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Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation
BACKGROUND: Chromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet. In fission yeast, telomeres localize to the nuclear periphery via interaction of the telomeric protein Rap1 with the membrane protein Bqt4. During meiotic prophase, the meiotic proteins Bqt1-2 bind R...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4660835/ https://www.ncbi.nlm.nih.gov/pubmed/26058898 http://dx.doi.org/10.1186/s12915-015-0149-x |
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author | Amelina, Hanna Subramaniam, Shaan Moiseeva, Vera Armstrong, Christine Anne Pearson, Siân Rosanna Tomita, Kazunori |
author_facet | Amelina, Hanna Subramaniam, Shaan Moiseeva, Vera Armstrong, Christine Anne Pearson, Siân Rosanna Tomita, Kazunori |
author_sort | Amelina, Hanna |
collection | PubMed |
description | BACKGROUND: Chromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet. In fission yeast, telomeres localize to the nuclear periphery via interaction of the telomeric protein Rap1 with the membrane protein Bqt4. During meiotic prophase, the meiotic proteins Bqt1-2 bind Rap1 and tether to the spindle pole body to form the bouquet. Although it is known that this polarized chromosomal arrangement plays a crucial role in meiotic progression, the molecular mechanisms of telomere bouquet regulation are poorly understood. RESULTS: Here, we detected high levels of Rap1 phospho-modification throughout meiotic prophase, and identified a maximum of 35 phosphorylation sites. Concomitant phosphomimetic mutation of the modification sites suggests that Rap1 hyper-phosphorylation does not directly regulate telomere bouquet formation or dissociation. Despite the negative charge conferred by its highly phosphorylated state, Rap1 maintains interactions with its binding partners. Interestingly, mutations that change the charge of negatively charged residues within the Bqt1-2 binding site of Rap1 abolished the affinity to the Bqt1-2 complex, suggesting that the intrinsic negative charge of Rap1 is crucial for telomere bouquet formation. CONCLUSIONS: Whereas Rap1 hyper-phosphorylation observed in meiotic prophase does not have an apparent role in bouquet formation, the intrinsic negative charge of Rap1 is important for forming interactions with its binding partners. Thus, Rap1 is able to retain bouquet formation under heavily phosphorylated status. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-015-0149-x) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4660835 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-46608352015-11-27 Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation Amelina, Hanna Subramaniam, Shaan Moiseeva, Vera Armstrong, Christine Anne Pearson, Siân Rosanna Tomita, Kazunori BMC Biol Research Article BACKGROUND: Chromosomes reorganize in early meiotic prophase to form the so-called telomere bouquet. In fission yeast, telomeres localize to the nuclear periphery via interaction of the telomeric protein Rap1 with the membrane protein Bqt4. During meiotic prophase, the meiotic proteins Bqt1-2 bind Rap1 and tether to the spindle pole body to form the bouquet. Although it is known that this polarized chromosomal arrangement plays a crucial role in meiotic progression, the molecular mechanisms of telomere bouquet regulation are poorly understood. RESULTS: Here, we detected high levels of Rap1 phospho-modification throughout meiotic prophase, and identified a maximum of 35 phosphorylation sites. Concomitant phosphomimetic mutation of the modification sites suggests that Rap1 hyper-phosphorylation does not directly regulate telomere bouquet formation or dissociation. Despite the negative charge conferred by its highly phosphorylated state, Rap1 maintains interactions with its binding partners. Interestingly, mutations that change the charge of negatively charged residues within the Bqt1-2 binding site of Rap1 abolished the affinity to the Bqt1-2 complex, suggesting that the intrinsic negative charge of Rap1 is crucial for telomere bouquet formation. CONCLUSIONS: Whereas Rap1 hyper-phosphorylation observed in meiotic prophase does not have an apparent role in bouquet formation, the intrinsic negative charge of Rap1 is important for forming interactions with its binding partners. Thus, Rap1 is able to retain bouquet formation under heavily phosphorylated status. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-015-0149-x) contains supplementary material, which is available to authorized users. BioMed Central 2015-06-10 /pmc/articles/PMC4660835/ /pubmed/26058898 http://dx.doi.org/10.1186/s12915-015-0149-x Text en © Amelina et al. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Amelina, Hanna Subramaniam, Shaan Moiseeva, Vera Armstrong, Christine Anne Pearson, Siân Rosanna Tomita, Kazunori Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title | Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title_full | Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title_fullStr | Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title_full_unstemmed | Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title_short | Telomere protein Rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
title_sort | telomere protein rap1 is a charge resistant scaffolding protein in chromosomal bouquet formation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4660835/ https://www.ncbi.nlm.nih.gov/pubmed/26058898 http://dx.doi.org/10.1186/s12915-015-0149-x |
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