Broad Heterochromatic Domains Open in Gonocyte Development Prior to De Novo DNA Methylation

Soichiro Yamanaka; Hidenori Nishihara; Hidehiro Toh; Luis Augusto Eijy Nagai; Kosuke Hashimoto; Sung Joon Park; Aoi Shibuya; Ana Maria Suzuki; Yujiro Tanaka; Kenta Nakai; Piero Carninci; Hiroyuki Sasaki; Haruhiko Siomi

doi:10.1016/j.devcel.2019.07.023

Broad Heterochromatic Domains Open in Gonocyte Development Prior to De Novo DNA Methylation

Soichiro Yamanaka, Hidenori Nishihara, Hidehiro Toh, Luis Augusto Eijy Nagai, Kosuke Hashimoto, Sung Joon Park, Aoi Shibuya, Ana Maria Suzuki, Yujiro Tanaka, Kenta Nakai, Piero Carninci, Hiroyuki Sasaki, Haruhiko Siomi

分子生物学

研究成果: Article › 査読

19 被引用数 (Scopus)

抄録

Genome-wide de novo DNA methylation occurs in mouse gonocytes, arrested male embryonic germ cells. However, how the methylome gets established in the genome of arrested cells remains unexplored. Yamanaka et al. report that multiple chromatin reprogramming pathways allow the access of methyltransferases to DNA in gonocytes.

本文言語	English
ページ（範囲）	21-34.e5
ジャーナル	Developmental Cell
巻	51
号	1
DOI	https://doi.org/10.1016/j.devcel.2019.07.023
出版ステータス	Published - 2019 10月 7

ASJC Scopus subject areas

分子生物学
生化学、遺伝学、分子生物学（全般）
発生生物学
細胞生物学

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10.1016/j.devcel.2019.07.023

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@article{0118eee946444b8b8d7f1c90dc5eef40,

title = "Broad Heterochromatic Domains Open in Gonocyte Development Prior to De Novo DNA Methylation",

abstract = "Genome-wide de novo DNA methylation occurs in mouse gonocytes, arrested male embryonic germ cells. However, how the methylome gets established in the genome of arrested cells remains unexplored. Yamanaka et al. report that multiple chromatin reprogramming pathways allow the access of methyltransferases to DNA in gonocytes.",

keywords = "ATAC-seq, de novo DNA methylation, gene cluster, gene desert, gonocyte, transposon",

author = "Soichiro Yamanaka and Hidenori Nishihara and Hidehiro Toh and {Eijy Nagai}, {Luis Augusto} and Kosuke Hashimoto and Park, {Sung Joon} and Aoi Shibuya and Suzuki, {Ana Maria} and Yujiro Tanaka and Kenta Nakai and Piero Carninci and Hiroyuki Sasaki and Haruhiko Siomi",

