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Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods

BACKGROUND: The growth and development of skeletal muscle are regulated by protein-coding genes and non-coding RNA. Circular RNA (circRNA) is a type of non-coding RNA involved in a variety of biological processes, especially in post-transcriptional regulation. To better understand the regulatory mec...

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Autores principales: Lei, Qiuxia, Hu, Xin, Han, Haixia, Wang, Jie, Liu, Wei, Zhou, Yan, Cao, Dingguo, Li, Fuwei, Liu, Jie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9063329/
https://www.ncbi.nlm.nih.gov/pubmed/35505302
http://dx.doi.org/10.1186/s12864-022-08525-5
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author Lei, Qiuxia
Hu, Xin
Han, Haixia
Wang, Jie
Liu, Wei
Zhou, Yan
Cao, Dingguo
Li, Fuwei
Liu, Jie
author_facet Lei, Qiuxia
Hu, Xin
Han, Haixia
Wang, Jie
Liu, Wei
Zhou, Yan
Cao, Dingguo
Li, Fuwei
Liu, Jie
author_sort Lei, Qiuxia
collection PubMed
description BACKGROUND: The growth and development of skeletal muscle are regulated by protein-coding genes and non-coding RNA. Circular RNA (circRNA) is a type of non-coding RNA involved in a variety of biological processes, especially in post-transcriptional regulation. To better understand the regulatory mechanism of circRNAs during the development of muscle in chicken, we performed RNA-seq with linear RNA depletion for chicken breast muscle in 12 (E 12) and17 (E 17) day embryos, and 1 (D 1), 14 (D 14), 56 (D 56), and 98 (D 98) days post-hatch. RESULTS: We identified 5755 differentially expressed (DE)-circRNAs during muscle development. We profiled the expression of DE-circRNAs and mRNAs (identified in our previous study) at up to six time points during chicken muscle development and uncovered a significant profile (profile 16) for circRNA upregulation during aging in muscle tissues. To investigate competing endogenous RNA (ceRNA) regulation in muscle and identify muscle-related circRNAs, we constructed a circRNA-miRNA-mRNA regulatory network using the circRNAs and mRNAs from profile 16 and miRNAs identified in our previous study, which included 361 miRNAs, 68 circRNAs, 599 mRNAs, and 31,063 interacting pairs. Functional annotation showed that upregulated circRNAs might contribute to glycolysis/gluconeogenesis, biosynthesis of amino acids, pyruvate metabolism, carbon metabolism, glycogen and sucrose metabolism through the ceRNA network, and thus affected postnatal muscle development by regulating muscle protein deposition. Of them, circRNA225 and circRNA226 from the same host gene might be key circRNAs that could regulate muscle development by interacting with seven common miRNAs and 207 mRNAs. Our experiments also demonstrated that there were interactions among circRNA225, gga-miR-1306-5p, and heat shock protein alpha 8 (HSPA8). CONCLUSIONS: Our results suggest that adequate supply of nutrients such as energy and protein after hatching may be a key factor in ensuring chicken yield, and provide several candidate circRNAs for future studies concerning ceRNA regulation during chicken muscle development. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08525-5.
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spelling pubmed-90633292022-05-04 Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods Lei, Qiuxia Hu, Xin Han, Haixia Wang, Jie Liu, Wei Zhou, Yan Cao, Dingguo Li, Fuwei Liu, Jie BMC Genomics Research BACKGROUND: The growth and development of skeletal muscle are regulated by protein-coding genes and non-coding RNA. Circular RNA (circRNA) is a type of non-coding RNA involved in a variety of biological processes, especially in post-transcriptional regulation. To better understand the regulatory mechanism of circRNAs during the development of muscle in chicken, we performed RNA-seq with linear RNA depletion for chicken breast muscle in 12 (E 12) and17 (E 17) day embryos, and 1 (D 1), 14 (D 14), 56 (D 56), and 98 (D 98) days post-hatch. RESULTS: We identified 5755 differentially expressed (DE)-circRNAs during muscle development. We profiled the expression of DE-circRNAs and mRNAs (identified in our previous study) at up to six time points during chicken muscle development and uncovered a significant profile (profile 16) for circRNA upregulation during aging in muscle tissues. To investigate competing endogenous RNA (ceRNA) regulation in muscle and identify muscle-related circRNAs, we constructed a circRNA-miRNA-mRNA regulatory network using the circRNAs and mRNAs from profile 16 and miRNAs identified in our previous study, which included 361 miRNAs, 68 circRNAs, 599 mRNAs, and 31,063 interacting pairs. Functional annotation showed that upregulated circRNAs might contribute to glycolysis/gluconeogenesis, biosynthesis of amino acids, pyruvate metabolism, carbon metabolism, glycogen and sucrose metabolism through the ceRNA network, and thus affected postnatal muscle development by regulating muscle protein deposition. Of them, circRNA225 and circRNA226 from the same host gene might be key circRNAs that could regulate muscle development by interacting with seven common miRNAs and 207 mRNAs. Our experiments also demonstrated that there were interactions among circRNA225, gga-miR-1306-5p, and heat shock protein alpha 8 (HSPA8). CONCLUSIONS: Our results suggest that adequate supply of nutrients such as energy and protein after hatching may be a key factor in ensuring chicken yield, and provide several candidate circRNAs for future studies concerning ceRNA regulation during chicken muscle development. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08525-5. BioMed Central 2022-05-03 /pmc/articles/PMC9063329/ /pubmed/35505302 http://dx.doi.org/10.1186/s12864-022-08525-5 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lei, Qiuxia
Hu, Xin
Han, Haixia
Wang, Jie
Liu, Wei
Zhou, Yan
Cao, Dingguo
Li, Fuwei
Liu, Jie
Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title_full Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title_fullStr Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title_full_unstemmed Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title_short Integrative analysis of circRNA, miRNA, and mRNA profiles to reveal ceRNA regulation in chicken muscle development from the embryonic to post-hatching periods
title_sort integrative analysis of circrna, mirna, and mrna profiles to reveal cerna regulation in chicken muscle development from the embryonic to post-hatching periods
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9063329/
https://www.ncbi.nlm.nih.gov/pubmed/35505302
http://dx.doi.org/10.1186/s12864-022-08525-5
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