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

Author:

Lara-Gonzalez Pablo12ORCID,Variyar Smriti34ORCID,Moghareh Shabnam1ORCID,Nguyen Anh Cao Ngoc1ORCID,Kizhedathu Amrutha1ORCID,Budrewicz Jacqueline2ORCID,Schlientz Aleesa34ORCID,Varshney Neha34ORCID,Bellaart Andrew34ORCID,Oegema Karen234ORCID,Bardwell Lee1ORCID,Desai Arshad234ORCID

Affiliation:

1. University of California, Irvine 1 Department of Developmental and Cell Biology, , Irvine, CA, USA

2. Ludwig Institute for Cancer Research 2 , La Jolla, CA, USA

3. University of California, San Diego 3 Department of Cell and Developmental Biology, , San Diego, CA, USA

4. University of California, San Diego 4 Department of Cellular and Molecular Medicine, , San Diego, CA, USA

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.

Funder

NIH Office of Research Infrastructure Programs

National Institutes of Health

Ludwig Institute for Cancer Research

Publisher

Rockefeller University Press

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