note = "Funding Information: We thank all members of the Siomi laboratory, especially Drs. Yuka Iwasaki and Hirotsugu Ishizu, for discussions and comments on this work. We also thank Drs. Kei-ichiro Ishiguro ( Kumamoto University ), Yoshiyuki Seki ( Kwansei Gakuin University ), and Satoshi Namekawa ( Cincinnati Children{\textquoteright}s Hospital Medical Center ) for critical reading of the manuscript. We are also grateful to Dr. Kuniya Abe ( RIKEN ) for shearing the Ddx4-Venus TG mouse. Finally, we thank Edanz ( www.edanzediting.co.jp ) for editing the English text of a draft of this manuscript. This work was partly performed in the Cooperative Research Project Program of the Medical Institute of Bioregulation, Kyushu University . We are grateful to the Collaborative Research Resources, School of Medicine, Keio University for technical support and reagents. Computations were partially performed on the supercomputer system of SIROKANE at the Human Genome Center, The Institute of Medical Sciences, University of Tokyo , and that of the Institute of Statistical Mathematics. S.Y. is supported by Takeda Science Foundation and Keio Gijuku Academic Development Funds. This work was supported by Grants-in-Aid for Scientific Research on Innovative Areas ( 25112010 to H. Sasaki, 16H01403 to K.N., 18H04710 to S.P., and 26112513 and 16H01411 to S.Y.) from the Japan Society for the Promotion of Science (JSPS). A Grant-in-Aid for Challenging Exploratory Research ( 17K19424 ) to H.N. and a Grant-in-Aid for Young Scientists (A) ( 26710011 ) to S.Y. from JSPS also supported the present work. K.H. is supported by a research grant from MEXT to the RIKEN Center for Integrative Medical Sciences. H. Siomi was supported by a Grant-in-Aid for Scientific Research (S) ( 25221003 ) from JSPS and is a recipient of funding for the Project for Elucidating and Controlling Mechanisms of Aging and Longevity ( 1005442 ) from the Japan Agency for Medical Research and Development (AMED). Funding Information: We thank all members of the Siomi laboratory, especially Drs. Yuka Iwasaki and Hirotsugu Ishizu, for discussions and comments on this work. We also thank Drs. Kei-ichiro Ishiguro (Kumamoto University), Yoshiyuki Seki (Kwansei Gakuin University), and Satoshi Namekawa (Cincinnati Children's Hospital Medical Center) for critical reading of the manuscript. We are also grateful to Dr. Kuniya Abe (RIKEN) for shearing the Ddx4-Venus TG mouse. Finally, we thank Edanz (www.edanzediting.co.jp) for editing the English text of a draft of this manuscript. This work was partly performed in the Cooperative Research Project Program of the Medical Institute of Bioregulation, Kyushu University. We are grateful to the Collaborative Research Resources, School of Medicine, Keio University for technical support and reagents. Computations were partially performed on the supercomputer system of SIROKANE at the Human Genome Center, The Institute of Medical Sciences, University of Tokyo, and that of the Institute of Statistical Mathematics. S.Y. is supported by Takeda Science Foundation and Keio Gijuku Academic Development Funds. This work was supported by Grants-in-Aid for Scientific Research on Innovative Areas (25112010 to H. Sasaki, 16H01403 to K.N. 18H04710 to S.P. and 26112513 and 16H01411 to S.Y.) from the Japan Society for the Promotion of Science (JSPS). A Grant-in-Aid for Challenging Exploratory Research (17K19424) to H.N. and a Grant-in-Aid for Young Scientists (A) (26710011) to S.Y. from JSPS also supported the present work. K.H. is supported by a research grant from MEXT to the RIKEN Center for Integrative Medical Sciences. H. Siomi was supported by a Grant-in-Aid for Scientific Research (S) (25221003) from JSPS and is a recipient of funding for the Project for Elucidating and Controlling Mechanisms of Aging and Longevity (1005442) from the Japan Agency for Medical Research and Development (AMED). S.Y. and H. Siomi conceived of the project and designed the experiments. S.Y. H.N. H.T. K.H. L.A.E.N. and S.-J.P. performed the computational analysis. H.N. analyzed the detailed transposon profiles for ATAC-seq and ChIP-seq. A.S. A.M.S. and Y.T. helped with the DNA library preparation for ATAC-seq, nanoCAGE-seq, and ChIP-seq, respectively. K.N. helped the Hi-C data analysis. P.C. helped the acquisition and the analysis of nanoCAGE-seq data. H. Sasaki helped the analysis of DNA methylation profiles and revised the paper. S.Y. and H. Siomi wrote the paper with the inputs from all authors. All authors commented on and agreed with the contents of this paper. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2019 Elsevier Inc.",

year = "2019",

month = oct,

day = "7",

doi = "10.1016/j.devcel.2019.07.023",

language = "English",

volume = "51",

pages = "21--34.e5",

journal = "Developmental Cell",

issn = "1534-5807",

publisher = "Cell Press",

number = "1",

}

TY - JOUR

T1 - Broad Heterochromatic Domains Open in Gonocyte Development Prior to De Novo DNA Methylation

