Structures of CENP-C cupin domains at regional centromeres reveal unique patterns of dimerization and recruitment functions for the inner pocket

J Biol Chem. 2019 Sep 20;294(38):14119-14134. doi: 10.1074/jbc.RA119.008464. Epub 2019 Jul 31.

Abstract

The successful assembly and regulation of the kinetochore are critical for the equal and accurate segregation of genetic material during the cell cycle. CENP-C (centromere protein C), a conserved inner kinetochore component, has been broadly characterized as a scaffolding protein and is required for the recruitment of multiple kinetochore proteins to the centromere. At its C terminus, CENP-C harbors a conserved cupin domain that has an established role in protein dimerization. Although the crystal structure of the Saccharomyces cerevisiae Mif2CENP-C cupin domain has been determined, centromeric organization and kinetochore composition vary greatly between S. cerevisiae (point centromere) and other eukaryotes (regional centromere). Therefore, whether the structural and functional role of the cupin domain is conserved throughout evolution requires investigation. Here, we report the crystal structures of the Schizosaccharomyces pombe and Drosophila melanogaster CENP-C cupin domains at 2.52 and 1.81 Å resolutions, respectively. Although the central jelly roll architecture is conserved among the three determined CENP-C cupin domain structures, the cupin domains from organisms with regional centromeres contain additional structural features that aid in dimerization. Moreover, we found that the S. pombe Cnp3CENP-C jelly roll fold harbors an inner binding pocket that is used to recruit the meiosis-specific protein Moa1. In summary, our results unveil the evolutionarily conserved and unique features of the CENP-C cupin domain and uncover the mechanism by which it functions as a recruitment factor.

Keywords: CENP-C; Moa1; X-ray crystallography; analytical ultracentrifugation; centromere; cupin domain; fission yeast; kinetochore; meiosis.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle Proteins / metabolism
  • Centromere / metabolism
  • Centromere Protein A / metabolism
  • Chromosomal Proteins, Non-Histone / metabolism*
  • Chromosomal Proteins, Non-Histone / ultrastructure*
  • Crystallography, X-Ray / methods
  • DNA-Binding Proteins / metabolism
  • Dimerization
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / ultrastructure
  • Drosophila melanogaster / metabolism
  • Histones / metabolism
  • Kinetochores / metabolism
  • Kinetochores / ultrastructure
  • Schizosaccharomyces / metabolism
  • Schizosaccharomyces pombe Proteins / metabolism

Substances

  • CENP-C protein, Drosophila
  • Cell Cycle Proteins
  • Centromere Protein A
  • Chromosomal Proteins, Non-Histone
  • DNA-Binding Proteins
  • Drosophila Proteins
  • Histones
  • Moa1 protein, S pombe
  • Schizosaccharomyces pombe Proteins
  • centromere protein C

Associated data

  • PDB/2VPV
  • PDB/6O2D
  • PDB/6O2K