MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells
Abstract 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, re...
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| Format: | Article |
| Language: | English |
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BMC
2017-06-01
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| Series: | Genome Biology |
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| Online Access: | http://link.springer.com/article/10.1186/s13059-017-1243-x |
| _version_ | 1811325457009737728 |
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| author | Ying Zhang Chong Tang Tian Yu Ruirui Zhang Huili Zheng Wei Yan |
| author_facet | Ying Zhang Chong Tang Tian Yu Ruirui Zhang Huili Zheng Wei Yan |
| author_sort | Ying Zhang |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-13T14:34:39Z |
| format | Article |
| id | doaj.art-2a79ca2961134fd4ac3773dd6ce55566 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-13T14:34:39Z |
| publishDate | 2017-06-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-2a79ca2961134fd4ac3773dd6ce555662022-12-22T02:43:05ZengBMCGenome Biology1474-760X2017-06-0118111810.1186/s13059-017-1243-xMicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cellsYing Zhang0Chong Tang1Tian Yu2Ruirui Zhang3Huili Zheng4Wei Yan5Department of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Center for Molecular MedicineDepartment of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Center for Molecular MedicineDepartment of Biology, University of NevadaDepartment of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Center for Molecular MedicineDepartment of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Center for Molecular MedicineDepartment of Physiology and Cell Biology, University of Nevada, Reno School of Medicine, Center for Molecular MedicineAbstract 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.http://link.springer.com/article/10.1186/s13059-017-1243-xSmall RNAmiRNA3′ UTR lengthDelayed translationmRNA fateGerm cell |
| spellingShingle | Ying Zhang Chong Tang Tian Yu Ruirui Zhang Huili Zheng Wei Yan MicroRNAs control mRNA fate by compartmentalization based on 3′ UTR length in male germ cells Genome Biology Small RNA miRNA 3′ UTR length Delayed translation mRNA fate Germ cell |
| 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 | Small RNA miRNA 3′ UTR length Delayed translation mRNA fate Germ cell |
| url | http://link.springer.com/article/10.1186/s13059-017-1243-x |
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