Distinct TERB1 Domains Regulate Different Protein Interactions in Meiotic Telomere Movement

• Published in: Cell reports (Cambridge) 2017-11, Vol.21 (7), p.1715-1726
• Main Authors: Zhang, Jingjing, Tu, Zhaowei, Watanabe, Yoshinori, Shibuya, Hiroki
• Format: Article
• Language: English
• Subjects: Animals; Binding Sites; Carrier Proteins - chemistry; Carrier Proteins - genetics; Carrier Proteins - metabolism; Cell Biology; Cell Cycle Proteins - chemistry; Cell Cycle Proteins - genetics; Cell Cycle Proteins - metabolism; Cellbiologi; Chromosomal Proteins, Non-Histone - genetics; Chromosomal Proteins, Non-Histone - metabolism; chromosome; Cohesins; germ cell; MAJIN; Male; Meiosis; Membrane Proteins - genetics; Membrane Proteins - metabolism; Mice; Mice, Inbred C57BL; Nuclear Envelope - metabolism; Protein Binding; shelterin; Spermatocytes - cytology; Spermatocytes - metabolism; telomere; 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; TERB1; TERB2; TRF1
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2017.10.061

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. [Display omitted] •Deletion of TRF1 in spermatocytes impairs the assembly of meiotic telomere complex•Identification of distinct TERB2 binding domain in TERB1•T2B domain in TERB1 is essential for telomere and nuclear envelope attachment•Cohesin recruitment by TERB1 MYB domain is required for efficient telomere movement During meiosis, telomeres attach to the nuclear envelope and drive the chromosome movement required for the pairing of homologous chromosomes. Zhang et al. reveal protein interaction networks within mammalian meiotic telomere complex, mediated by various domains of TERB1, which enable the sequential assembly of the complex and subsequent telomere movements.