The Transcriptome and DNA Methylome Landscapes of Human Primordial Germ Cells

Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions...

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Published in	Cell Vol. 161; no. 6; pp. 1437 - 1452
Main Authors	Guo, Fan, Yan, Liying, Guo, Hongshan, Li, Lin, Hu, Boqiang, Zhao, Yangyu, Yong, Jun, Hu, Yuqiong, Wang, Xiaoye, Wei, Yuan, Wang, Wei, Li, Rong, Yan, Jie, Zhi, Xu, Zhang, Yan, Jin, Hongyan, Zhang, Wenxin, Hou, Yu, Zhu, Ping, Li, Jingyun, Zhang, Ling, Liu, Sirui, Ren, Yixin, Zhu, Xiaohui, Wen, Lu, Gao, Yi Qin, Tang, Fuchou, Qiao, Jie
Format	Journal Article
Language	English
Published	United States Elsevier Inc 04.06.2015
Subjects	Cell Movement Chromosomes, Human, X Cluster Analysis DNA DNA Methylation Embryo, Mammalian - metabolism epigenetics Female females genes Germ Cells - metabolism gonads Histones - metabolism Humans landscapes Male males oocytes pregnancy Principal Component Analysis SOX Transcription Factors - metabolism totipotency Transcriptome
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Abstract	Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions. Human PGCs show unique transcription patterns involving the simultaneous expression of both pluripotency genes and germline-specific genes, with a subset of them displaying developmental-stage-specific features. Furthermore, we analyze the DNA methylome of human PGCs and find global demethylation of their genomes. Approximately 10 to 11 weeks after gestation, the PGCs are nearly devoid of any DNA methylation, with only 7.8% and 6.0% of the median methylation levels in male and female PGCs, respectively. Our work paves the way toward deciphering the complex epigenetic reprogramming of the germline with the aim of restoring totipotency in fertilized oocytes. [Display omitted] •The transcriptomes of human PGCs are relatively homogeneous between 4 and 11 weeks•The inactivated X chromosomes in PGCs are already reactivated in 4 week embryos•Individual meiotic PGCs exhibit strongly heterogeneous gene expression patterns•The global erasure of DNA methylation in human PGCs is completed at 10 to 11 weeks The transcriptome of human primordial germ cells from the migrating stage to the gonadal stage reveals that both pluripotency genes and germline-specific genes are simultaneously expressed within the same individual cells. The global erasure of DNA methylation creates a super-hypomethylated germline genome.
AbstractList	Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions. Human PGCs show unique transcription patterns involving the simultaneous expression of both pluripotency genes and germline-specific genes, with a subset of them displaying developmental-stage-specific features. Furthermore, we analyze the DNA methylome of human PGCs and find global demethylation of their genomes. Approximately 10 to 11 weeks after gestation, the PGCs are nearly devoid of any DNA methylation, with only 7.8% and 6.0% of the median methylation levels in male and female PGCs, respectively. Our work paves the way toward deciphering the complex epigenetic reprogramming of the germline with the aim of restoring totipotency in fertilized oocytes. [Display omitted] •The transcriptomes of human PGCs are relatively homogeneous between 4 and 11 weeks•The inactivated X chromosomes in PGCs are already reactivated in 4 week embryos•Individual meiotic PGCs exhibit strongly heterogeneous gene expression patterns•The global erasure of DNA methylation in human PGCs is completed at 10 to 11 weeks The transcriptome of human primordial germ cells from the migrating stage to the gonadal stage reveals that both pluripotency genes and germline-specific genes are simultaneously expressed within the same individual cells. The global erasure of DNA methylation creates a super-hypomethylated germline genome. Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions. Human PGCs show unique transcription patterns involving the simultaneous expression of both pluripotency genes and germline-specific genes, with a subset of them displaying developmental-stage-specific features. Furthermore, we analyze the DNA methylome of human PGCs and find global demethylation of their genomes. Approximately 10 to 11 weeks after gestation, the PGCs are nearly devoid of any DNA methylation, with only 7.8% and 6.0% of the median methylation levels in male and female PGCs, respectively. Our work paves the way toward deciphering the complex epigenetic reprogramming of the germline with the aim of restoring totipotency in fertilized oocytes.Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions. Human PGCs show unique transcription patterns involving the simultaneous expression of both pluripotency genes and germline-specific genes, with a subset of them displaying developmental-stage-specific features. Furthermore, we analyze the DNA methylome of human PGCs and find global demethylation of their genomes. Approximately 10 to 11 weeks after gestation, the PGCs are nearly devoid of any DNA methylation, with only 7.8% and 6.0% of the median methylation levels in male and female PGCs, respectively. Our work paves the way toward deciphering the complex epigenetic reprogramming of the germline with the aim of restoring totipotency in fertilized oocytes. Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the transcriptome of human primordial germ cells (PGCs) from the migrating stage to the gonadal stage at single-cell and single-base resolutions. Human PGCs show unique transcription patterns involving the simultaneous expression of both pluripotency genes and germline-specific genes, with a subset of them displaying developmental-stage-specific features. Furthermore, we analyze the DNA methylome of human PGCs and find global demethylation of their genomes. Approximately 10 to 11 weeks after gestation, the PGCs are nearly devoid of any DNA methylation, with only 7.8% and 6.0% of the median methylation levels in male and female PGCs, respectively. Our work paves the way toward deciphering the complex epigenetic reprogramming of the germline with the aim of restoring totipotency in fertilized oocytes.
