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MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells

BACKGROUND: Post-transcriptional regulation of gene expression can be achieved through the control of mRNA stability, cytoplasmic compartmentalization, 3′ UTR length and translational efficacy. Spermiogenesis, a process through which haploid male germ cells differentiate into spermatozoa, represents...

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Autores principales: Zhang, Ying, Tang, Chong, Yu, Tian, Zhang, Ruirui, Zheng, Huili, Yan, Wei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5471846/
https://www.ncbi.nlm.nih.gov/pubmed/28615029
http://dx.doi.org/10.1186/s13059-017-1243-x
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author Zhang, Ying
Tang, Chong
Yu, Tian
Zhang, Ruirui
Zheng, Huili
Yan, Wei
author_facet Zhang, Ying
Tang, Chong
Yu, Tian
Zhang, Ruirui
Zheng, Huili
Yan, Wei
author_sort Zhang, Ying
collection PubMed
description BACKGROUND: Post-transcriptional regulation of gene expression can be achieved through the control of mRNA stability, cytoplasmic compartmentalization, 3′ UTR length and translational efficacy. Spermiogenesis, a process through which haploid male germ cells differentiate into spermatozoa, represents an ideal model for studying post-transcriptional regulation in vivo because it involves a large number of transcripts that are physically sequestered in ribonucleoprotein particles (RNPs) and thus subjected to delayed translation. To explore how small RNAs regulate mRNA fate, we conducted RNA-Seq analyses to determine not only the levels of both mRNAs and small noncoding RNAs, but also their cytoplasmic compartmentalization during spermiogenesis. RESULT: Among all small noncoding RNAs studied, miRNAs displayed the most dynamic changes in both abundance and subcytoplasmic localization. mRNAs with shorter 3′ UTRs became increasingly enriched in RNPs from pachytene spermatocytes to round spermatids, and the enrichment of shorter 3′ UTR mRNAs in RNPs coincided with newly synthesized miRNAs that target these mRNAs at sites closer to the stop codon. In contrast, the translocation of longer 3′ UTR mRNAs from RNPs to polysomes correlated with the production of new miRNAs that target these mRNAs at sites distal to the stop codon. CONCLUSIONS: miRNAs appear to control cytoplasmic compartmentalization of mRNAs based on 3′ UTR length. Our data suggest that transcripts with longer 3′ UTRs tend to contain distal miRNA binding sites and are thus targeted to polysomes for translation followed by degradation. In contrast, those with shorter 3′ UTRs only possess proximal miRNA binding sites, which, therefore, are targeted into RNPs for enrichment and delayed translation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-017-1243-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-54718462017-06-19 MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells Zhang, Ying Tang, Chong Yu, Tian Zhang, Ruirui Zheng, Huili Yan, Wei Genome Biol Research BACKGROUND: Post-transcriptional regulation of gene expression can be achieved through the control of mRNA stability, cytoplasmic compartmentalization, 3′ UTR length and translational efficacy. Spermiogenesis, a process through which haploid male germ cells differentiate into spermatozoa, represents an ideal model for studying post-transcriptional regulation in vivo because it involves a large number of transcripts that are physically sequestered in ribonucleoprotein particles (RNPs) and thus subjected to delayed translation. To explore how small RNAs regulate mRNA fate, we conducted RNA-Seq analyses to determine not only the levels of both mRNAs and small noncoding RNAs, but also their cytoplasmic compartmentalization during spermiogenesis. RESULT: Among all small noncoding RNAs studied, miRNAs displayed the most dynamic changes in both abundance and subcytoplasmic localization. mRNAs with shorter 3′ UTRs became increasingly enriched in RNPs from pachytene spermatocytes to round spermatids, and the enrichment of shorter 3′ UTR mRNAs in RNPs coincided with newly synthesized miRNAs that target these mRNAs at sites closer to the stop codon. In contrast, the translocation of longer 3′ UTR mRNAs from RNPs to polysomes correlated with the production of new miRNAs that target these mRNAs at sites distal to the stop codon. CONCLUSIONS: miRNAs appear to control cytoplasmic compartmentalization of mRNAs based on 3′ UTR length. Our data suggest that transcripts with longer 3′ UTRs tend to contain distal miRNA binding sites and are thus targeted to polysomes for translation followed by degradation. In contrast, those with shorter 3′ UTRs only possess proximal miRNA binding sites, which, therefore, are targeted into RNPs for enrichment and delayed translation. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-017-1243-x) contains supplementary material, which is available to authorized users. BioMed Central 2017-06-15 /pmc/articles/PMC5471846/ /pubmed/28615029 http://dx.doi.org/10.1186/s13059-017-1243-x Text en © The Author(s). 2017 Open AccessThis article is 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 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Zhang, Ying
Tang, Chong
Yu, Tian
Zhang, Ruirui
Zheng, Huili
Yan, Wei
MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title_full MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title_fullStr MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title_full_unstemmed MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title_short MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
title_sort micrornas control mrna fate by compartmentalization based on 3′ utr length in male germ cells
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5471846/
https://www.ncbi.nlm.nih.gov/pubmed/28615029
http://dx.doi.org/10.1186/s13059-017-1243-x
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