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LSM14B controls oocyte mRNA storage and stability to ensure female fertility

Controlled mRNA storage and stability is essential for oocyte meiosis and early embryonic development. However, how to regulate mRNA storage and stability in mammalian oogenesis remains elusive. Here we showed that LSM14B, a component of membraneless compartments including P-body-like granules and m...

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Autores principales: Shan, Li-Ying, Tian, Yu, Liu, Wen-Xiang, Fan, Hai-Tao, Li, Feng-Guo, Liu, Wen-Juan, Li, Ang, Shen, Wei, Sun, Qing-Yuan, Liu, Yong-Bin, Zhou, Yang, Zhang, Teng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10425512/
https://www.ncbi.nlm.nih.gov/pubmed/37578641
http://dx.doi.org/10.1007/s00018-023-04898-2
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author Shan, Li-Ying
Tian, Yu
Liu, Wen-Xiang
Fan, Hai-Tao
Li, Feng-Guo
Liu, Wen-Juan
Li, Ang
Shen, Wei
Sun, Qing-Yuan
Liu, Yong-Bin
Zhou, Yang
Zhang, Teng
author_facet Shan, Li-Ying
Tian, Yu
Liu, Wen-Xiang
Fan, Hai-Tao
Li, Feng-Guo
Liu, Wen-Juan
Li, Ang
Shen, Wei
Sun, Qing-Yuan
Liu, Yong-Bin
Zhou, Yang
Zhang, Teng
author_sort Shan, Li-Ying
collection PubMed
description Controlled mRNA storage and stability is essential for oocyte meiosis and early embryonic development. However, how to regulate mRNA storage and stability in mammalian oogenesis remains elusive. Here we showed that LSM14B, a component of membraneless compartments including P-body-like granules and mitochondria-associated ribonucleoprotein domain (MARDO) in germ cell, is indispensable for female fertility. To reveal loss of LSM14B disrupted primordial follicle assembly and caused mRNA reduction in non-growing oocytes, which was concomitant with the impaired assembly of P-body-like granules. 10× Genomics single-cell RNA-sequencing and immunostaining were performed. Meanwhile, we conducted RNA-seq analysis of GV-stage oocytes and found that Lsm14b deficiency not only impaired the maternal mRNA accumulation but also disrupted the translation in fully grown oocytes, which was closely associated with dissolution of MARDO components. Moreover, Lsm14b-deficient oocytes reassembled a pronucleus containing decondensed chromatin after extrusion of the first polar body, through compromising the activation of maturation promoting factor, while the defects were restored via WEE1/2 inhibitor. Together, our findings reveal that Lsm14b plays a pivotal role in mammalian oogenesis by specifically controlling of oocyte mRNA storage and stability. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00018-023-04898-2.
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spelling pubmed-104255122023-08-16 LSM14B controls oocyte mRNA storage and stability to ensure female fertility Shan, Li-Ying Tian, Yu Liu, Wen-Xiang Fan, Hai-Tao Li, Feng-Guo Liu, Wen-Juan Li, Ang Shen, Wei Sun, Qing-Yuan Liu, Yong-Bin Zhou, Yang Zhang, Teng Cell Mol Life Sci Original Article Controlled mRNA storage and stability is essential for oocyte meiosis and early embryonic development. However, how to regulate mRNA storage and stability in mammalian oogenesis remains elusive. Here we showed that LSM14B, a component of membraneless compartments including P-body-like granules and mitochondria-associated ribonucleoprotein domain (MARDO) in germ cell, is indispensable for female fertility. To reveal loss of LSM14B disrupted primordial follicle assembly and caused mRNA reduction in non-growing oocytes, which was concomitant with the impaired assembly of P-body-like granules. 10× Genomics single-cell RNA-sequencing and immunostaining were performed. Meanwhile, we conducted RNA-seq analysis of GV-stage oocytes and found that Lsm14b deficiency not only impaired the maternal mRNA accumulation but also disrupted the translation in fully grown oocytes, which was closely associated with dissolution of MARDO components. Moreover, Lsm14b-deficient oocytes reassembled a pronucleus containing decondensed chromatin after extrusion of the first polar body, through compromising the activation of maturation promoting factor, while the defects were restored via WEE1/2 inhibitor. Together, our findings reveal that Lsm14b plays a pivotal role in mammalian oogenesis by specifically controlling of oocyte mRNA storage and stability. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00018-023-04898-2. Springer International Publishing 2023-08-14 2023 /pmc/articles/PMC10425512/ /pubmed/37578641 http://dx.doi.org/10.1007/s00018-023-04898-2 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Shan, Li-Ying
Tian, Yu
Liu, Wen-Xiang
Fan, Hai-Tao
Li, Feng-Guo
Liu, Wen-Juan
Li, Ang
Shen, Wei
Sun, Qing-Yuan
Liu, Yong-Bin
Zhou, Yang
Zhang, Teng
LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title_full LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title_fullStr LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title_full_unstemmed LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title_short LSM14B controls oocyte mRNA storage and stability to ensure female fertility
title_sort lsm14b controls oocyte mrna storage and stability to ensure female fertility
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10425512/
https://www.ncbi.nlm.nih.gov/pubmed/37578641
http://dx.doi.org/10.1007/s00018-023-04898-2
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