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Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish

Early embryogenesis relies on maternally inherited mRNAs. Although the mechanism of maternal mRNA degradation during maternal-to-zygotic transition (MZT) has been extensively studied in vertebrates, how the embryos maintain maternal mRNA stability remains unclear. Here, we identify Igf2bp3 as an imp...

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Autores principales: Ren, Fan, Lin, Qiaohong, Gong, Gaorui, Du, Xian, Dan, Hong, Qin, Wenying, Miao, Ran, Xiong, Yang, Xiao, Rui, Li, Xiaohui, Gui, Jian-Fang, Mei, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7054421/
https://www.ncbi.nlm.nih.gov/pubmed/32127635
http://dx.doi.org/10.1038/s42003-020-0827-2
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author Ren, Fan
Lin, Qiaohong
Gong, Gaorui
Du, Xian
Dan, Hong
Qin, Wenying
Miao, Ran
Xiong, Yang
Xiao, Rui
Li, Xiaohui
Gui, Jian-Fang
Mei, Jie
author_facet Ren, Fan
Lin, Qiaohong
Gong, Gaorui
Du, Xian
Dan, Hong
Qin, Wenying
Miao, Ran
Xiong, Yang
Xiao, Rui
Li, Xiaohui
Gui, Jian-Fang
Mei, Jie
author_sort Ren, Fan
collection PubMed
description Early embryogenesis relies on maternally inherited mRNAs. Although the mechanism of maternal mRNA degradation during maternal-to-zygotic transition (MZT) has been extensively studied in vertebrates, how the embryos maintain maternal mRNA stability remains unclear. Here, we identify Igf2bp3 as an important regulator of maternal mRNA stability in zebrafish. Depletion of maternal igf2bp3 destabilizes maternal mRNAs prior to MZT and leads to severe developmental defects, including abnormal cytoskeleton organization and cell division. However, the process of oogenesis and the expression levels of maternal mRNAs in unfertilized eggs are normal in maternal igf2bp3 mutants. Gene ontology analysis revealed that these functions are largely mediated by Igf2bp3-bound mRNAs. Indeed, Igf2bp3 depletion destabilizes while its overexpression enhances its targeting maternal mRNAs. Interestingly, igf2bp3 overexpression in wild-type embryos also causes a developmental delay. Altogether, these findings highlight an important function of Igf2bp3 in controlling early zebrafish embryogenesis by binding and regulating the stability of maternal mRNAs.
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spelling pubmed-70544212020-03-19 Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish Ren, Fan Lin, Qiaohong Gong, Gaorui Du, Xian Dan, Hong Qin, Wenying Miao, Ran Xiong, Yang Xiao, Rui Li, Xiaohui Gui, Jian-Fang Mei, Jie Commun Biol Article Early embryogenesis relies on maternally inherited mRNAs. Although the mechanism of maternal mRNA degradation during maternal-to-zygotic transition (MZT) has been extensively studied in vertebrates, how the embryos maintain maternal mRNA stability remains unclear. Here, we identify Igf2bp3 as an important regulator of maternal mRNA stability in zebrafish. Depletion of maternal igf2bp3 destabilizes maternal mRNAs prior to MZT and leads to severe developmental defects, including abnormal cytoskeleton organization and cell division. However, the process of oogenesis and the expression levels of maternal mRNAs in unfertilized eggs are normal in maternal igf2bp3 mutants. Gene ontology analysis revealed that these functions are largely mediated by Igf2bp3-bound mRNAs. Indeed, Igf2bp3 depletion destabilizes while its overexpression enhances its targeting maternal mRNAs. Interestingly, igf2bp3 overexpression in wild-type embryos also causes a developmental delay. Altogether, these findings highlight an important function of Igf2bp3 in controlling early zebrafish embryogenesis by binding and regulating the stability of maternal mRNAs. Nature Publishing Group UK 2020-03-03 /pmc/articles/PMC7054421/ /pubmed/32127635 http://dx.doi.org/10.1038/s42003-020-0827-2 Text en © The Author(s) 2020 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Ren, Fan
Lin, Qiaohong
Gong, Gaorui
Du, Xian
Dan, Hong
Qin, Wenying
Miao, Ran
Xiong, Yang
Xiao, Rui
Li, Xiaohui
Gui, Jian-Fang
Mei, Jie
Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title_full Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title_fullStr Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title_full_unstemmed Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title_short Igf2bp3 maintains maternal RNA stability and ensures early embryo development in zebrafish
title_sort igf2bp3 maintains maternal rna stability and ensures early embryo development in zebrafish
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7054421/
https://www.ncbi.nlm.nih.gov/pubmed/32127635
http://dx.doi.org/10.1038/s42003-020-0827-2
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