Author	Li, Lin Wang, Wei Jin, Hongyan Yan, Liying Hu, Boqiang Zhu, Xiaohui Wei, Yuan Ren, Yixin Yan, Jie Wang, Xiaoye Zhang, Yan Zhang, Ling Liu, Sirui Li, Rong Tang, Fuchou Wen, Lu Zhi, Xu Qiao, Jie Guo, Hongshan Guo, Fan Zhao, Yangyu Li, Jingyun Zhu, Ping Gao, Yi Qin Hou, Yu Zhang, Wenxin Hu, Yuqiong Yong, Jun
Author_xml	– sequence: 1 givenname: Fan surname: Guo fullname: Guo, Fan organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 2 givenname: Liying surname: Yan fullname: Yan, Liying organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 3 givenname: Hongshan surname: Guo fullname: Guo, Hongshan organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 4 givenname: Lin surname: Li fullname: Li, Lin organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 5 givenname: Boqiang surname: Hu fullname: Hu, Boqiang organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 6 givenname: Yangyu surname: Zhao fullname: Zhao, Yangyu organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 7 givenname: Jun surname: Yong fullname: Yong, Jun organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 8 givenname: Yuqiong surname: Hu fullname: Hu, Yuqiong organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 9 givenname: Xiaoye surname: Wang fullname: Wang, Xiaoye organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 10 givenname: Yuan surname: Wei fullname: Wei, Yuan organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 11 givenname: Wei surname: Wang fullname: Wang, Wei organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 12 givenname: Rong surname: Li fullname: Li, Rong organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 13 givenname: Jie surname: Yan fullname: Yan, Jie organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 14 givenname: Xu surname: Zhi fullname: Zhi, Xu organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 15 givenname: Yan surname: Zhang fullname: Zhang, Yan organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 16 givenname: Hongyan surname: Jin fullname: Jin, Hongyan organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 17 givenname: Wenxin surname: Zhang fullname: Zhang, Wenxin organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 18 givenname: Yu surname: Hou fullname: Hou, Yu organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 19 givenname: Ping surname: Zhu fullname: Zhu, Ping organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 20 givenname: Jingyun surname: Li fullname: Li, Jingyun organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 21 givenname: Ling surname: Zhang fullname: Zhang, Ling organization: Institute of Theoretical and Computational Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, PRC – sequence: 22 givenname: Sirui surname: Liu fullname: Liu, Sirui organization: Institute of Theoretical and Computational Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, PRC – sequence: 23 givenname: Yixin surname: Ren fullname: Ren, Yixin organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 24 givenname: Xiaohui surname: Zhu fullname: Zhu, Xiaohui organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 25 givenname: Lu surname: Wen fullname: Wen, Lu organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 26 givenname: Yi Qin surname: Gao fullname: Gao, Yi Qin organization: Institute of Theoretical and Computational Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, PRC – sequence: 27 givenname: Fuchou surname: Tang fullname: Tang, Fuchou email: tangfuchou@pku.edu.cn organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC – sequence: 28 givenname: Jie surname: Qiao fullname: Qiao, Jie email: jie.qiao@263.net organization: Biodynamic Optical Imaging Center and Department of Obstetrics and Gynecology, College of Life Sciences, Third Hospital, Peking University, Beijing 100871, PRC
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Snippet	Germ cells are vital for transmitting genetic information from one generation to the next and for maintaining the continuation of species. Here, we analyze the...
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SubjectTerms	Cell Movement Chromosomes, Human, X Cluster Analysis DNA DNA Methylation Embryo, Mammalian - metabolism epigenetics Female females genes Germ Cells - metabolism gonads Histones - metabolism Humans landscapes Male males oocytes pregnancy Principal Component Analysis SOX Transcription Factors - metabolism totipotency Transcriptome
Title	The Transcriptome and DNA Methylome Landscapes of Human Primordial Germ Cells
URI	https://dx.doi.org/10.1016/j.cell.2015.05.015 https://www.ncbi.nlm.nih.gov/pubmed/26046443 https://www.proquest.com/docview/1686421232 https://www.proquest.com/docview/2000224885
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