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Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species

BACKGROUND: The transcriptional changes around zygotic genome activation (ZGA) in preimplantation embryos are critical for studying mechanisms of embryonic developmental arrest and searching for key transcription factors. However, studies on the transcription profile of porcine ZGA are limited. RESU...

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Autores principales: Zhai, Yanhui, Yu, Hao, An, Xinglan, Zhang, Zhiren, Zhang, Meng, Zhang, Sheng, Li, Qi, Li, Ziyi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9700911/
https://www.ncbi.nlm.nih.gov/pubmed/36434523
http://dx.doi.org/10.1186/s12864-022-09015-4
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author Zhai, Yanhui
Yu, Hao
An, Xinglan
Zhang, Zhiren
Zhang, Meng
Zhang, Sheng
Li, Qi
Li, Ziyi
author_facet Zhai, Yanhui
Yu, Hao
An, Xinglan
Zhang, Zhiren
Zhang, Meng
Zhang, Sheng
Li, Qi
Li, Ziyi
author_sort Zhai, Yanhui
collection PubMed
description BACKGROUND: The transcriptional changes around zygotic genome activation (ZGA) in preimplantation embryos are critical for studying mechanisms of embryonic developmental arrest and searching for key transcription factors. However, studies on the transcription profile of porcine ZGA are limited. RESULTS: In this study, we performed RNA sequencing in porcine in vivo developed (IVV) and somatic cell nuclear transfer (SCNT) embryo at different stages and compared the transcriptional activity of porcine embryos with mouse, bovine and human embryos. The results showed that the transcriptome map of the early porcine embryos was significantly changed at the 4-cell stage, and 5821 differentially expressed genes (DEGs) in SCNT embryos failed to be reprogrammed or activated during ZGA, which mainly enrichment to metabolic pathways. c-MYC was identified as the highest expressed transcription factor during ZGA. By treating with 10,058-F4, an inhibitor of c-MYC, the cleavage rate (38.33 ± 3.4%) and blastocyst rate (23.33 ± 4.3%) of porcine embryos were significantly lower than those of the control group (50.82 ± 2.7% and 34.43 ± 1.9%). Cross-species analysis of transcriptome during ZGA showed that pigs and bovines had the highest similarity coefficient in biological processes. KEGG pathway analysis indicated that there were 10 co-shared pathways in the four species. CONCLUSIONS: Our results reveal that embryos with impaired developmental competence may be arrested at an early stage of development. c-MYC helps promote ZGA and preimplantation embryonic development in pigs. Pigs and bovines have the highest coefficient of similarity in biological processes during ZGA. This study provides an important reference for further studying the reprogramming regulatory mechanism of porcine embryos during ZGA. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-09015-4.
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spelling pubmed-97009112022-11-27 Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species Zhai, Yanhui Yu, Hao An, Xinglan Zhang, Zhiren Zhang, Meng Zhang, Sheng Li, Qi Li, Ziyi BMC Genomics Research BACKGROUND: The transcriptional changes around zygotic genome activation (ZGA) in preimplantation embryos are critical for studying mechanisms of embryonic developmental arrest and searching for key transcription factors. However, studies on the transcription profile of porcine ZGA are limited. RESULTS: In this study, we performed RNA sequencing in porcine in vivo developed (IVV) and somatic cell nuclear transfer (SCNT) embryo at different stages and compared the transcriptional activity of porcine embryos with mouse, bovine and human embryos. The results showed that the transcriptome map of the early porcine embryos was significantly changed at the 4-cell stage, and 5821 differentially expressed genes (DEGs) in SCNT embryos failed to be reprogrammed or activated during ZGA, which mainly enrichment to metabolic pathways. c-MYC was identified as the highest expressed transcription factor during ZGA. By treating with 10,058-F4, an inhibitor of c-MYC, the cleavage rate (38.33 ± 3.4%) and blastocyst rate (23.33 ± 4.3%) of porcine embryos were significantly lower than those of the control group (50.82 ± 2.7% and 34.43 ± 1.9%). Cross-species analysis of transcriptome during ZGA showed that pigs and bovines had the highest similarity coefficient in biological processes. KEGG pathway analysis indicated that there were 10 co-shared pathways in the four species. CONCLUSIONS: Our results reveal that embryos with impaired developmental competence may be arrested at an early stage of development. c-MYC helps promote ZGA and preimplantation embryonic development in pigs. Pigs and bovines have the highest coefficient of similarity in biological processes during ZGA. This study provides an important reference for further studying the reprogramming regulatory mechanism of porcine embryos during ZGA. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-09015-4. BioMed Central 2022-11-24 /pmc/articles/PMC9700911/ /pubmed/36434523 http://dx.doi.org/10.1186/s12864-022-09015-4 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
Zhai, Yanhui
Yu, Hao
An, Xinglan
Zhang, Zhiren
Zhang, Meng
Zhang, Sheng
Li, Qi
Li, Ziyi
Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title_full Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title_fullStr Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title_full_unstemmed Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title_short Profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
title_sort profiling the transcriptomic signatures and identifying the patterns of zygotic genome activation – a comparative analysis between early porcine embryos and their counterparts in other three mammalian species
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9700911/
https://www.ncbi.nlm.nih.gov/pubmed/36434523
http://dx.doi.org/10.1186/s12864-022-09015-4
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