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Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction

Chromosome segregation errors in oocytes lead to the production of aneuploid eggs, which are the leading cause of pregnancy loss and of several congenital diseases such as Down syndrome. The frequency of chromosome segregation errors in oocytes increases with maternal age, especially at a late stage...

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Autores principales: Mishina, Tappei, Tabata, Namine, Hayashi, Tetsutaro, Yoshimura, Mika, Umeda, Mana, Mori, Masashi, Ikawa, Yayoi, Hamada, Hiroshi, Nikaido, Itoshi, Kitajima, Tomoya S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8373347/
https://www.ncbi.nlm.nih.gov/pubmed/34245092
http://dx.doi.org/10.1111/acel.13428
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author Mishina, Tappei
Tabata, Namine
Hayashi, Tetsutaro
Yoshimura, Mika
Umeda, Mana
Mori, Masashi
Ikawa, Yayoi
Hamada, Hiroshi
Nikaido, Itoshi
Kitajima, Tomoya S.
author_facet Mishina, Tappei
Tabata, Namine
Hayashi, Tetsutaro
Yoshimura, Mika
Umeda, Mana
Mori, Masashi
Ikawa, Yayoi
Hamada, Hiroshi
Nikaido, Itoshi
Kitajima, Tomoya S.
author_sort Mishina, Tappei
collection PubMed
description Chromosome segregation errors in oocytes lead to the production of aneuploid eggs, which are the leading cause of pregnancy loss and of several congenital diseases such as Down syndrome. The frequency of chromosome segregation errors in oocytes increases with maternal age, especially at a late stage of reproductive life. How aging at various life stages affects oocytes differently remains poorly understood. In this study, we describe aging‐associated changes in the transcriptome profile of mouse oocytes throughout reproductive life. Our single‐oocyte comprehensive RNA sequencing using RamDA‐seq revealed that oocytes undergo transcriptome changes at a late reproductive stage, whereas their surrounding cumulus cells exhibit transcriptome changes at an earlier stage. Calorie restriction, a paradigm that reportedly prevents aging‐associated egg aneuploidy, promotes a transcriptome shift in oocytes with the up‐regulation of genes involved in chromosome segregation. This shift is accompanied by the improved maintenance of chromosomal cohesin, the loss of which is a hallmark of oocyte aging and causes chromosome segregation errors. These findings have implications for understanding how oocytes undergo aging‐associated functional decline throughout their reproductive life in a context‐dependent manner.
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spelling pubmed-83733472021-08-24 Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction Mishina, Tappei Tabata, Namine Hayashi, Tetsutaro Yoshimura, Mika Umeda, Mana Mori, Masashi Ikawa, Yayoi Hamada, Hiroshi Nikaido, Itoshi Kitajima, Tomoya S. Aging Cell Original Articles Chromosome segregation errors in oocytes lead to the production of aneuploid eggs, which are the leading cause of pregnancy loss and of several congenital diseases such as Down syndrome. The frequency of chromosome segregation errors in oocytes increases with maternal age, especially at a late stage of reproductive life. How aging at various life stages affects oocytes differently remains poorly understood. In this study, we describe aging‐associated changes in the transcriptome profile of mouse oocytes throughout reproductive life. Our single‐oocyte comprehensive RNA sequencing using RamDA‐seq revealed that oocytes undergo transcriptome changes at a late reproductive stage, whereas their surrounding cumulus cells exhibit transcriptome changes at an earlier stage. Calorie restriction, a paradigm that reportedly prevents aging‐associated egg aneuploidy, promotes a transcriptome shift in oocytes with the up‐regulation of genes involved in chromosome segregation. This shift is accompanied by the improved maintenance of chromosomal cohesin, the loss of which is a hallmark of oocyte aging and causes chromosome segregation errors. These findings have implications for understanding how oocytes undergo aging‐associated functional decline throughout their reproductive life in a context‐dependent manner. John Wiley and Sons Inc. 2021-07-10 2021-08 /pmc/articles/PMC8373347/ /pubmed/34245092 http://dx.doi.org/10.1111/acel.13428 Text en © 2021 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Mishina, Tappei
Tabata, Namine
Hayashi, Tetsutaro
Yoshimura, Mika
Umeda, Mana
Mori, Masashi
Ikawa, Yayoi
Hamada, Hiroshi
Nikaido, Itoshi
Kitajima, Tomoya S.
Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title_full Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title_fullStr Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title_full_unstemmed Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title_short Single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
title_sort single‐oocyte transcriptome analysis reveals aging‐associated effects influenced by life stage and calorie restriction
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8373347/
https://www.ncbi.nlm.nih.gov/pubmed/34245092
http://dx.doi.org/10.1111/acel.13428
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