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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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    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.
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