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Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos

BACKGROUND: Long non-coding RNAs (lncRNAs), a type of epigenetic regulator, are thought to play important roles in embryonic development in mice, and several developmental defects are associated with epigenetic modification disorders. The most dramatic epigenetic reprogramming event occurs during so...

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Autores principales: Wu, Fengrui, Liu, Yong, Wu, Qingqing, Li, Dengkun, Zhang, Ling, Wu, Xiaoqing, Wang, Rong, Zhang, Di, Gao, Shaorong, Li, Wenyong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107955/
https://www.ncbi.nlm.nih.gov/pubmed/30139326
http://dx.doi.org/10.1186/s12864-018-5021-2
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author Wu, Fengrui
Liu, Yong
Wu, Qingqing
Li, Dengkun
Zhang, Ling
Wu, Xiaoqing
Wang, Rong
Zhang, Di
Gao, Shaorong
Li, Wenyong
author_facet Wu, Fengrui
Liu, Yong
Wu, Qingqing
Li, Dengkun
Zhang, Ling
Wu, Xiaoqing
Wang, Rong
Zhang, Di
Gao, Shaorong
Li, Wenyong
author_sort Wu, Fengrui
collection PubMed
description BACKGROUND: Long non-coding RNAs (lncRNAs), a type of epigenetic regulator, are thought to play important roles in embryonic development in mice, and several developmental defects are associated with epigenetic modification disorders. The most dramatic epigenetic reprogramming event occurs during somatic cell nuclear transfer (SCNT) when the expression profile of a differentiated cell is abolished, and a newly embryo-specific expression profile is established. However, the molecular mechanism underlying somatic reprogramming remains unclear, and the dynamics and functions of lncRNAs in this process have not yet been illustrated, resulting in inefficient reprogramming. RESULTS: In this study, 63 single-cell RNA-seq libraries were first generated and sequenced. A total of 7009 mouse polyadenylation lncRNAs (including 5204 novel lncRNAs) were obtained, and a comprehensive analysis of in vivo and SCNT mouse pre-implantation embryo lncRNAs was further performed based on our single-cell RNA sequencing data. Expression profile analysis revealed that lncRNAs were expressed in a developmental stage-specific manner during mouse early-stage embryonic development, whereas a more temporal and spatially specific expression pattern was identified in mouse SCNT embryos with changes in the state of chromatin during somatic cell reprogramming, leading to incomplete zygotic genome activation, oocyte to embryo transition and 2-cell to 4-cell transition. No obvious differences between other stages and mouse NTC or NTM embryos at the same stage were observed. Gene oncology (GO) enrichment analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis and weighted gene co-expression network analysis (WGCNA) of lncRNAs and their association with known protein-coding genes suggested that several lncRNAs and their associated with known protein-coding genes might be involved in mouse embryonic development and cell reprogramming. CONCLUSIONS: This is a novel report on the expression landscapes of lncRNAs of mouse NT embryos by scRNA-seq analysis. This study will provide insight into the molecular mechanism underlying the involvement of lncRNAs in mouse pre-implantation embryonic development and epigenetic reprogramming in mammalian species after SCNT-based cloning. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5021-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-61079552018-08-29 Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos Wu, Fengrui Liu, Yong Wu, Qingqing Li, Dengkun Zhang, Ling Wu, Xiaoqing Wang, Rong Zhang, Di Gao, Shaorong Li, Wenyong BMC Genomics Database BACKGROUND: Long non-coding RNAs (lncRNAs), a type of epigenetic regulator, are thought to play important roles in embryonic development in mice, and several developmental defects are associated with epigenetic modification disorders. The most dramatic epigenetic reprogramming event occurs during somatic cell nuclear transfer (SCNT) when the expression profile of a differentiated cell is abolished, and a newly embryo-specific expression profile is established. However, the molecular mechanism underlying somatic reprogramming remains unclear, and the dynamics and functions of lncRNAs in this process have not yet been illustrated, resulting in inefficient reprogramming. RESULTS: In this study, 63 single-cell RNA-seq libraries were first generated and sequenced. A total of 7009 mouse polyadenylation lncRNAs (including 5204 novel lncRNAs) were obtained, and a comprehensive analysis of in vivo and SCNT mouse pre-implantation embryo lncRNAs was further performed based on our single-cell RNA sequencing data. Expression profile analysis revealed that lncRNAs were expressed in a developmental stage-specific manner during mouse early-stage embryonic development, whereas a more temporal and spatially specific expression pattern was identified in mouse SCNT embryos with changes in the state of chromatin during somatic cell reprogramming, leading to incomplete zygotic genome activation, oocyte to embryo transition and 2-cell to 4-cell transition. No obvious differences between other stages and mouse NTC or NTM embryos at the same stage were observed. Gene oncology (GO) enrichment analysis, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis and weighted gene co-expression network analysis (WGCNA) of lncRNAs and their association with known protein-coding genes suggested that several lncRNAs and their associated with known protein-coding genes might be involved in mouse embryonic development and cell reprogramming. CONCLUSIONS: This is a novel report on the expression landscapes of lncRNAs of mouse NT embryos by scRNA-seq analysis. This study will provide insight into the molecular mechanism underlying the involvement of lncRNAs in mouse pre-implantation embryonic development and epigenetic reprogramming in mammalian species after SCNT-based cloning. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5021-2) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-23 /pmc/articles/PMC6107955/ /pubmed/30139326 http://dx.doi.org/10.1186/s12864-018-5021-2 Text en © The Author(s). 2018 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 Database
Wu, Fengrui
Liu, Yong
Wu, Qingqing
Li, Dengkun
Zhang, Ling
Wu, Xiaoqing
Wang, Rong
Zhang, Di
Gao, Shaorong
Li, Wenyong
Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title_full Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title_fullStr Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title_full_unstemmed Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title_short Long non-coding RNAs potentially function synergistically in the cellular reprogramming of SCNT embryos
title_sort long non-coding rnas potentially function synergistically in the cellular reprogramming of scnt embryos
topic Database
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107955/
https://www.ncbi.nlm.nih.gov/pubmed/30139326
http://dx.doi.org/10.1186/s12864-018-5021-2
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