IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36284-8.html
   My bibliography  Save this article

Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats

Author

Listed:
  • Miguel Angel Brieño-Enríquez

    (University of Pittsburgh
    University of Pittsburgh School of Medicine)

  • Mariela Faykoo-Martinez

    (University of Toronto
    University of Toronto, Mississauga
    The Hospital for Sick Children)

  • Meagan Goben

    (University of Pittsburgh)

  • Jennifer K. Grenier

    (Cornell University)

  • Ashley McGrath

    (Cornell University)

  • Alexandra M. Prado

    (Cornell University)

  • Jacob Sinopoli

    (Cornell University)

  • Kate Wagner

    (Cornell University)

  • Patrick T. Walsh

    (University of Pittsburgh)

  • Samia H. Lopa

    (University of Pittsburgh)

  • Diana J. Laird

    (University of California San Francisco)

  • Paula E. Cohen

    (Cornell University)

  • Michael D. Wilson

    (The Hospital for Sick Children
    University of Toronto)

  • Melissa M. Holmes

    (University of Toronto
    University of Toronto, Mississauga)

  • Ned J. Place

    (Cornell University)

Abstract

In the long-lived naked mole-rat (NMR), the entire process of oogenesis occurs postnatally. Germ cell numbers increase significantly in NMRs between postnatal days 5 (P5) and P8, and germs cells positive for proliferation markers (Ki-67, pHH3) are present at least until P90. Using pluripotency markers (SOX2 and OCT4) and the primordial germ cell (PGC) marker BLIMP1, we show that PGCs persist up to P90 alongside germ cells in all stages of female differentiation and undergo mitosis both in vivo and in vitro. We identified VASA+ SOX2+ cells at 6 months and at 3-years in subordinate and reproductively activated females. Reproductive activation was associated with proliferation of VASA+ SOX2+ cells. Collectively, our results suggest that highly desynchronized germ cell development and the maintenance of a small population of PGCs that can expand upon reproductive activation are unique strategies that could help to maintain the NMR’s ovarian reserve for its 30-year reproductive lifespan.

