An SMC-domain protein in fission yeast links telomeres to the meiotic centrosome

Mol Cell. 2004 Nov 19;16(4):619-30. doi: 10.1016/j.molcel.2004.10.027.

Abstract

Abnormal centrosomal structures similar to those occurring in human cancers are induced in fission yeast by overexpression of the pericentrin homolog Pcp1p. Analysis of abnormal Pcp1p-containing structures with quantitative mass spectrometry and isotope-coded affinity tags identified a coiled-coil, structural maintenance of chromosomes (SMC) domain protein. This protein, termed Ccq1p (coiled-coil protein quantitatively enriched), localizes with Taz1p to telomeres in normal vegetative cells. Fluorescence resonance energy transfer (FRET) measurements indicate that Ccq1p also interacts with centrosomal Pcp1p in mating pheromone-stimulated cells containing centrosomally clustered telomeres. We provide evidence that the Ccq1p-Pcp1p interaction, while essential for meiosis, is deleterious when forced to occur during vegetative growth. Cells lacking one ccq1 allele exhibit a loss-of-function phenotype including abnormally long cell length, chromosome segregation failure, telomeric shortening, and defective telomeric clustering during meiotic prophase. Our data indicate a mechanism underlying meiotic chromosomal bouquet formation and suggest a recruitment model for supernumerary centrosome toxicity.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Alleles
  • Cell Nucleus / metabolism
  • Centrosome / metabolism*
  • Chromosomes, Fungal
  • Fluorescence Resonance Energy Transfer
  • Mass Spectrometry
  • Meiosis
  • Microscopy, Fluorescence
  • Models, Biological
  • Models, Molecular
  • Oligonucleotide Array Sequence Analysis
  • Open Reading Frames
  • Peptide Mapping
  • Plasmids
  • Protein Structure, Tertiary
  • RNA, Messenger / metabolism
  • Schizosaccharomyces / cytology
  • Schizosaccharomyces / genetics
  • Schizosaccharomyces / metabolism*
  • Schizosaccharomyces pombe Proteins / chemistry*
  • Schizosaccharomyces pombe Proteins / genetics
  • Schizosaccharomyces pombe Proteins / metabolism*
  • Telomere / metabolism*
  • Telomere-Binding Proteins / metabolism

Substances

  • RNA, Messenger
  • Schizosaccharomyces pombe Proteins
  • Telomere-Binding Proteins
  • taz1 protein, S pombe