Small changes in phospho-occupancy at the kinetochore-microtubule interface drive mitotic fidelity

J Cell Biol. 2022 Sep 5;221(9):e202107107. doi: 10.1083/jcb.202107107. Epub 2022 Jul 25.

Abstract

Kinetochore protein phosphorylation promotes the correction of erroneous microtubule attachments to ensure faithful chromosome segregation during cell division. Determining how phosphorylation executes error correction requires an understanding of whether kinetochore substrates are completely (i.e., all-or-none) or only fractionally phosphorylated. Using quantitative mass spectrometry (MS), we measured phospho-occupancy on the conserved kinetochore protein Hec1 (NDC80) that directly binds microtubules. None of the positions measured exceeded ∼50% phospho-occupancy, and the cumulative phospho-occupancy changed by only ∼20% in response to changes in microtubule attachment status. The narrow dynamic range of phospho-occupancy is maintained, in part, by the ongoing phosphatase activity. Further, both Cdk1-Cyclin B1 and Aurora kinases phosphorylate Hec1 to enhance error correction in response to different types of microtubule attachment errors. The low inherent phospho-occupancy promotes microtubule attachment to kinetochores while the high sensitivity of kinetochore-microtubule attachments to small changes in phospho-occupancy drives error correction and ensures high mitotic fidelity.

Publication types

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

MeSH terms

  • Aurora Kinases / metabolism
  • CDC2 Protein Kinase / metabolism
  • Chromosome Segregation
  • Cyclin B1 / metabolism
  • Cytoskeletal Proteins* / metabolism
  • HeLa Cells
  • Humans
  • Kinetochores* / metabolism
  • Microtubules* / metabolism
  • Mitosis*
  • Phosphorylation

Substances

  • CCNB1 protein, human
  • Cyclin B1
  • Cytoskeletal Proteins
  • NDC80 protein, human
  • Aurora Kinases
  • CDC2 Protein Kinase
  • CDK1 protein, human