MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae

BACKGROUND: MicroRNAs (miRNAs) are critical regulators responding to acute environmental stresses in both plants and animals. By modulating gene expression, miRNAs either restore or reconstitute a new expression program to enhance cell tolerance to stresses. Cold shock is one of the stresses that ca...

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Autores principales: Hung, I-Chen, Hsiao, Yu-Chuan, Sun, H. Sunny, Chen, Tsung-Ming, Lee, Shyh-Jye
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5111229/
https://www.ncbi.nlm.nih.gov/pubmed/27846817
http://dx.doi.org/10.1186/s12864-016-3239-4
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author Hung, I-Chen
Hsiao, Yu-Chuan
Sun, H. Sunny
Chen, Tsung-Ming
Lee, Shyh-Jye
author_facet Hung, I-Chen
Hsiao, Yu-Chuan
Sun, H. Sunny
Chen, Tsung-Ming
Lee, Shyh-Jye
author_sort Hung, I-Chen
collection PubMed
description BACKGROUND: MicroRNAs (miRNAs) are critical regulators responding to acute environmental stresses in both plants and animals. By modulating gene expression, miRNAs either restore or reconstitute a new expression program to enhance cell tolerance to stresses. Cold shock is one of the stresses that can induce acute physiological responses and transcriptional changes in aquatic creatures. Previous genomic studies have revealed many cold-affected genes in fish larvae and adults, however, the role of miRNAs in acute cold response is still ambiguous. To elucidate the regulatory roles of miRNAs in the cold-inducible responses, we performed small RNA-seq and RNA-seq analyses and found potential cold regulatory miRNAs and genes. We further investigated their interactions and involvements in cold tolerance. RESULTS: Small RNA-seq and RNA-seq identified 29 up-/26 down-regulated miRNAs and 908 up-/468 down-regulated genes, respectively, in responding to cold shock for 4 h at 18 °C. miRNA and transcriptomic analyses showed these miRNAs and mRNAs are involved in similar biological processes and pathways. Gene ontology enrichment analyses revealed the cold-induced genes were enriched in pathways, including melanogenesis, GnRH pathway, circadian rhythm, etc. We were particularly interested in the changes in circadian clock genes that affect daily metabolism. The enrichment of circadian clock genes was also observed in previous fish cold acclimation studies, but have not been characterized. To characterize the functional roles of circadian clock genes in cold tolerance, we individually overexpressed selected clock genes in zebrafish larvae and found one of the core clock genes per2 resulted in better recovery from cold shock. In addition, we validated the interaction of per2 with its associate miRNA, dre-mir-29b, which is also cold-inducible. It suggests the transcription of per2 can be modulated by miRNA upon cold shock. CONCLUSIONS: Collectively, our observations suggest that miRNAs are fine turners for regulating genomic plasticity against cold shock. We further showed that the fine tuning of core clock gene per2 via its associated miRNA, dre-mir-29b, can enhance the cold tolerance of zebrafish larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3239-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-51112292016-11-21 MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae Hung, I-Chen Hsiao, Yu-Chuan Sun, H. Sunny Chen, Tsung-Ming Lee, Shyh-Jye BMC Genomics Research Article BACKGROUND: MicroRNAs (miRNAs) are critical regulators responding to acute environmental stresses in both plants and animals. By modulating gene expression, miRNAs either restore or reconstitute a new expression program to enhance cell tolerance to stresses. Cold shock is one of the stresses that can induce acute physiological responses and transcriptional changes in aquatic creatures. Previous genomic studies have revealed many cold-affected genes in fish larvae and adults, however, the role of miRNAs in acute cold response is still ambiguous. To elucidate the regulatory roles of miRNAs in the cold-inducible responses, we performed small RNA-seq and RNA-seq analyses and found potential cold regulatory miRNAs and genes. We further investigated their interactions and involvements in cold tolerance. RESULTS: Small RNA-seq and RNA-seq identified 29 up-/26 down-regulated miRNAs and 908 up-/468 down-regulated genes, respectively, in responding to cold shock for 4 h at 18 °C. miRNA and transcriptomic analyses showed these miRNAs and mRNAs are involved in similar biological processes and pathways. Gene ontology enrichment analyses revealed the cold-induced genes were enriched in pathways, including melanogenesis, GnRH pathway, circadian rhythm, etc. We were particularly interested in the changes in circadian clock genes that affect daily metabolism. The enrichment of circadian clock genes was also observed in previous fish cold acclimation studies, but have not been characterized. To characterize the functional roles of circadian clock genes in cold tolerance, we individually overexpressed selected clock genes in zebrafish larvae and found one of the core clock genes per2 resulted in better recovery from cold shock. In addition, we validated the interaction of per2 with its associate miRNA, dre-mir-29b, which is also cold-inducible. It suggests the transcription of per2 can be modulated by miRNA upon cold shock. CONCLUSIONS: Collectively, our observations suggest that miRNAs are fine turners for regulating genomic plasticity against cold shock. We further showed that the fine tuning of core clock gene per2 via its associated miRNA, dre-mir-29b, can enhance the cold tolerance of zebrafish larvae. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-016-3239-4) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-15 /pmc/articles/PMC5111229/ /pubmed/27846817 http://dx.doi.org/10.1186/s12864-016-3239-4 Text en © The Author(s). 2016 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 Article
Hung, I-Chen
Hsiao, Yu-Chuan
Sun, H. Sunny
Chen, Tsung-Ming
Lee, Shyh-Jye
MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title_full MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title_fullStr MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title_full_unstemmed MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title_short MicroRNAs regulate gene plasticity during cold shock in zebrafish larvae
title_sort micrornas regulate gene plasticity during cold shock in zebrafish larvae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5111229/
https://www.ncbi.nlm.nih.gov/pubmed/27846817
http://dx.doi.org/10.1186/s12864-016-3239-4
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