AU - Yamanaka, Soichiro

AU - Nishihara, Hidenori

AU - Toh, Hidehiro

AU - Eijy Nagai, Luis Augusto

AU - Hashimoto, Kosuke

AU - Park, Sung Joon

AU - Shibuya, Aoi

AU - Suzuki, Ana Maria

AU - Tanaka, Yujiro

AU - Nakai, Kenta

AU - Carninci, Piero

AU - Sasaki, Hiroyuki

AU - Siomi, Haruhiko

N1 - Funding Information: We thank all members of the Siomi laboratory, especially Drs. Yuka Iwasaki and Hirotsugu Ishizu, for discussions and comments on this work. We also thank Drs. Kei-ichiro Ishiguro ( Kumamoto University ), Yoshiyuki Seki ( Kwansei Gakuin University ), and Satoshi Namekawa ( Cincinnati Children’s Hospital Medical Center ) for critical reading of the manuscript. We are also grateful to Dr. Kuniya Abe ( RIKEN ) for shearing the Ddx4-Venus TG mouse. Finally, we thank Edanz ( www.edanzediting.co.jp ) for editing the English text of a draft of this manuscript. This work was partly performed in the Cooperative Research Project Program of the Medical Institute of Bioregulation, Kyushu University . We are grateful to the Collaborative Research Resources, School of Medicine, Keio University for technical support and reagents. Computations were partially performed on the supercomputer system of SIROKANE at the Human Genome Center, The Institute of Medical Sciences, University of Tokyo , and that of the Institute of Statistical Mathematics. S.Y. is supported by Takeda Science Foundation and Keio Gijuku Academic Development Funds. This work was supported by Grants-in-Aid for Scientific Research on Innovative Areas ( 25112010 to H. Sasaki, 16H01403 to K.N., 18H04710 to S.P., and 26112513 and 16H01411 to S.Y.) from the Japan Society for the Promotion of Science (JSPS). A Grant-in-Aid for Challenging Exploratory Research ( 17K19424 ) to H.N. and a Grant-in-Aid for Young Scientists (A) ( 26710011 ) to S.Y. from JSPS also supported the present work. K.H. is supported by a research grant from MEXT to the RIKEN Center for Integrative Medical Sciences. H. Siomi was supported by a Grant-in-Aid for Scientific Research (S) ( 25221003 ) from JSPS and is a recipient of funding for the Project for Elucidating and Controlling Mechanisms of Aging and Longevity ( 1005442 ) from the Japan Agency for Medical Research and Development (AMED). Funding Information: We thank all members of the Siomi laboratory, especially Drs. Yuka Iwasaki and Hirotsugu Ishizu, for discussions and comments on this work. We also thank Drs. Kei-ichiro Ishiguro (Kumamoto University), Yoshiyuki Seki (Kwansei Gakuin University), and Satoshi Namekawa (Cincinnati Children's Hospital Medical Center) for critical reading of the manuscript. We are also grateful to Dr. Kuniya Abe (RIKEN) for shearing the Ddx4-Venus TG mouse. Finally, we thank Edanz (www.edanzediting.co.jp) for editing the English text of a draft of this manuscript. This work was partly performed in the Cooperative Research Project Program of the Medical Institute of Bioregulation, Kyushu University. We are grateful to the Collaborative Research Resources, School of Medicine, Keio University for technical support and reagents. Computations were partially performed on the supercomputer system of SIROKANE at the Human Genome Center, The Institute of Medical Sciences, University of Tokyo, and that of the Institute of Statistical Mathematics. S.Y. is supported by Takeda Science Foundation and Keio Gijuku Academic Development Funds. This work was supported by Grants-in-Aid for Scientific Research on Innovative Areas (25112010 to H. Sasaki, 16H01403 to K.N. 18H04710 to S.P. and 26112513 and 16H01411 to S.Y.) from the Japan Society for the Promotion of Science (JSPS). A Grant-in-Aid for Challenging Exploratory Research (17K19424) to H.N. and a Grant-in-Aid for Young Scientists (A) (26710011) to S.Y. from JSPS also supported the present work. K.H. is supported by a research grant from MEXT to the RIKEN Center for Integrative Medical Sciences. H. Siomi was supported by a Grant-in-Aid for Scientific Research (S) (25221003) from JSPS and is a recipient of funding for the Project for Elucidating and Controlling Mechanisms of Aging and Longevity (1005442) from the Japan Agency for Medical Research and Development (AMED). S.Y. and H. Siomi conceived of the project and designed the experiments. S.Y. H.N. H.T. K.H. L.A.E.N. and S.-J.P. performed the computational analysis. H.N. analyzed the detailed transposon profiles for ATAC-seq and ChIP-seq. A.S. A.M.S. and Y.T. helped with the DNA library preparation for ATAC-seq, nanoCAGE-seq, and ChIP-seq, respectively. K.N. helped the Hi-C data analysis. P.C. helped the acquisition and the analysis of nanoCAGE-seq data. H. Sasaki helped the analysis of DNA methylation profiles and revised the paper. S.Y. and H. Siomi wrote the paper with the inputs from all authors. All authors commented on and agreed with the contents of this paper. The authors declare no competing interests. Publisher Copyright: © 2019 Elsevier Inc.

PY - 2019/10/7

Y1 - 2019/10/7

N2 - Genome-wide de novo DNA methylation occurs in mouse gonocytes, arrested male embryonic germ cells. However, how the methylome gets established in the genome of arrested cells remains unexplored. Yamanaka et al. report that multiple chromatin reprogramming pathways allow the access of methyltransferases to DNA in gonocytes.

AB - Genome-wide de novo DNA methylation occurs in mouse gonocytes, arrested male embryonic germ cells. However, how the methylome gets established in the genome of arrested cells remains unexplored. Yamanaka et al. report that multiple chromatin reprogramming pathways allow the access of methyltransferases to DNA in gonocytes.

KW - ATAC-seq

KW - de novo DNA methylation

KW - gene cluster

KW - gene desert

KW - gonocyte

KW - transposon

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UR - http://www.scopus.com/inward/citedby.url?scp=85072703324&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2019.07.023

DO - 10.1016/j.devcel.2019.07.023

M3 - Article

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AN - SCOPUS:85072703324

SN - 1534-5807

VL - 51

SP - 21-34.e5

JO - Developmental Cell

JF - Developmental Cell

IS - 1

ER -

Broad Heterochromatic Domains Open in Gonocyte Development Prior to De Novo DNA Methylation

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