A Dual Inhibitory Mechanism Sufficient to Maintain Cell-Cycle-Restricted CENP-A Assembly

Mol Cell. 2017 Jan 19;65(2):231-246. doi: 10.1016/j.molcel.2016.11.021. Epub 2016 Dec 22.

Abstract

Chromatin featuring the H3 variant CENP-A at the centromere is critical for its mitotic function and epigenetic maintenance. Assembly of centromeric chromatin is restricted to G1 phase through inhibitory action of Cdk1/2 kinases in other phases of the cell cycle. Here, we identify the two key targets sufficient to maintain cell-cycle control of CENP-A assembly. We uncovered a single phosphorylation site in the licensing factor M18BP1 and a cyclin A binding site in the CENP-A chaperone, HJURP, that mediated specific inhibitory phosphorylation. Simultaneous expression of mutant proteins lacking these residues results in complete uncoupling from the cell cycle. Consequently, CENP-A assembly is fully recapitulated under high Cdk activities, indistinguishable from G1 assembly. We find that Cdk-mediated inhibition is exerted by sequestering active factors away from the centromere. Finally, we show that displacement of M18BP1 from the centromere is critical for the assembly mechanism of CENP-A.

Keywords: CENP-A; cell cycle; centromere; chromatin; cyclin dependent kinase; epigenetics; histone variant; kinetochore; mitosis.

MeSH terms

  • Autoantigens / genetics
  • Autoantigens / metabolism*
  • CDC2 Protein Kinase
  • Centromere / genetics
  • Centromere / metabolism*
  • Centromere Protein A
  • Chromatin / genetics
  • Chromatin / metabolism*
  • Chromatin Assembly and Disassembly*
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Cyclin A / genetics
  • Cyclin A / metabolism
  • Cyclin-Dependent Kinase 2 / genetics
  • Cyclin-Dependent Kinase 2 / metabolism
  • Cyclin-Dependent Kinases / genetics
  • Cyclin-Dependent Kinases / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • G1 Phase Cell Cycle Checkpoints*
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Mutation
  • Phosphorylation
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Signal Transduction
  • Transfection

Substances

  • Autoantigens
  • CENPA protein, human
  • Centromere Protein A
  • Chromatin
  • Chromosomal Proteins, Non-Histone
  • Cyclin A
  • DNA-Binding Proteins
  • HJURP protein, human
  • MIS18BP1 protein, human
  • CDC2 Protein Kinase
  • CDK1 protein, human
  • CDK2 protein, human
  • Cyclin-Dependent Kinase 2
  • Cyclin-Dependent Kinases