IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-31759-6.html
   My bibliography  Save this article

PRC1-mediated epigenetic programming is required to generate the ovarian reserve

Author

Listed:
  • Mengwen Hu

    (University of California, Davis
    Perinatal Institute, Cincinnati Children’s Hospital Medical Center)

  • Yu-Han Yeh

    (University of California, Davis
    Perinatal Institute, Cincinnati Children’s Hospital Medical Center)

  • Yasuhisa Munakata

    (University of California, Davis
    Perinatal Institute, Cincinnati Children’s Hospital Medical Center)

  • Hironori Abe

    (University of California, Davis
    Perinatal Institute, Cincinnati Children’s Hospital Medical Center)

  • Akihiko Sakashita

    (Perinatal Institute, Cincinnati Children’s Hospital Medical Center
    Keio University School of Medicine)

  • So Maezawa

    (Perinatal Institute, Cincinnati Children’s Hospital Medical Center
    Tokyo University of Science)

  • Miguel Vidal

    (Centro de Investigaciones Biológicas Margarita Salas, Department of Cellular and Molecular Biology)

  • Haruhiko Koseki

    (RIKEN Center for Allergy and Immunology)

  • Neil Hunter

    (University of California, Davis
    University of California, Davis)

  • Richard M. Schultz

    (University of Pennsylvania
    University of California, Davis)

  • Satoshi H. Namekawa

    (University of California, Davis
    Perinatal Institute, Cincinnati Children’s Hospital Medical Center)

Abstract

The ovarian reserve defines the female reproductive lifespan, which in humans spans decades due to robust maintenance of meiotic arrest in oocytes residing in primordial follicles. Epigenetic reprogramming, including DNA demethylation, accompanies meiotic entry, but the chromatin changes that underpin the generation and preservation of ovarian reserves are poorly defined. We report that the Polycomb Repressive Complex 1 (PRC1) establishes repressive chromatin states in perinatal mouse oocytes that directly suppress the gene expression program of meiotic prophase-I and thereby enable the transition to dictyate arrest. PRC1 dysfuction causes depletion of the ovarian reserve and leads to premature ovarian failure. Our study demonstrates a fundamental role for PRC1-mediated gene silencing in female reproductive lifespan, and reveals a critical window of epigenetic programming required to establish ovarian reserve.

