Molecular basis of CENP-C association with the CENP-A nucleosome at yeast centromeres

Genes Dev. 2017 Oct 1;31(19):1958-1972. doi: 10.1101/gad.304782.117. Epub 2017 Oct 26.

Abstract

Histone CENP-A-containing nucleosomes play an important role in nucleating kinetochores at centromeres for chromosome segregation. However, the molecular mechanisms by which CENP-A nucleosomes engage with kinetochore proteins are not well understood. Here, we report the finding of a new function for the budding yeast Cse4/CENP-A histone-fold domain interacting with inner kinetochore protein Mif2/CENP-C. Strikingly, we also discovered that AT-rich centromere DNA has an important role for Mif2 recruitment. Mif2 contacts one side of the nucleosome dyad, engaging with both Cse4 residues and AT-rich nucleosomal DNA. Both interactions are directed by a contiguous DNA- and histone-binding domain (DHBD) harboring the conserved CENP-C motif, an AT hook, and RK clusters (clusters enriched for arginine-lysine residues). Human CENP-C has two related DHBDs that bind preferentially to DNA sequences of higher AT content. Our findings suggest that a DNA composition-based mechanism together with residues characteristic for the CENP-A histone variant contribute to the specification of centromere identity.

Keywords: AT-rich DNA; Cse4/CENP-A; Mif2/CENP-C; budding yeast; centromere; nucleosome.

MeSH terms

  • AT Rich Sequence
  • Centromere / chemistry
  • Centromere / metabolism*
  • Centromere Protein A / chemistry
  • Centromere Protein A / metabolism*
  • Chromosomal Proteins, Non-Histone / chemistry
  • Chromosomal Proteins, Non-Histone / metabolism*
  • DNA, Satellite / metabolism
  • DNA-Binding Proteins / metabolism
  • Dimerization
  • Humans
  • Models, Molecular*
  • Nucleosomes / chemistry*
  • Nucleosomes / metabolism*
  • Protein Binding
  • Protein Structure, Tertiary
  • Saccharomyces cerevisiae Proteins / metabolism
  • Saccharomyces cerevisiae* / chemistry
  • Saccharomyces cerevisiae* / metabolism

Substances

  • CSE4 protein, S cerevisiae
  • Centromere Protein A
  • Chromosomal Proteins, Non-Histone
  • DNA, Satellite
  • DNA-Binding Proteins
  • MIF2 protein, S cerevisiae
  • Nucleosomes
  • Saccharomyces cerevisiae Proteins
  • centromere protein C