we show that cyclin B3 is the dominant driver of rapid embryonic mitoses in the C. elegans embryo. Cyclins B1 and B2 support slow mitosis (NEBD to anaphase ∼600 s), but the presence of cyclin B3 dominantly drives the approximately threefold faster mitosis observed in wildtype. Multiple mitotic events are slowed down in cyclin B1 and B2-driven mitosis, and cyclin B3-associated Cdk1 H1 kinase activity is ∼25-fold more active than cyclin B1-associated Cdk1. Addition of cyclin B1 to fast cyclin B3-only mitosis introduces an ∼60-s delay between completion of chromosome alignment and anaphase onset; this delay, which is important for segregation fidelity, is dependent on inhibitory phosphorylation of the anaphase activator Cdc20. Thus, cyclin B3 dominance, coupled to a cyclin B1-dependent delay that acts via Cdc20 phosphorylation, sets the rapid pace and ensures mitotic fidelity in the early C. elegans embryo.

MeSH terms

  • Animals
  • CDC2 Protein Kinase / genetics
  • CDC2 Protein Kinase / metabolism
  • Caenorhabditis elegans Proteins* / genetics
  • Caenorhabditis elegans Proteins* / metabolism
  • Caenorhabditis elegans* / embryology
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Cdc20 Proteins / genetics
  • Cdc20 Proteins / metabolism
  • Cyclin B / genetics
  • Cyclin B / metabolism
  • Cyclin B1* / genetics
  • Cyclin B1* / metabolism
  • Cyclin B2 / genetics
  • Cyclin B2 / metabolism
  • Embryo, Nonmammalian* / metabolism
  • Mitosis*
  • Phosphorylation

Substances

  • Caenorhabditis elegans Proteins
  • CDC2 Protein Kinase
  • Cdc20 Proteins
  • Cyclin B
  • Cyclin B1
  • Cyclin B2
  • CYB-3 protein, C elegans