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Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition

Maternal messenger ribonucleic acids (mRNAs) are driven by a highly orchestrated scheme of recruitment to polysomes and translational activation. However, selecting and regulating individual mRNAs for the translation from a competitive pool of mRNAs are little‐known processes. This research shows th...

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Autores principales: Guo, Jing, Zhao, Hailian, Zhang, Jue, Lv, Xiangjiang, Zhang, Shen, Su, Ruibao, Zheng, Wei, Dai, Jing, Meng, Fei, Gong, Fei, Lu, Guangxiu, Xue, Yuanchao, Lin, Ge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104655/
https://www.ncbi.nlm.nih.gov/pubmed/36755190
http://dx.doi.org/10.1002/advs.202205500
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author Guo, Jing
Zhao, Hailian
Zhang, Jue
Lv, Xiangjiang
Zhang, Shen
Su, Ruibao
Zheng, Wei
Dai, Jing
Meng, Fei
Gong, Fei
Lu, Guangxiu
Xue, Yuanchao
Lin, Ge
author_facet Guo, Jing
Zhao, Hailian
Zhang, Jue
Lv, Xiangjiang
Zhang, Shen
Su, Ruibao
Zheng, Wei
Dai, Jing
Meng, Fei
Gong, Fei
Lu, Guangxiu
Xue, Yuanchao
Lin, Ge
author_sort Guo, Jing
collection PubMed
description Maternal messenger ribonucleic acids (mRNAs) are driven by a highly orchestrated scheme of recruitment to polysomes and translational activation. However, selecting and regulating individual mRNAs for the translation from a competitive pool of mRNAs are little‐known processes. This research shows that the maternal eukaryotic translation initiation factor 4e1b (Eif4e1b) expresses during the oocyte‐to‐embryo transition (OET), and maternal deletion of Eif4e1b leads to multiple defects concerning oogenesis and embryonic developmental competence during OET. The linear amplification of complementary deoxyribonucleic acid (cDNA) ends, and sequencing (LACE‐seq) is used to identify the distinct subset of mRNA and its CG‐rich binding sites within the 5′ untranslated region (UTR) targeted by eIF4E1B. The proteomics analyses indicate that eIF4E1B‐specific bound genes show stronger downregulation at the protein level, which further verify a group of proteins that plays a crucial role in oocyte maturation and embryonic developmental competence is insufficiently synthesized in Eif4e1b‐cKO oocytes during OET. Moreover, the biochemical results in vitro are combined to further confirm the maternal‐specific translation activation model assembled by eIF4E1B and 3′UTR‐associated mRNA binding proteins. The findings demonstrate the indispensability of eIF4E1B for selective translation activation in mammalian oocytes and provide a potential network regulated by eIF4E1B in OET.
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spelling pubmed-101046552023-04-15 Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition Guo, Jing Zhao, Hailian Zhang, Jue Lv, Xiangjiang Zhang, Shen Su, Ruibao Zheng, Wei Dai, Jing Meng, Fei Gong, Fei Lu, Guangxiu Xue, Yuanchao Lin, Ge Adv Sci (Weinh) Research Articles Maternal messenger ribonucleic acids (mRNAs) are driven by a highly orchestrated scheme of recruitment to polysomes and translational activation. However, selecting and regulating individual mRNAs for the translation from a competitive pool of mRNAs are little‐known processes. This research shows that the maternal eukaryotic translation initiation factor 4e1b (Eif4e1b) expresses during the oocyte‐to‐embryo transition (OET), and maternal deletion of Eif4e1b leads to multiple defects concerning oogenesis and embryonic developmental competence during OET. The linear amplification of complementary deoxyribonucleic acid (cDNA) ends, and sequencing (LACE‐seq) is used to identify the distinct subset of mRNA and its CG‐rich binding sites within the 5′ untranslated region (UTR) targeted by eIF4E1B. The proteomics analyses indicate that eIF4E1B‐specific bound genes show stronger downregulation at the protein level, which further verify a group of proteins that plays a crucial role in oocyte maturation and embryonic developmental competence is insufficiently synthesized in Eif4e1b‐cKO oocytes during OET. Moreover, the biochemical results in vitro are combined to further confirm the maternal‐specific translation activation model assembled by eIF4E1B and 3′UTR‐associated mRNA binding proteins. The findings demonstrate the indispensability of eIF4E1B for selective translation activation in mammalian oocytes and provide a potential network regulated by eIF4E1B in OET. John Wiley and Sons Inc. 2023-02-08 /pmc/articles/PMC10104655/ /pubmed/36755190 http://dx.doi.org/10.1002/advs.202205500 Text en © 2023 The Authors. Advanced Science published by Wiley‐VCH GmbH 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 Research Articles
Guo, Jing
Zhao, Hailian
Zhang, Jue
Lv, Xiangjiang
Zhang, Shen
Su, Ruibao
Zheng, Wei
Dai, Jing
Meng, Fei
Gong, Fei
Lu, Guangxiu
Xue, Yuanchao
Lin, Ge
Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title_full Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title_fullStr Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title_full_unstemmed Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title_short Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition
title_sort selective translation of maternal mrna by eif4e1b controls oocyte to embryo transition
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104655/
https://www.ncbi.nlm.nih.gov/pubmed/36755190
http://dx.doi.org/10.1002/advs.202205500
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