The Ndc80 complex targets Bod1 to human mitotic kinetochores

Open Biol. 2017 Nov;7(11):170099. doi: 10.1098/rsob.170099.

Abstract

Regulation of protein phosphatase activity by endogenous protein inhibitors is an important mechanism to control protein phosphorylation in cells. We recently identified Biorientation defective 1 (Bod1) as a small protein inhibitor of protein phosphatase 2A containing the B56 regulatory subunit (PP2A-B56). This phosphatase controls the amount of phosphorylation of several kinetochore proteins and thus the establishment of load-bearing chromosome-spindle attachments in time for accurate separation of sister chromatids in mitosis. Like PP2A-B56, Bod1 directly localizes to mitotic kinetochores and is required for correct segregation of mitotic chromosomes. In this report, we have probed the spatio-temporal regulation of Bod1 during mitotic progression. Kinetochore localization of Bod1 increases from nuclear envelope breakdown until metaphase. Phosphorylation of Bod1 at threonine 95 (T95), which increases Bod1's binding to and inhibition of PP2A-B56, peaks in prometaphase when PP2A-B56 localization to kinetochores is highest. We demonstrate here that kinetochore targeting of Bod1 depends on the outer kinetochore protein Ndc80 and not PP2A-B56. Crucially, Bod1 depletion functionally affects Ndc80 phosphorylation at the N-terminal serine 55 (S55), as well as a number of other phosphorylation sites within the outer kinetochore, including Knl1 at serine 24 and 60 (S24, S60), and threonine T943 and T1155 (T943, T1155). Therefore, Ndc80 recruits a phosphatase inhibitor to kinetochores which directly feeds forward to regulate Ndc80, and Knl1 phosphorylation, including sites that mediate the attachment of microtubules to kinetochores.

Keywords: BOD1; Knl1; Ndc80 complex; PP2A inhibitor; chromosome segregation; kinetochore.

MeSH terms

  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromosome Segregation
  • Cytoskeletal Proteins
  • Feedback, Physiological
  • HeLa Cells
  • Humans
  • Kinetochores / metabolism*
  • Microtubule-Associated Proteins / metabolism
  • Mitosis*
  • Nuclear Envelope / metabolism
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphorylation
  • Protein Binding
  • Protein Processing, Post-Translational

Substances

  • Bod1 protein, human
  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • Knl1 protein, human
  • Microtubule-Associated Proteins
  • NDC80 protein, human
  • Nuclear Proteins