Suggested Citation

  • Mengwen Hu & Yu-Han Yeh & Yasuhisa Munakata & Hironori Abe & Akihiko Sakashita & So Maezawa & Miguel Vidal & Haruhiko Koseki & Neil Hunter & Richard M. Schultz & Satoshi H. Namekawa, 2022. "PRC1-mediated epigenetic programming is required to generate the ovarian reserve," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31759-6
    DOI: 10.1038/s41467-022-31759-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-31759-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-31759-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Hengbin Wang & Liangjun Wang & Hediye Erdjument-Bromage & Miguel Vidal & Paul Tempst & Richard S. Jones & Yi Zhang, 2004. "Role of histone H2A ubiquitination in Polycomb silencing," Nature, Nature, vol. 431(7010), pages 873-878, October.
    2. Tien-Chi Huang & Yi-Fang Wang & Eric Vazquez-Ferrer & Ina Theofel & Cristina E. Requena & Courtney W. Hanna & Gavin Kelsey & Petra Hajkova, 2021. "Sex-specific chromatin remodelling safeguards transcription in germ cells," Nature, Nature, vol. 600(7890), pages 737-742, December.
    3. Mengcheng Luo & Fang Yang & N. Adrian Leu & Jessica Landaiche & Mary Ann Handel & Ricardo Benavente & Sophie La Salle & P. Jeremy Wang, 2013. "MEIOB exhibits single-stranded DNA-binding and exonuclease activities and is essential for meiotic recombination," Nature Communications, Nature, vol. 4(1), pages 1-12, December.
    4. Nobuhiko Hamazaki & Hirohisa Kyogoku & Hiromitsu Araki & Fumihito Miura & Chisako Horikawa & Norio Hamada & So Shimamoto & Orie Hikabe & Kinichi Nakashima & Tomoya S. Kitajima & Takashi Ito & Harry G., 2021. "Reconstitution of the oocyte transcriptional network with transcription factors," Nature, Nature, vol. 589(7841), pages 264-269, January.
    5. Helena Santos-Rosa & Robert Schneider & Andrew J. Bannister & Julia Sherriff & Bradley E. Bernstein & N. C. Tolga Emre & Stuart L. Schreiber & Jane Mellor & Tony Kouzarides, 2002. "Active genes are tri-methylated at K4 of histone H3," Nature, Nature, vol. 419(6905), pages 407-411, September.
    6. Shihori Yokobayashi & Ching-Yeu Liang & Hubertus Kohler & Peter Nestorov & Zichuan Liu & Miguel Vidal & Maarten van Lohuizen & Tim C. Roloff & Antoine H. F. M. Peters, 2013. "PRC1 coordinates timing of sexual differentiation of female primordial germ cells," Nature, Nature, vol. 495(7440), pages 236-240, March.
    7. Haojie Li & Robert Liefke & Junyi Jiang & Jesse Vigoda Kurland & Wei Tian & Pujuan Deng & Weidi Zhang & Qian He & Dinshaw J. Patel & Martha L. Bulyk & Yang Shi & Zhanxin Wang, 2017. "Polycomb-like proteins link the PRC2 complex to CpG islands," Nature, Nature, vol. 549(7671), pages 287-291, September.
    8. Abed AlFatah Mansour & Ohad Gafni & Leehee Weinberger & Asaf Zviran & Muneef Ayyash & Yoach Rais & Vladislav Krupalnik & Mirie Zerbib & Daniela Amann-Zalcenstein & Itay Maza & Shay Geula & Sergey Viuk, 2012. "The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming," Nature, Nature, vol. 488(7411), pages 409-413, August.
    9. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    10. Emilie Abby & Sophie Tourpin & Jonathan Ribeiro & Katrin Daniel & Sébastien Messiaen & Delphine Moison & Justine Guerquin & Jean-Charles Gaillard & Jean Armengaud & Francina Langa & Attila Toth & Emma, 2016. "Implementation of meiosis prophase I programme requires a conserved retinoid-independent stabilizer of meiotic transcripts," Nature Communications, Nature, vol. 7(1), pages 1-16, April.
    11. Shinpei Yamaguchi & Kwonho Hong & Rui Liu & Li Shen & Azusa Inoue & Dinh Diep & Kun Zhang & Yi Zhang, 2012. "Tet1 controls meiosis by regulating meiotic gene expression," Nature, Nature, vol. 492(7429), pages 443-447, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ryuki Shimada & Yuzuru Kato & Naoki Takeda & Sayoko Fujimura & Kei-ichiro Yasunaga & Shingo Usuki & Hitoshi Niwa & Kimi Araki & Kei-ichiro Ishiguro, 2023. "STRA8–RB interaction is required for timely entry of meiosis in mouse female germ cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Daniel Bsteh & Hagar F. Moussa & Georg Michlits & Ramesh Yelagandula & Jingkui Wang & Ulrich Elling & Oliver Bell, 2023. "Loss of cohesin regulator PDS5A reveals repressive role of Polycomb loops," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Wenjing Yan & Yongwang Zhong & Xin Hu & Tuan Xu & Yinghua Zhang & Stephen Kales & Yanyan Qu & Daniel C. Talley & Bolormaa Baljinnyam & Christopher A. LeClair & Anton Simeonov & Brian M. Polster & Ruil, 2023. "Auranofin targets UBA1 and enhances UBA1 activity by facilitating ubiquitin trans-thioesterification to E2 ubiquitin-conjugating enzymes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Xiangwei Li & Thomas Delerue & Ben Schöttker & Bernd Holleczek & Eva Grill & Annette Peters & Melanie Waldenberger & Barbara Thorand & Hermann Brenner, 2022. "Derivation and validation of an epigenetic frailty risk score in population-based cohorts of older adults," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    