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The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans

BACKGROUND: Meiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell. Reduction of ploidy depends on active chromosome movements during early meiotic prophase I. Chromosome movements require telomere attachment to the nuclear envelope. T...

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Autores principales: da Cruz, Irene, Brochier-Armanet, Céline, Benavente, Ricardo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7227075/
https://www.ncbi.nlm.nih.gov/pubmed/32408858
http://dx.doi.org/10.1186/s12862-020-01612-9
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author da Cruz, Irene
Brochier-Armanet, Céline
Benavente, Ricardo
author_facet da Cruz, Irene
Brochier-Armanet, Céline
Benavente, Ricardo
author_sort da Cruz, Irene
collection PubMed
description BACKGROUND: Meiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell. Reduction of ploidy depends on active chromosome movements during early meiotic prophase I. Chromosome movements require telomere attachment to the nuclear envelope. This attachment is mediated by telomere adaptor proteins. Telomere adaptor proteins have to date been identified in fission yeast and mice. In the mouse, they form a complex composed of the meiotic proteins TERB1, TERB2, and MAJIN. No sequence similarity was observed between these three mouse proteins and the adaptor proteins of fission yeast, raising the question of the evolutionary history and significance of this specific protein complex. RESULT: Here, we show the TERB1, TERB2, and MAJIN proteins are found throughout the Metazoa and even in early-branching non-bilateral phyla such as Cnidaria, Placozoa and Porifera. Metazoan TERB1, TERB2, and MAJIN showed comparable domain architecture across all clades. Furthermore, the protein domains involved in the formation of the complex as well as those involved for the interaction with the telomere shelterin protein and the LINC complexes revealed high sequence similarity. Finally, gene expression in the cnidarian Hydra vulgaris provided evidence that the TERB1-TERB2-MAJIN complex is selectively expressed in the germ line. CONCLUSION: Our results indicate that the TERB1-TERB2-MAJIN complex has an ancient origin in metazoans, suggesting conservation of meiotic functions.
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spelling pubmed-72270752020-05-27 The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans da Cruz, Irene Brochier-Armanet, Céline Benavente, Ricardo BMC Evol Biol Research Article BACKGROUND: Meiosis is essential for sexual reproduction and generates genetically diverse haploid gametes from a diploid germ cell. Reduction of ploidy depends on active chromosome movements during early meiotic prophase I. Chromosome movements require telomere attachment to the nuclear envelope. This attachment is mediated by telomere adaptor proteins. Telomere adaptor proteins have to date been identified in fission yeast and mice. In the mouse, they form a complex composed of the meiotic proteins TERB1, TERB2, and MAJIN. No sequence similarity was observed between these three mouse proteins and the adaptor proteins of fission yeast, raising the question of the evolutionary history and significance of this specific protein complex. RESULT: Here, we show the TERB1, TERB2, and MAJIN proteins are found throughout the Metazoa and even in early-branching non-bilateral phyla such as Cnidaria, Placozoa and Porifera. Metazoan TERB1, TERB2, and MAJIN showed comparable domain architecture across all clades. Furthermore, the protein domains involved in the formation of the complex as well as those involved for the interaction with the telomere shelterin protein and the LINC complexes revealed high sequence similarity. Finally, gene expression in the cnidarian Hydra vulgaris provided evidence that the TERB1-TERB2-MAJIN complex is selectively expressed in the germ line. CONCLUSION: Our results indicate that the TERB1-TERB2-MAJIN complex has an ancient origin in metazoans, suggesting conservation of meiotic functions. BioMed Central 2020-05-14 /pmc/articles/PMC7227075/ /pubmed/32408858 http://dx.doi.org/10.1186/s12862-020-01612-9 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
da Cruz, Irene
Brochier-Armanet, Céline
Benavente, Ricardo
The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title_full The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title_fullStr The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title_full_unstemmed The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title_short The TERB1-TERB2-MAJIN complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
title_sort terb1-terb2-majin complex of mouse meiotic telomeres dates back to the common ancestor of metazoans
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7227075/
https://www.ncbi.nlm.nih.gov/pubmed/32408858
http://dx.doi.org/10.1186/s12862-020-01612-9
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