Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes

Cell Rep. 2015 Apr 28;11(4):551-63. doi: 10.1016/j.celrep.2015.03.045. Epub 2015 Apr 16.

Abstract

Telomere-led rapid prophase movements (RPMs) in meiotic prophase have been observed in diverse eukaryote species. A shared feature of RPMs is that the force that drives the chromosomal movements is transmitted from the cytoskeleton, through the nuclear envelope, to the telomeres. Studies in mice suggested that dynein movement along microtubules is transmitted to telomeres through SUN1/KASH5 nuclear envelope bridges to generate RPMs. We monitored RPMs in mouse seminiferous tubules using 4D fluorescence imaging and quantitative motion analysis to characterize patterns of movement in the RPM process. We find that RPMs reflect a combination of nuclear rotation and individual chromosome movements. The telomeres move along microtubule tracks that are apparently continuous with the cytoskeletal network and exhibit characteristic arrangements at different stages of prophase. Quantitative measurements confirmed that SUN1/KASH5, microtubules, and dynein, but not actin, were necessary for RPMs and that defects in meiotic recombination and synapsis resulted in altered RPMs.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle Proteins / metabolism
  • Cytoskeletal Proteins
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microtubule-Associated Proteins / metabolism
  • Microtubules / metabolism
  • Nuclear Envelope / metabolism
  • Nuclear Envelope / ultrastructure
  • Nuclear Proteins / metabolism
  • Prophase*
  • Seminiferous Tubules / metabolism
  • Seminiferous Tubules / ultrastructure*
  • Telomere / genetics*
  • Telomere / ultrastructure

Substances

  • Cell Cycle Proteins
  • Cytoskeletal Proteins
  • KASH5 protein, mouse
  • Microtubule-Associated Proteins
  • Nuclear Proteins
  • SUN1 protein, mouse