Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development

Proper placental development is crucial for the conceptus to grow and survive, because the placenta is responsible for transporting nutrients and oxygen from the pregnant female to the developing fetus. However, the processes of placental morphogenesis and fold formation remain to be fully elucidate...

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Main Authors: Baohua Tan, Chen Zhou, Xupeng Zang, Xinming Zhao, Liyao Xiao, Jiekang Zeng, Linjun Hong, Zhenfang Wu, Ting Gu
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/6/5169
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author Baohua Tan
Chen Zhou
Xupeng Zang
Xinming Zhao
Liyao Xiao
Jiekang Zeng
Linjun Hong
Zhenfang Wu
Ting Gu
author_facet Baohua Tan
Chen Zhou
Xupeng Zang
Xinming Zhao
Liyao Xiao
Jiekang Zeng
Linjun Hong
Zhenfang Wu
Ting Gu
author_sort Baohua Tan
collection DOAJ
description Proper placental development is crucial for the conceptus to grow and survive, because the placenta is responsible for transporting nutrients and oxygen from the pregnant female to the developing fetus. However, the processes of placental morphogenesis and fold formation remain to be fully elucidated. In this study, we used whole-genome bisulfite sequencing and RNA sequencing to produce a global map of DNA methylation and gene expression changes in placentas from Tibetan pig fetuses 21, 28, and 35 days post-coitus. Substantial changes in morphology and histological structures at the uterine–placental interface were revealed via hematoxylin–eosin staining. Transcriptome analysis identified 3959 differentially expressed genes (DEGs) and revealed the key transcriptional properties in three stages. The DNA methylation level in the gene promoter was negatively correlated with gene expression. We identified a set of differentially methylated regions associated with placental developmental genes and transcription factors. The decrease in DNA methylation level in the promoter was associated with the transcriptional activation of 699 DEGs that were functionally enriched in cell adhesion and migration, extracellular matrix remodeling, and angiogenesis. Our analysis provides a valuable resource for understanding the mechanisms of DNA methylation in placental development. The methylation status of different genomic regions plays a key role in establishing transcriptional patterns from placental morphogenesis to fold formation.
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spelling doaj.art-9ac7ed18bf084bd489a51bfc9c8b4afa2023-11-17T11:30:03ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-03-01246516910.3390/ijms24065169Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental DevelopmentBaohua Tan0Chen Zhou1Xupeng Zang2Xinming Zhao3Liyao Xiao4Jiekang Zeng5Linjun Hong6Zhenfang Wu7Ting Gu8National Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaNational Engineering Research Center for Breeding Swine Industry, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaProper placental development is crucial for the conceptus to grow and survive, because the placenta is responsible for transporting nutrients and oxygen from the pregnant female to the developing fetus. However, the processes of placental morphogenesis and fold formation remain to be fully elucidated. In this study, we used whole-genome bisulfite sequencing and RNA sequencing to produce a global map of DNA methylation and gene expression changes in placentas from Tibetan pig fetuses 21, 28, and 35 days post-coitus. Substantial changes in morphology and histological structures at the uterine–placental interface were revealed via hematoxylin–eosin staining. Transcriptome analysis identified 3959 differentially expressed genes (DEGs) and revealed the key transcriptional properties in three stages. The DNA methylation level in the gene promoter was negatively correlated with gene expression. We identified a set of differentially methylated regions associated with placental developmental genes and transcription factors. The decrease in DNA methylation level in the promoter was associated with the transcriptional activation of 699 DEGs that were functionally enriched in cell adhesion and migration, extracellular matrix remodeling, and angiogenesis. Our analysis provides a valuable resource for understanding the mechanisms of DNA methylation in placental development. The methylation status of different genomic regions plays a key role in establishing transcriptional patterns from placental morphogenesis to fold formation.https://www.mdpi.com/1422-0067/24/6/5169DNA methylationpigplacental developmenttranscriptome
spellingShingle Baohua Tan
Chen Zhou
Xupeng Zang
Xinming Zhao
Liyao Xiao
Jiekang Zeng
Linjun Hong
Zhenfang Wu
Ting Gu
Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
International Journal of Molecular Sciences
DNA methylation
pig
placental development
transcriptome
title Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
title_full Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
title_fullStr Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
title_full_unstemmed Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
title_short Integrated Analysis of DNA Methylation and Gene Expression in Porcine Placental Development
title_sort integrated analysis of dna methylation and gene expression in porcine placental development
topic DNA methylation
pig
placental development
transcriptome
url https://www.mdpi.com/1422-0067/24/6/5169
work_keys_str_mv AT baohuatan integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT chenzhou integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT xupengzang integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT xinmingzhao integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT liyaoxiao integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT jiekangzeng integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT linjunhong integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT zhenfangwu integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment
AT tinggu integratedanalysisofdnamethylationandgeneexpressioninporcineplacentaldevelopment