Unattached kinetochores catalyze production of an anaphase inhibitor that requires a Mad2 template to prime Cdc20 for BubR1 binding

Dev Cell. 2009 Jan;16(1):105-17. doi: 10.1016/j.devcel.2008.11.005.

Abstract

Premature anaphase onset is prevented by the mitotic checkpoint through production of a "wait anaphase" inhibitor(s) that blocks recognition of cyclin B and securin by Cdc20-activated APC/C, an E3 ubiquitin ligase that targets them for destruction. Using physiologically relevant levels of Mad2, Bub3, BubR1, and Cdc20, we demonstrate that unattached kinetochores on purified chromosomes catalytically generate a diffusible Cdc20 inhibitor or inhibit Cdc20 already bound to APC/C. Furthermore, the chromosome-produced inhibitor requires both recruitment of Mad2 by Mad1 that is stably bound at unattached kinetochores and dimerization-competent Mad2. We show that purified chromosomes promote BubR1 binding to APC/C-Cdc20 by acting directly on Mad2, but not BubR1. Our results support a model in which immobilized Mad1/Mad2 at kinetochores provides a template for initial assembly of Mad2 bound to Cdc20 that is then converted to a final mitotic checkpoint inhibitor with Cdc20 bound to BubR1.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaphase / physiology*
  • Anaphase-Promoting Complex-Cyclosome
  • Calcium-Binding Proteins / chemistry
  • Calcium-Binding Proteins / genetics
  • Calcium-Binding Proteins / metabolism*
  • Cdc20 Proteins
  • Cell Cycle Proteins / chemistry
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromosomes / metabolism
  • Dimerization
  • HeLa Cells
  • Humans
  • Kinetochores / metabolism*
  • Mad2 Proteins
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism
  • Poly-ADP-Ribose Binding Proteins
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Repressor Proteins / chemistry
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Ubiquitin-Protein Ligase Complexes / antagonists & inhibitors*
  • Ubiquitin-Protein Ligase Complexes / metabolism

Substances

  • BUB3 protein, human
  • Calcium-Binding Proteins
  • Cdc20 Proteins
  • Cell Cycle Proteins
  • MAD1L1 protein, human
  • MAD2L1 protein, human
  • Mad2 Proteins
  • Nuclear Proteins
  • Poly-ADP-Ribose Binding Proteins
  • Recombinant Proteins
  • Repressor Proteins
  • CDC20 protein, human
  • Ubiquitin-Protein Ligase Complexes
  • Anaphase-Promoting Complex-Cyclosome
  • BUB1 protein, human
  • Bub1 spindle checkpoint protein
  • Protein Serine-Threonine Kinases