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Transcriptional profiles of bovine in vivo pre-implantation development

BACKGROUND: During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology. RESULTS: Here we report comprehensiv...

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Autores principales: Jiang, Zongliang, Sun, Jiangwen, Dong, Hong, Luo, Oscar, Zheng, Xinbao, Obergfell, Craig, Tang, Yong, Bi, Jinbo, O’Neill, Rachel, Ruan, Yijun, Chen, Jingbo, Tian, Xiuchun (Cindy)
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4162962/
https://www.ncbi.nlm.nih.gov/pubmed/25185836
http://dx.doi.org/10.1186/1471-2164-15-756
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author Jiang, Zongliang
Sun, Jiangwen
Dong, Hong
Luo, Oscar
Zheng, Xinbao
Obergfell, Craig
Tang, Yong
Bi, Jinbo
O’Neill, Rachel
Ruan, Yijun
Chen, Jingbo
Tian, Xiuchun (Cindy)
author_facet Jiang, Zongliang
Sun, Jiangwen
Dong, Hong
Luo, Oscar
Zheng, Xinbao
Obergfell, Craig
Tang, Yong
Bi, Jinbo
O’Neill, Rachel
Ruan, Yijun
Chen, Jingbo
Tian, Xiuchun (Cindy)
author_sort Jiang, Zongliang
collection PubMed
description BACKGROUND: During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology. RESULTS: Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development. CONCLUSIONS: This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-756) contains supplementary material, which is available to authorized users.
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spelling pubmed-41629622014-09-19 Transcriptional profiles of bovine in vivo pre-implantation development Jiang, Zongliang Sun, Jiangwen Dong, Hong Luo, Oscar Zheng, Xinbao Obergfell, Craig Tang, Yong Bi, Jinbo O’Neill, Rachel Ruan, Yijun Chen, Jingbo Tian, Xiuchun (Cindy) BMC Genomics Research Article BACKGROUND: During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology. RESULTS: Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development. CONCLUSIONS: This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-756) contains supplementary material, which is available to authorized users. BioMed Central 2014-09-04 /pmc/articles/PMC4162962/ /pubmed/25185836 http://dx.doi.org/10.1186/1471-2164-15-756 Text en © Jiang et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. 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, and reproduction in any medium, provided the original work is properly credited. 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
Jiang, Zongliang
Sun, Jiangwen
Dong, Hong
Luo, Oscar
Zheng, Xinbao
Obergfell, Craig
Tang, Yong
Bi, Jinbo
O’Neill, Rachel
Ruan, Yijun
Chen, Jingbo
Tian, Xiuchun (Cindy)
Transcriptional profiles of bovine in vivo pre-implantation development
title Transcriptional profiles of bovine in vivo pre-implantation development
title_full Transcriptional profiles of bovine in vivo pre-implantation development
title_fullStr Transcriptional profiles of bovine in vivo pre-implantation development
title_full_unstemmed Transcriptional profiles of bovine in vivo pre-implantation development
title_short Transcriptional profiles of bovine in vivo pre-implantation development
title_sort transcriptional profiles of bovine in vivo pre-implantation development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4162962/
https://www.ncbi.nlm.nih.gov/pubmed/25185836
http://dx.doi.org/10.1186/1471-2164-15-756
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