Suggested Citation

  • Miguel Angel Brieño-Enríquez & Mariela Faykoo-Martinez & Meagan Goben & Jennifer K. Grenier & Ashley McGrath & Alexandra M. Prado & Jacob Sinopoli & Kate Wagner & Patrick T. Walsh & Samia H. Lopa & Di, 2023. "Postnatal oogenesis leads to an exceptionally large ovarian reserve in naked mole-rats," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36284-8
    DOI: 10.1038/s41467-023-36284-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36284-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36284-8?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. W Hamish B Wallace & Thomas W Kelsey, 2010. "Human Ovarian Reserve from Conception to the Menopause," PLOS ONE, Public Library of Science, vol. 5(1), pages 1-9, January.
    2. Margarida Cardoso-Moreira & Jean Halbert & Delphine Valloton & Britta Velten & Chunyan Chen & Yi Shao & Angélica Liechti & Kelly Ascenção & Coralie Rummel & Svetlana Ovchinnikova & Pavel V. Mazin & Io, 2019. "Gene expression across mammalian organ development," Nature, Nature, vol. 571(7766), pages 505-509, July.
    3. Xiao Tian & Jorge Azpurua & Christopher Hine & Amita Vaidya & Max Myakishev-Rempel & Julia Ablaeva & Zhiyong Mao & Eviatar Nevo & Vera Gorbunova & Andrei Seluanov, 2013. "High-molecular-mass hyaluronan mediates the cancer resistance of the naked mole rat," Nature, Nature, vol. 499(7458), pages 346-349, July.
    4. Shingo Miyawaki & Yoshimi Kawamura & Yuki Oiwa & Atsushi Shimizu & Tsuyoshi Hachiya & Hidemasa Bono & Ikuko Koya & Yohei Okada & Tokuhiro Kimura & Yoshihiro Tsuchiya & Sadafumi Suzuki & Nobuyuki Onish, 2016. "Tumour resistance in induced pluripotent stem cells derived from naked mole-rats," Nature Communications, Nature, vol. 7(1), pages 1-9, September.
    5. Yasuhide Ohinata & Bernhard Payer & Dónal O'Carroll & Katia Ancelin & Yukiko Ono & Mitsue Sano & Sheila C. Barton & Tetyana Obukhanych & Michel Nussenzweig & Alexander Tarakhovsky & Mitinori Saitou & , 2005. "Blimp1 is a critical determinant of the germ cell lineage in mice," Nature, Nature, vol. 436(7048), pages 207-213, July.
    6. 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.
    7. Fumio Nakaki & Katsuhiko Hayashi & Hiroshi Ohta & Kazuki Kurimoto & Yukihiro Yabuta & Mitinori Saitou, 2013. "Induction of mouse germ-cell fate by transcription factors in vitro," Nature, Nature, vol. 501(7466), pages 222-226, September.
    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. Shengyong Yu & Chunhua Zhou & Jiangping He & Zhaokai Yao & Xingnan Huang & Bowen Rong & Hong Zhu & Shijie Wang & Shuyan Chen & Xialian Wang & Baomei Cai & Guoqing Zhao & Yuhan Chen & Lizhan Xiao & He , 2022. "BMP4 drives primed to naïve transition through PGC-like state," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Shamir Montazid & Sheila Bandyopadhyay & Daniel W. Hart & Nan Gao & Brian Johnson & Sri G. Thrumurthy & Dustin J. Penn & Bettina Wernisch & Mukesh Bansal & Philipp M. Altrock & Fabian Rost & Patrycja , 2023. "Adult stem cell activity in naked mole rats for long-term tissue maintenance," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Jiexiang Zhao & Ping Lu & Cong Wan & Yaping Huang & Manman Cui & Xinyan Yang & Yuqiong Hu & Yi Zheng & Ji Dong & Mei Wang & Shu Zhang & Zhaoting Liu & Shuhui Bian & Xiaoman Wang & Rui Wang & Shaofang , 2021. "Cell-fate transition and determination analysis of mouse male germ cells throughout development," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    4. Feifei Yuan & Jihong Yang & Fanglin Ma & Zhe Hu & Vikas Malik & Ruge Zang & Dan Li & Xianle Shi & Xin Huang & Hongwei Zhou & Jianlong Wang, 2025. "Pluripotency factor Tex10 finetunes Wnt signaling for spermatogenesis and primordial germ cell development," Nature Communications, Nature, vol. 16(1), pages 1-22, December.
    5. Tzuhua D. Lin & Nimrod D. Rubinstein & Nicole L. Fong & Megan Smith & Wendy Craft & Baby Martin-McNulty & Rebecca Perry & Martha A. Delaney & Margaret A. Roy & Rochelle Buffenstein, 2024. "Evolution of T cells in the cancer-resistant naked mole-rat," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    6. Amir Dailamy & Weiqi Lyu & Sami Nourreddine & Michael Tong & Joseph Rainaldi & Daniella McDonald & Rebecca Panwala & Alysson Muotri & Michael S. Breen & Kun Zhang & Prashant Mali, 2024. "Charting and probing the activity of ADARs in human development and cell-fate specification," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Gershoni, Naomi & Low, Corinne, 2021. "The power of time: The impact of free IVF on Women’s human capital investments," European Economic Review, Elsevier, vol. 133(C).
