A kinetochore-independent mechanism drives anaphase chromosome separation during acentrosomal meiosis

Nat Cell Biol. 2010 Sep;12(9):894-901. doi: 10.1038/ncb2093. Epub 2010 Aug 22.

Abstract

Although assembly of acentrosomal meiotic spindles has been extensively studied, little is known about the segregation of chromosomes on these spindles. Here, we show in Caenorhabditis elegans oocytes that the kinetochore protein, KNL-1, directs assembly of meiotic kinetochores that orient chromosomes. However, in contrast to mitosis, chromosome separation during meiotic anaphase is kinetochore-independent. Before anaphase, meiotic kinetochores and spindle poles disassemble along with the microtubules on the poleward side of chromosomes. During anaphase, microtubules then form between the separating chromosomes. Functional analysis implicated a set of proteins that localize to a ring-shaped domain between kinetochores during pre-anaphase spindle assembly and anaphase separation. These proteins are localized by the chromosomal passenger complex, which regulates the loss of meiotic chromosome cohesion. Thus, meiotic segregation in C. elegans is a two-stage process, where kinetochores orient chromosomes, but are then dispensable for their separation. We suggest that separation is controlled by a meiosis-specific chromosomal domain to coordinate cohesin removal and chromosome segregation.

Publication types

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

MeSH terms

  • Anaphase / physiology*
  • Aneuploidy
  • Animals
  • Aurora Kinase B
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / physiology
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • Chromosome Segregation / physiology*
  • Chromosomes / metabolism
  • Histones / metabolism
  • Kinesins / genetics
  • Kinesins / metabolism
  • Kinetochores / physiology*
  • Meiosis / physiology*
  • Metaphase / physiology
  • Microscopy, Confocal
  • Microscopy, Fluorescence
  • Microtubule-Associated Proteins / genetics
  • Microtubule-Associated Proteins / metabolism
  • Microtubules / metabolism
  • Oocytes / cytology
  • Oocytes / physiology
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • RNA Interference
  • RNA, Double-Stranded / genetics

Substances

  • Caenorhabditis elegans Proteins
  • Chromosomal Proteins, Non-Histone
  • HCP-2 protein, C elegans
  • Histones
  • KLP-19 protein, C elegans
  • KNL-1 protein, C elegans
  • Microtubule-Associated Proteins
  • RNA, Double-Stranded
  • hcp-1 protein, C elegans
  • Aurora Kinase B
  • Bub1 spindle checkpoint protein
  • Protein Serine-Threonine Kinases
  • air-2 protein, C elegans
  • Kinesins