Dynamic DNA methylation of ovaries during pubertal transition in gilts

Abstract Background In female mammals, the initiation of puberty, coupling with the dramatically morphological changes in ovaries, indicates the sexual and follicular maturation. Previous studies have suggested that the disrupted DNA methylation results in the delayed puberty. However, to date, the...

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Main Authors: Xiaolong Yuan, Shaopan Ye, Zitao Chen, Xiangchun Pan, Shuwen Huang, Zhonghui Li, Yuyi Zhong, Ning Gao, Hao Zhang, Jiaqi Li, Zhe Zhang
Format: Article
Language:English
Published: BMC 2019-06-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-019-5884-x
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author Xiaolong Yuan
Shaopan Ye
Zitao Chen
Xiangchun Pan
Shuwen Huang
Zhonghui Li
Yuyi Zhong
Ning Gao
Hao Zhang
Jiaqi Li
Zhe Zhang
author_facet Xiaolong Yuan
Shaopan Ye
Zitao Chen
Xiangchun Pan
Shuwen Huang
Zhonghui Li
Yuyi Zhong
Ning Gao
Hao Zhang
Jiaqi Li
Zhe Zhang
author_sort Xiaolong Yuan
collection DOAJ
description Abstract Background In female mammals, the initiation of puberty, coupling with the dramatically morphological changes in ovaries, indicates the sexual and follicular maturation. Previous studies have suggested that the disrupted DNA methylation results in the delayed puberty. However, to date, the changes in ovarian methylomes during pubertal transition have not been investigated. In this study, using gilts as a pubertal model, the genome-wide DNA methylation were profiled to explore their dynamics during pubertal transition across Pre-, In- and Post-puberty. Results During pubertal transition, the follicles underwent maturation and luteinization, coupled with the significant changes in the mRNA expression of DNMT1 and DNMT3a. DNA methylation levels of In-puberty were higher than that of Pre- and Post-puberty at the locations of genes and CpG islands (CGIs). Analysis of the DNA methylation changes identified 12,313, 20,960 and 17,694 differentially methylated CpGs (DMCs) for the comparisons of Pre- vs. In-, In vs. Post-, and Pre- vs. Post-puberty, respectively. Moreover, the CGIs, upstream and exonic regions showed a significant underrepresentation of DMCs, but the CGI shores, CGI shelves, intronic, downstream and intergenic regions showed a significant overrepresentation of DMCs. Furthermore, biological functions of these methylation changes enriched in PI3K-Akt signaling pathway, GnRH signaling pathway, and Insulin secretion, and the mRNA expressions of several genes of these signaling pathway, including MMP2, ESR1, GSK3B, FGF21, IGF1R, and TAC3, were significantly changed across Pre-, In- and Post-puberty in ovaries. Conclusions During pubertal transition in gilts, the DNA methylation changes of ovaries were likely to affect the transcription of genes related to PI3K-Akt signaling pathway, GnRH signaling pathway, and Insulin secretion. These observations can provide new insight into the epigenetic mechanism of follicular and sexual maturation during pubertal transition in mammals.
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spelling doaj.art-7aba8731039a4eeabb12f681c9a4e6a02022-12-22T01:19:23ZengBMCBMC Genomics1471-21642019-06-0120111310.1186/s12864-019-5884-xDynamic DNA methylation of ovaries during pubertal transition in giltsXiaolong Yuan0Shaopan Ye1Zitao Chen2Xiangchun Pan3Shuwen Huang4Zhonghui Li5Yuyi Zhong6Ning Gao7Hao Zhang8Jiaqi Li9Zhe Zhang10National Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityState Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, North Third Road, Guangzhou Higher Education Mega CenterNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityNational Engineering Research Center for Breeding Swine Industry, Guangdong Provincial Key Lab of Agro-Animal Genomics and Molecular Breeding, College of Animal Science, South China Agricultural UniversityAbstract Background In female mammals, the initiation of puberty, coupling with the dramatically morphological changes in ovaries, indicates the sexual and follicular maturation. Previous studies have suggested that the disrupted DNA methylation results in the delayed puberty. However, to date, the changes in ovarian methylomes during pubertal transition have not been investigated. In this study, using gilts as a pubertal model, the genome-wide DNA methylation were profiled to explore their dynamics during pubertal transition across Pre-, In- and Post-puberty. Results During pubertal transition, the follicles underwent maturation and luteinization, coupled with the significant changes in the mRNA expression of DNMT1 and DNMT3a. DNA methylation levels of In-puberty were higher than that of Pre- and Post-puberty at the locations of genes and CpG islands (CGIs). Analysis of the DNA methylation changes identified 12,313, 20,960 and 17,694 differentially methylated CpGs (DMCs) for the comparisons of Pre- vs. In-, In vs. Post-, and Pre- vs. Post-puberty, respectively. Moreover, the CGIs, upstream and exonic regions showed a significant underrepresentation of DMCs, but the CGI shores, CGI shelves, intronic, downstream and intergenic regions showed a significant overrepresentation of DMCs. Furthermore, biological functions of these methylation changes enriched in PI3K-Akt signaling pathway, GnRH signaling pathway, and Insulin secretion, and the mRNA expressions of several genes of these signaling pathway, including MMP2, ESR1, GSK3B, FGF21, IGF1R, and TAC3, were significantly changed across Pre-, In- and Post-puberty in ovaries. Conclusions During pubertal transition in gilts, the DNA methylation changes of ovaries were likely to affect the transcription of genes related to PI3K-Akt signaling pathway, GnRH signaling pathway, and Insulin secretion. These observations can provide new insight into the epigenetic mechanism of follicular and sexual maturation during pubertal transition in mammals.http://link.springer.com/article/10.1186/s12864-019-5884-xGenome-wide DNA methylationDNMTsOvariesPubertal transitionGilts
spellingShingle Xiaolong Yuan
Shaopan Ye
Zitao Chen
Xiangchun Pan
Shuwen Huang
Zhonghui Li
Yuyi Zhong
Ning Gao
Hao Zhang
Jiaqi Li
Zhe Zhang
Dynamic DNA methylation of ovaries during pubertal transition in gilts
BMC Genomics
Genome-wide DNA methylation
DNMTs
Ovaries
Pubertal transition
Gilts
title Dynamic DNA methylation of ovaries during pubertal transition in gilts
title_full Dynamic DNA methylation of ovaries during pubertal transition in gilts
title_fullStr Dynamic DNA methylation of ovaries during pubertal transition in gilts
title_full_unstemmed Dynamic DNA methylation of ovaries during pubertal transition in gilts
title_short Dynamic DNA methylation of ovaries during pubertal transition in gilts
title_sort dynamic dna methylation of ovaries during pubertal transition in gilts
topic Genome-wide DNA methylation
DNMTs
Ovaries
Pubertal transition
Gilts
url http://link.springer.com/article/10.1186/s12864-019-5884-x
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