    8. Tran N. Chau & Prakash Raj Timilsena & Sai Pavan Bathala & Sanchari Kundu & Bastiaan O. R. Bargmann & Song Li, 2025. "Orthologous marker groups reveal broad cell identity conservation across plant single-cell transcriptomes," Nature Communications, Nature, vol. 16(1), pages 1-11, December.
    9. Michael Travisano & Michihisa Maeda & Fumie Fuji & Toshiaki Kudo, 2018. "Rapid adaptation to near extinction in microbial experimental evolution," Journal of Bioeconomics, Springer, vol. 20(1), pages 141-152, April.
    10. Iqra Saani & Nitish Raj & Raja Sood & Shahbaz Ansari & Haider Abbas Mandviwala & Elisabet Sanchez & Stergios Boussios, 2023. "Clinical Challenges in the Management of Malignant Ovarian Germ Cell Tumours," IJERPH, MDPI, vol. 20(12), pages 1-16, June.
    11. Naomi Gershoni & Corinne Low, 2021. "Older Yet Fairer: How Extended Reproductive Time Horizons Reshaped Marriage Patterns in Israel," American Economic Journal: Applied Economics, American Economic Association, vol. 13(1), pages 198-234, January.
    12. Michelle K. Y. Seah & Brenda Y. Han & Yan Huang & Louise J. H. Rasmussen & Andrina J. Stäubli & Judith Bello-Rodríguez & Andrew Chi-Ho Chan & Maxime Gasnier & Heike Wollmann & Ernesto Guccione & Danie, 2025. "Maternal PRDM10 activates essential genes for oocyte-to-embryo transition," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    13. Marie Sémon & Marion Mouginot & Manon Peltier & Claudine Corneloup & Philippe Veber & Laurent Guéguen & Sophie Pantalacci, 2025. "Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
    14. Thomas W Kelsey & Eleanor Ginbey & Moti M Chowdhury & Louise E Bath & Richard A Anderson & W Hamish B Wallace, 2016. "A Validated Normative Model for Human Uterine Volume from Birth to Age 40 Years," PLOS ONE, Public Library of Science, vol. 11(6), pages 1-14, June.
    15. Thomas W Kelsey & Lucy Q Li & Rod T Mitchell & Ashley Whelan & Richard A Anderson & W Hamish B Wallace, 2014. "A Validated Age-Related Normative Model for Male Total Testosterone Shows Increasing Variance but No Decline after Age 40 Years," PLOS ONE, Public Library of Science, vol. 9(10), pages 1-11, October.
    16. Juexin Wang & Jinpu Li & Skyler T. Kramer & Li Su & Yuzhou Chang & Chunhui Xu & Michael T. Eadon & Krzysztof Kiryluk & Qin Ma & Dong Xu, 2023. "Dimension-agnostic and granularity-based spatially variable gene identification using BSP," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Tara N. Yankee & Sungryong Oh & Emma Wentworth Winchester & Andrea Wilderman & Kelsey Robinson & Tia Gordon & Jill A. Rosenfeld & Jennifer VanOudenhove & Daryl A. Scott & Elizabeth J. Leslie & Justin , 2023. "Integrative analysis of transcriptome dynamics during human craniofacial development identifies candidate disease genes," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    18. Marion Müller & Rose Eghbalian & Jes-Niels Boeckel & Karen S. Frese & Jan Haas & Elham Kayvanpour & Farbod Sedaghat-Hamedani & Maximilian K. Lackner & Oguz F. Tugrul & Thomas Ruppert & Rewati Tappu & , 2022. "NIMA-related kinase 9 regulates the phosphorylation of the essential myosin light chain in the heart," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    19. Rong Hua & Yuan-Shuo Ma & Lu Yang & Jun-Jun Hao & Qin-Yang Hua & Lu-Ye Shi & Xiao-Qing Yao & Hao-Yu Zhi & Zhen Liu, 2024. "Experimental evidence for cancer resistance in a bat species," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Guillem Sanchez Sanchez & Stephan Emmrich & Maria Georga & Ariadni Papadaki & Sofia Kossida & Andrei Seluanov & Vera Gorbunova & David Vermijlen, 2024. "Invariant γδTCR natural killer-like effector T cells in the naked mole-rat," Nature Communications, Nature, vol. 15(1), pages 1-17, 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:14:y:2023:i:1:d:10.1038_s41467-023-36284-8. 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.