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Speedy A-Cdk2 binding mediates initial telomere-nuclear envelope attachment during meiotic prophase i independent of Cdk2 activation

Tu, Zhaowei ; Bayazit, Mustafa Bilal ; Liu, Hongbin ; Zhang, Jingjing ; Busayavalasa, Kiran ; Risal, Sanjiv ; Shao, Jingchen ; Satyanarayana, Ande ; Coppola, Vincenzo and Tessarollo, Lino , et al. (2017) In Proceedings of the National Academy of Sciences of the United States of America 114(3). p.592-597
Abstract

Telomere attachment to the nuclear envelope (NE) is a prerequisite for chromosomemovement duringmeiotic prophase I that is required for pairing of homologous chromosomes, synapsis, and homologous recombination. Here we show that Speedy A, a noncanonical activator of cyclin-dependent kinases (Cdks), is specifically localized to telomeres in prophase I male and female germ cells in mice, and plays an essential role in the telomere-NE attachment. Deletion of Spdya in mice disrupts telomere-NE attachment, and this impairs homologous pairing and synapsis and leads to zygotene arrest in male and female germ cells. In addition, we have identified a telomere localization domain on Speedy A covering the distal N terminus and the Cdk2- binding... (More)

Telomere attachment to the nuclear envelope (NE) is a prerequisite for chromosomemovement duringmeiotic prophase I that is required for pairing of homologous chromosomes, synapsis, and homologous recombination. Here we show that Speedy A, a noncanonical activator of cyclin-dependent kinases (Cdks), is specifically localized to telomeres in prophase I male and female germ cells in mice, and plays an essential role in the telomere-NE attachment. Deletion of Spdya in mice disrupts telomere-NE attachment, and this impairs homologous pairing and synapsis and leads to zygotene arrest in male and female germ cells. In addition, we have identified a telomere localization domain on Speedy A covering the distal N terminus and the Cdk2- binding Ringo domain, and this domain is essential for the localization of Speedy A to telomeres. Furthermore, we found that the binding of Cdk2 to Speedy A is indispensable for Cdk2's localization on telomeres, suggesting that Speedy A and Cdk2 might be the initial components that are recruited to the NE for forming the meiotic telomere complex. However, Speedy A-Cdk2-mediated telomere-NE attachment is independent of Cdk2 activation. Our results thus indicate that Speedy A and Cdk2 might mediate the initial telomere-NE attachment for the efficient assembly of the telomere complex that is essential for meiotic prophase I progression.

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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Cdk2, Germ cells, Meiosis, Speedy A, Telomere
in
Proceedings of the National Academy of Sciences of the United States of America
volume
114
issue
3
pages
6 pages
publisher
National Acad Sciences
external identifiers
  • scopus:85009820898
  • pmid:28031483
ISSN
0027-8424
DOI
10.1073/pnas.1618465114
language
English
LU publication?
no
id
f5a8dfe4-04f1-4c73-83ac-8f76cd18352f
date added to LUP
2019-09-18 10:24:31
date last changed
2021-03-09 03:27:21
@article{f5a8dfe4-04f1-4c73-83ac-8f76cd18352f,
  abstract     = {<p>Telomere attachment to the nuclear envelope (NE) is a prerequisite for chromosomemovement duringmeiotic prophase I that is required for pairing of homologous chromosomes, synapsis, and homologous recombination. Here we show that Speedy A, a noncanonical activator of cyclin-dependent kinases (Cdks), is specifically localized to telomeres in prophase I male and female germ cells in mice, and plays an essential role in the telomere-NE attachment. Deletion of Spdya in mice disrupts telomere-NE attachment, and this impairs homologous pairing and synapsis and leads to zygotene arrest in male and female germ cells. In addition, we have identified a telomere localization domain on Speedy A covering the distal N terminus and the Cdk2- binding Ringo domain, and this domain is essential for the localization of Speedy A to telomeres. Furthermore, we found that the binding of Cdk2 to Speedy A is indispensable for Cdk2's localization on telomeres, suggesting that Speedy A and Cdk2 might be the initial components that are recruited to the NE for forming the meiotic telomere complex. However, Speedy A-Cdk2-mediated telomere-NE attachment is independent of Cdk2 activation. Our results thus indicate that Speedy A and Cdk2 might mediate the initial telomere-NE attachment for the efficient assembly of the telomere complex that is essential for meiotic prophase I progression.</p>},
  author       = {Tu, Zhaowei and Bayazit, Mustafa Bilal and Liu, Hongbin and Zhang, Jingjing and Busayavalasa, Kiran and Risal, Sanjiv and Shao, Jingchen and Satyanarayana, Ande and Coppola, Vincenzo and Tessarollo, Lino and Singh, Meenakshi and Zheng, Chunwei and Han, Chunsheng and Chen, Zijiang and Kaldis, Philipp and Gustafsson, Jan Åke and Liu, Kui},
  issn         = {0027-8424},
  language     = {eng},
  month        = {01},
  number       = {3},
  pages        = {592--597},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences of the United States of America},
  title        = {Speedy A-Cdk2 binding mediates initial telomere-nuclear envelope attachment during meiotic prophase i independent of Cdk2 activation},
  url          = {http://dx.doi.org/10.1073/pnas.1618465114},
  doi          = {10.1073/pnas.1618465114},
  volume       = {114},
  year         = {2017},
}