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MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans

Considering complicated microRNA (miRNA) biogenesis and action mechanisms, it was thought so high energy-consuming for a cell to afford simultaneous over-expression of many miRNAs. Thus it prompts that an alternative miRNA regulation pattern on protein-encoding genes must exist, which has characteri...

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Autores principales: Chen, Xue, Zhao, Wei, Yuan, Ye, Bai, Yan, Sun, Yong, Zhu, Wenliang, Du, Zhimin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5560240/
https://www.ncbi.nlm.nih.gov/pubmed/28828274
http://dx.doi.org/10.7717/peerj.3682
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author Chen, Xue
Zhao, Wei
Yuan, Ye
Bai, Yan
Sun, Yong
Zhu, Wenliang
Du, Zhimin
author_facet Chen, Xue
Zhao, Wei
Yuan, Ye
Bai, Yan
Sun, Yong
Zhu, Wenliang
Du, Zhimin
author_sort Chen, Xue
collection PubMed
description Considering complicated microRNA (miRNA) biogenesis and action mechanisms, it was thought so high energy-consuming for a cell to afford simultaneous over-expression of many miRNAs. Thus it prompts that an alternative miRNA regulation pattern on protein-encoding genes must exist, which has characteristics of energy-saving and precise protein output. In this study, expression tendency of proteins encoded by miRNAs’ target genes was evaluated in human organ scale, followed by quantitative assessment of miRNA synergism. Expression tendency analysis suggests that universally expressed proteins (UEPs) tend to physically interact in clusters and participate in fundamental biological activities whereas disorderly expressed proteins (DEPs) are inclined to relatively independently execute organ-specific functions. Consistent with this, miRNAs that mainly target UEP-encoding mRNAs, such as miR-21, tend to collaboratively or even synergistically act with other miRNAs in fine-tuning protein output. Synergistic gene regulation may maximize miRNAs’ efficiency with less dependence on miRNAs’ abundance and overcome the deficiency that targeting plenty of genes by single miRNA makes miRNA-mediated regulation high-throughput but insufficient due to target gene dilution effect. Furthermore, our in vitro experiment verified that merely 25 nM transfection of miR-21 be sufficient to influence the overall state of various human cells. Thus miR-21 was identified as a hub in synergistic miRNA–miRNA interaction network. Our findings suggest that synergistic miRNA–miRNA interaction is an important endogenous miRNA regulation mode, which ensures adequate potency of miRNAs at low abundance, especially those implicated in fundamental biological regulation.
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spelling pubmed-55602402017-08-21 MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans Chen, Xue Zhao, Wei Yuan, Ye Bai, Yan Sun, Yong Zhu, Wenliang Du, Zhimin PeerJ Bioinformatics Considering complicated microRNA (miRNA) biogenesis and action mechanisms, it was thought so high energy-consuming for a cell to afford simultaneous over-expression of many miRNAs. Thus it prompts that an alternative miRNA regulation pattern on protein-encoding genes must exist, which has characteristics of energy-saving and precise protein output. In this study, expression tendency of proteins encoded by miRNAs’ target genes was evaluated in human organ scale, followed by quantitative assessment of miRNA synergism. Expression tendency analysis suggests that universally expressed proteins (UEPs) tend to physically interact in clusters and participate in fundamental biological activities whereas disorderly expressed proteins (DEPs) are inclined to relatively independently execute organ-specific functions. Consistent with this, miRNAs that mainly target UEP-encoding mRNAs, such as miR-21, tend to collaboratively or even synergistically act with other miRNAs in fine-tuning protein output. Synergistic gene regulation may maximize miRNAs’ efficiency with less dependence on miRNAs’ abundance and overcome the deficiency that targeting plenty of genes by single miRNA makes miRNA-mediated regulation high-throughput but insufficient due to target gene dilution effect. Furthermore, our in vitro experiment verified that merely 25 nM transfection of miR-21 be sufficient to influence the overall state of various human cells. Thus miR-21 was identified as a hub in synergistic miRNA–miRNA interaction network. Our findings suggest that synergistic miRNA–miRNA interaction is an important endogenous miRNA regulation mode, which ensures adequate potency of miRNAs at low abundance, especially those implicated in fundamental biological regulation. PeerJ Inc. 2017-08-14 /pmc/articles/PMC5560240/ /pubmed/28828274 http://dx.doi.org/10.7717/peerj.3682 Text en ©2017 Chen et al. http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Bioinformatics
Chen, Xue
Zhao, Wei
Yuan, Ye
Bai, Yan
Sun, Yong
Zhu, Wenliang
Du, Zhimin
MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title_full MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title_fullStr MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title_full_unstemmed MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title_short MicroRNAs tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
title_sort micrornas tend to synergistically control expression of genes encoding extensively-expressed proteins in humans
topic Bioinformatics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5560240/
https://www.ncbi.nlm.nih.gov/pubmed/28828274
http://dx.doi.org/10.7717/peerj.3682
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