6. Ramachandran Prakasam & Angela Bonadiman & Roberta Andreotti & Emanuela Zuccaro & Davide Dalfovo & Caterina Marchioretti & Debasmita Tripathy & Gianluca Petris & Eric N. Anderson & Alice Migazzi & Lau, 2023. "LSD1/PRMT6-targeting gene therapy to attenuate androgen receptor toxic gain-of-function ameliorates spinobulbar muscular atrophy phenotypes in flies and mice," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    7. Li Guo & Cheng Hu & Yang Liu & Xiaoyu Chen & Deli Song & Runling Shen & Zhanzhen Liu & Xudong Jia & Qinfen Zhang & Yuanzhu Gao & Zhezhi Deng & Tao Zuo & Jun Hu & Wenbo Zhu & Jing Cai & Guangmei Yan & , 2023. "Directed natural evolution generates a next-generation oncolytic virus with a high potency and safety profile," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    9. Tianshi Feng & Xuemei Zhao & Ping Gu & Wah Yang & Cunchuan Wang & Qingyu Guo & Qiaoyun Long & Qing Liu & Ying Cheng & Jin Li & Cynthia Kwan Yui Cheung & Donghai Wu & Xinyu Kong & Yong Xu & Dewei Ye & , 2022. "Adipocyte-derived lactate is a signalling metabolite that potentiates adipose macrophage inflammation via targeting PHD2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Elisa Bellucci & Andrea Benazzo & Chunming Xu & Elena Bitocchi & Monica Rodriguez & Saleh Alseekh & Valerio Di Vittori & Tania Gioia & Kerstin Neumann & Gaia Cortinovis & Giulia Frascarelli & Ester Mu, 2023. "Selection and adaptive introgression guided the complex evolutionary history of the European common bean," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Jiayin Peng & Lili Han & Biao Liu & Jiawen Song & Yuang Wang & Kunpeng Wang & Qian Guo & XinYan Liu & Yu Li & Jujin Zhang & Wenqing Wu & Sheng Li & Xin Fu & Cheng-le Zhuang & Weikang Zhang & Shengbao , 2023. "Gli1 marks a sentinel muscle stem cell population for muscle regeneration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Elisa Setten & Alessandra Castagna & Josué Manik Nava-Sedeño & Jonathan Weber & Roberta Carriero & Andreas Reppas & Valery Volk & Jessica Schmitz & Wilfried Gwinner & Haralampos Hatzikirou & Friedrich, 2022. "Understanding fibrosis pathogenesis via modeling macrophage-fibroblast interplay in immune-metabolic context," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    13. Yanjiang Liu & Gongcheng Hu & Shengxiong Yang & Mingze Yao & Zicong Liu & Chenghong Yan & Yulin Wen & Wangfang Ping & Juehan Wang & Yawei Song & Xiaotao Dong & Guangjin Pan & Hongjie Yao, 2023. "Functional dissection of PRC1 subunits RYBP and YAF2 during neural differentiation of embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Dafne Ibarra-Morales & Michael Rauer & Piergiuseppe Quarato & Leily Rabbani & Fides Zenk & Mariana Schulte-Sasse & Francesco Cardamone & Alejandro Gomez-Auli & Germano Cecere & Nicola Iovino, 2021. "Histone variant H2A.Z regulates zygotic genome activation," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    15. Tingting Bo & Jie Li & Ganlu Hu & Ge Zhang & Wei Wang & Qian Lv & Shaoling Zhao & Junjie Ma & Meng Qin & Xiaohui Yao & Meiyun Wang & Guang-Zhong Wang & Zheng Wang, 2023. "Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    16. Hao Chen & Frederick J. King & Bin Zhou & Yu Wang & Carter J. Canedy & Joel Hayashi & Yang Zhong & Max W. Chang & Lars Pache & Julian L. Wong & Yong Jia & John Joslin & Tao Jiang & Christopher Benner , 2024. "Drug target prediction through deep learning functional representation of gene signatures," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. Matthieu Dos Santos & Akansha M. Shah & Yichi Zhang & Svetlana Bezprozvannaya & Kenian Chen & Lin Xu & Weichun Lin & John R. McAnally & Rhonda Bassel-Duby & Ning Liu & Eric N. Olson, 2023. "Opposing gene regulatory programs governing myofiber development and maturation revealed at single nucleus resolution," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    18. Gaofei Li & Yicong Sun & Immanuel Kwok & Liting Yang & Wanying Wen & Peixian Huang & Mei Wu & Jing Li & Zhibin Huang & Zhaoyuan Liu & Shuai He & Wan Peng & Jin-Xin Bei & Florent Ginhoux & Lai Guan Ng , 2024. "Cebp1 and Cebpβ transcriptional axis controls eosinophilopoiesis in zebrafish," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    19. Mei Zhao & Tianxiao Wang & Frederico O. Gleber-Netto & Zhen Chen & Daniel J. McGrail & Javier A. Gomez & Wutong Ju & Mayur A. Gadhikar & Wencai Ma & Li Shen & Qi Wang & Ximing Tang & Sen Pathak & Mari, 2024. "Mutant p53 gains oncogenic functions through a chromosomal instability-induced cytosolic DNA response," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    20. Yingyan Yu & Zhen Zhang & Xiaorui Dong & Ruixin Yang & Zhongqu Duan & Zhen Xiang & Jun Li & Guichao Li & Fazhe Yan & Hongzhang Xue & Du Jiao & Jinyuan Lu & Huimin Lu & Wenmin Zhang & Yangzhen Wei & Sh, 2022. "Pangenomic analysis of Chinese gastric cancer," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-31759-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.