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The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition

Metazoan embryos undergo a maternal-to-zygotic transition (MZT) during which maternal gene products are eliminated and the zygotic genome becomes transcriptionally active. During this process, RNA-binding proteins (RBPs) and the microRNA-induced silencing complex (miRISC) target maternal mRNAs for d...

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Autores principales: Luo, Hua, Li, Xiao, Claycomb, Julie M., Lipshitz, Howard D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Genetics Society of America 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100853/
https://www.ncbi.nlm.nih.gov/pubmed/27591754
http://dx.doi.org/10.1534/g3.116.034199
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author Luo, Hua
Li, Xiao
Claycomb, Julie M.
Lipshitz, Howard D.
author_facet Luo, Hua
Li, Xiao
Claycomb, Julie M.
Lipshitz, Howard D.
author_sort Luo, Hua
collection PubMed
description Metazoan embryos undergo a maternal-to-zygotic transition (MZT) during which maternal gene products are eliminated and the zygotic genome becomes transcriptionally active. During this process, RNA-binding proteins (RBPs) and the microRNA-induced silencing complex (miRISC) target maternal mRNAs for degradation. In Drosophila, the Smaug (SMG), Brain tumor (BRAT), and Pumilio (PUM) RBPs bind to and direct the degradation of largely distinct subsets of maternal mRNAs. SMG has also been shown to be required for zygotic synthesis of mRNAs and several members of the miR-309 family of microRNAs (miRNAs) during the MZT. Here, we have carried out global analysis of small RNAs both in wild-type and in smg mutants. Our results show that 85% of all miRNA species encoded by the genome are present during the MZT. Whereas loss of SMG has no detectable effect on Piwi-interacting RNAs (piRNAs) or small interfering RNAs (siRNAs), zygotic production of more than 70 species of miRNAs fails or is delayed in smg mutants. SMG is also required for the synthesis and stability of a key miRISC component, Argonaute 1 (AGO1), but plays no role in accumulation of the Argonaute family proteins associated with piRNAs or siRNAs. In smg mutants, maternal mRNAs that are predicted targets of the SMG-dependent zygotic miRNAs fail to be cleared. BRAT and PUM share target mRNAs with these miRNAs but not with SMG itself. We hypothesize that SMG controls the MZT, not only through direct targeting of a subset of maternal mRNAs for degradation but, indirectly, through production and function of miRNAs and miRISC, which act together with BRAT and/or PUM to control clearance of a distinct subset of maternal mRNAs.
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spelling pubmed-51008532016-11-09 The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition Luo, Hua Li, Xiao Claycomb, Julie M. Lipshitz, Howard D. G3 (Bethesda) Investigations Metazoan embryos undergo a maternal-to-zygotic transition (MZT) during which maternal gene products are eliminated and the zygotic genome becomes transcriptionally active. During this process, RNA-binding proteins (RBPs) and the microRNA-induced silencing complex (miRISC) target maternal mRNAs for degradation. In Drosophila, the Smaug (SMG), Brain tumor (BRAT), and Pumilio (PUM) RBPs bind to and direct the degradation of largely distinct subsets of maternal mRNAs. SMG has also been shown to be required for zygotic synthesis of mRNAs and several members of the miR-309 family of microRNAs (miRNAs) during the MZT. Here, we have carried out global analysis of small RNAs both in wild-type and in smg mutants. Our results show that 85% of all miRNA species encoded by the genome are present during the MZT. Whereas loss of SMG has no detectable effect on Piwi-interacting RNAs (piRNAs) or small interfering RNAs (siRNAs), zygotic production of more than 70 species of miRNAs fails or is delayed in smg mutants. SMG is also required for the synthesis and stability of a key miRISC component, Argonaute 1 (AGO1), but plays no role in accumulation of the Argonaute family proteins associated with piRNAs or siRNAs. In smg mutants, maternal mRNAs that are predicted targets of the SMG-dependent zygotic miRNAs fail to be cleared. BRAT and PUM share target mRNAs with these miRNAs but not with SMG itself. We hypothesize that SMG controls the MZT, not only through direct targeting of a subset of maternal mRNAs for degradation but, indirectly, through production and function of miRNAs and miRISC, which act together with BRAT and/or PUM to control clearance of a distinct subset of maternal mRNAs. Genetics Society of America 2016-09-01 /pmc/articles/PMC5100853/ /pubmed/27591754 http://dx.doi.org/10.1534/g3.116.034199 Text en Copyright © 2016 Luo et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigations
Luo, Hua
Li, Xiao
Claycomb, Julie M.
Lipshitz, Howard D.
The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title_full The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title_fullStr The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title_full_unstemmed The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title_short The Smaug RNA-Binding Protein Is Essential for microRNA Synthesis During the Drosophila Maternal-to-Zygotic Transition
title_sort smaug rna-binding protein is essential for microrna synthesis during the drosophila maternal-to-zygotic transition
topic Investigations
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100853/
https://www.ncbi.nlm.nih.gov/pubmed/27591754
http://dx.doi.org/10.1534/g3.116.034199
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