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Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization

In somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosi...

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Autores principales: Baumann, Claudia, Zhang, Xiangyu, Viveiros, Maria M., De La Fuente, Rabindranath
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645078/
https://www.ncbi.nlm.nih.gov/pubmed/37935356
http://dx.doi.org/10.1098/rsob.230133
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author Baumann, Claudia
Zhang, Xiangyu
Viveiros, Maria M.
De La Fuente, Rabindranath
author_facet Baumann, Claudia
Zhang, Xiangyu
Viveiros, Maria M.
De La Fuente, Rabindranath
author_sort Baumann, Claudia
collection PubMed
description In somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosis. Pericentric satellite RNAs are also expressed in human oocytes. However, the specific biological function(s) during oocyte meiosis remain to be established. Here, we use validated locked nucleic acid gapmers for major satellite RNA depletion followed by live cell imaging, and superresolution analysis to determine the role of pericentric non-coding RNAs during female meiosis. Depletion of satellite RNA induces mesoscale changes in pericentric heterochromatin structure leading to chromosome instability, kinetochore attachment errors and abnormal chromosome alignment. Chromosome misalignment is associated with spindle defects, microtubule instability and, unexpectedly, loss of acentriolar microtubule organizing centre (aMTOC) tethering to spindle poles. Pericentrin fragmentation and failure to assemble ring-like aMTOCs with loss of associated polo-like kinase 1 provide critical insight into the mechanisms leading to impaired spindle pole integrity. Inhibition of transcription or RNA splicing phenocopies the chromosome alignment errors and spindle defects, suggesting that pericentric transcription during oocyte meiosis is required to regulate heterochromatin structure, chromosome segregation and maintenance of spindle organization.
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spelling pubmed-106450782023-11-08 Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization Baumann, Claudia Zhang, Xiangyu Viveiros, Maria M. De La Fuente, Rabindranath Open Biol Short Communications In somatic cells, mitotic transcription of major satellite non-coding RNAs is tightly regulated and essential for heterochromatin formation and the maintenance of genome integrity. We recently demonstrated that major satellite transcripts are expressed, and chromatin-bound during mouse oocyte meiosis. Pericentric satellite RNAs are also expressed in human oocytes. However, the specific biological function(s) during oocyte meiosis remain to be established. Here, we use validated locked nucleic acid gapmers for major satellite RNA depletion followed by live cell imaging, and superresolution analysis to determine the role of pericentric non-coding RNAs during female meiosis. Depletion of satellite RNA induces mesoscale changes in pericentric heterochromatin structure leading to chromosome instability, kinetochore attachment errors and abnormal chromosome alignment. Chromosome misalignment is associated with spindle defects, microtubule instability and, unexpectedly, loss of acentriolar microtubule organizing centre (aMTOC) tethering to spindle poles. Pericentrin fragmentation and failure to assemble ring-like aMTOCs with loss of associated polo-like kinase 1 provide critical insight into the mechanisms leading to impaired spindle pole integrity. Inhibition of transcription or RNA splicing phenocopies the chromosome alignment errors and spindle defects, suggesting that pericentric transcription during oocyte meiosis is required to regulate heterochromatin structure, chromosome segregation and maintenance of spindle organization. The Royal Society 2023-11-08 /pmc/articles/PMC10645078/ /pubmed/37935356 http://dx.doi.org/10.1098/rsob.230133 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Short Communications
Baumann, Claudia
Zhang, Xiangyu
Viveiros, Maria M.
De La Fuente, Rabindranath
Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title_full Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title_fullStr Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title_full_unstemmed Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title_short Pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
title_sort pericentric major satellite transcription is essential for meiotic chromosome stability and spindle pole organization
topic Short Communications
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10645078/
https://www.ncbi.nlm.nih.gov/pubmed/37935356
http://dx.doi.org/10.1098/rsob.230133
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