Distinct TERB1 Domains Regulate Different Protein Interactions in Meiotic Telomere Movement

Cell Rep. 2017 Nov 14;21(7):1715-1726. doi: 10.1016/j.celrep.2017.10.061.

Abstract

Meiotic telomeres attach to the nuclear envelope (NE) and drive the chromosome movement required for the pairing of homologous chromosomes. The meiosis-specific telomere proteins TERB1, TERB2, and MAJIN are required to regulate these events, but their assembly processes are largely unknown. Here, we developed a germ-cell-specific knockout mouse of the canonical telomere-binding protein TRF1 and revealed an essential role for TRF1 in directing the assembly of TERB1-TERB2-MAJIN. Further, we identified a TERB2 binding (T2B) domain in TERB1 that is dispensable for the TRF1-TERB1 interaction but is essential for the subsequent TERB1-TERB2 interaction and therefore for telomere attachment to the NE. Meanwhile, cohesin recruitment at telomeres, which is required for efficient telomere movement, is mediated by the MYB-like domain of TERB1, but not by TERB2-MAJIN. Our results reveal distinct protein interactions through various domains of TERB1, which enable the sequential assembly of the meiotic telomere complex for their movements.

Keywords: MAJIN; TERB1; TERB2; TRF1; chromosome; germ cell; meiosis; shelterin; telomere.

MeSH terms

  • Animals
  • Binding Sites
  • Carrier Proteins / chemistry
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Cell Cycle Proteins / chemistry
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • Male
  • Meiosis*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Nuclear Envelope / metabolism
  • Protein Binding
  • Spermatocytes / cytology
  • Spermatocytes / metabolism
  • Telomere / genetics*
  • Telomere / metabolism
  • Telomere-Binding Proteins / chemistry
  • Telomere-Binding Proteins / genetics
  • Telomere-Binding Proteins / metabolism
  • Telomeric Repeat Binding Protein 1 / genetics
  • Telomeric Repeat Binding Protein 1 / metabolism

Substances

  • Carrier Proteins
  • Cell Cycle Proteins
  • Chromosomal Proteins, Non-Histone
  • MAJIN protein, mouse
  • Membrane Proteins
  • TERB1 protein, mouse
  • TERB2 protein, mouse
  • Telomere-Binding Proteins
  • Telomeric Repeat Binding Protein 1
  • cohesins