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Derivation of human primordial germ cell-like cells in an embryonic-like culture

Author

Listed:
  • Sajedeh Nasr Esfahani

    (University of Michigan)

  • Yi Zheng

    (University of Michigan
    Syracuse University)

  • Auriana Arabpour

    (University of California, Los Angeles
    University of California, Los Angeles
    University of California, Los Angeles)

  • Agnes M. Resto Irizarry

    (University of Michigan)

  • Norio Kobayashi

    (University of Michigan)

  • Xufeng Xue

    (University of Michigan)

  • Yue Shao

    (Tsinghua University)

  • Cheng Zhao

    (Division of Obstetrics and Gynecology, Karolinska Instituet)

  • Nicole L. Agranonik

    (University of California, Los Angeles)

  • Megan Sparrow

    (University of California, Los Angeles)

  • Timothy J. Hunt

    (University of California, Los Angeles)

  • Jared Faith

    (University of California, Los Angeles)

  • Mary Jasmine Lara

    (University of California, Los Angeles)

  • Qiu Ya Wu

    (University of California, Los Angeles)

  • Sherman Silber

    (Infertility Center of St. Louis, St. Luke’s Hospital)

  • Sophie Petropoulos

    (Division of Obstetrics and Gynecology, Karolinska Instituet
    Université de Montréal
    Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Axe Immunopathologie
    Université de Montréal)

  • Ran Yang

    (Karolinska Institutet)

  • Kenneth R. Chien

    (Karolinska Institutet)

  • Amander T. Clark

    (University of California, Los Angeles
    University of California, Los Angeles
    University of California, Los Angeles)

  • Jianping Fu

    (University of Michigan
    University of Michigan Medical School
    University of Michigan)

Abstract

Primordial germ cells (PGCs) are the embryonic precursors of sperm and eggs. They transmit genetic and epigenetic information across generations. Given the prominent role of germline defects in diseases such as infertility, detailed understanding of human PGC (hPGC) development has important implications in reproductive medicine and studying human evolution. Yet, hPGC specification remains an elusive process. Here, we report the induction of hPGC-like cells (hPGCLCs) in a bioengineered human pluripotent stem cell (hPSC) culture that mimics peri-implantation human development. In this culture, amniotic ectoderm-like cells (AMLCs), derived from hPSCs, induce hPGCLC specification from hPSCs through paracrine signaling downstream of ISL1. Our data further show functional roles of NODAL, WNT, and BMP signaling in hPGCLC induction. hPGCLCs are successfully derived from eight non-obstructive azoospermia (NOA) participant-derived hPSC lines using this biomimetic platform, demonstrating its promise for screening applications.

Suggested Citation

  • Sajedeh Nasr Esfahani & Yi Zheng & Auriana Arabpour & Agnes M. Resto Irizarry & Norio Kobayashi & Xufeng Xue & Yue Shao & Cheng Zhao & Nicole L. Agranonik & Megan Sparrow & Timothy J. Hunt & Jared Fai, 2024. "Derivation of human primordial germ cell-like cells in an embryonic-like culture," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43871-2
    DOI: 10.1038/s41467-023-43871-2
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    1. Ran Yang & Alexander Goedel & Yu Kang & Chenyang Si & Chu Chu & Yi Zheng & Zhenzhen Chen & Peter J. Gruber & Yao Xiao & Chikai Zhou & Nevin Witman & Elif Eroglu & Chuen-Yan Leung & Yongchang Chen & Ji, 2021. "Amnion signals are essential for mesoderm formation in primates," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Anna D. Senft & Elizabeth K. Bikoff & Elizabeth J. Robertson & Ita Costello, 2019. "Genetic dissection of Nodal and Bmp signalling requirements during primordial germ cell development in mouse," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    3. Sulagna Ghosh & Ralda Nehme & Lindy E. Barrett, 2022. "Greater genetic diversity is needed in human pluripotent stem cell models," Nature Communications, Nature, vol. 13(1), pages 1-7, December.
    4. Lifeng Xiang & Yu Yin & Yun Zheng & Yanping Ma & Yonggang Li & Zhigang Zhao & Junqiang Guo & Zongyong Ai & Yuyu Niu & Kui Duan & Jingjing He & Shuchao Ren & Dan Wu & Yun Bai & Zhouchun Shang & Xi Dai , 2020. "A developmental landscape of 3D-cultured human pre-gastrulation embryos," Nature, Nature, vol. 577(7791), pages 537-542, January.
    5. Toshihiro Kobayashi & Haixin Zhang & Walfred W. C. Tang & Naoko Irie & Sarah Withey & Doris Klisch & Anastasiya Sybirna & Sabine Dietmann & David A. Contreras & Robert Webb & Cinzia Allegrucci & Ramir, 2017. "Principles of early human development and germ cell program from conserved model systems," Nature, Nature, vol. 546(7658), pages 416-420, June.
    6. Yi Zheng & Xufeng Xue & Yue Shao & Sicong Wang & Sajedeh Nasr Esfahani & Zida Li & Jonathon M. Muncie & Johnathon N. Lakins & Valerie M. Weaver & Deborah L. Gumucio & Jianping Fu, 2019. "Controlled modelling of human epiblast and amnion development using stem cells," Nature, Nature, vol. 573(7774), pages 421-425, September.
    7. Tomonori Nakamura & Ikuhiro Okamoto & Kotaro Sasaki & Yukihiro Yabuta & Chizuru Iwatani & Hideaki Tsuchiya & Yasunari Seita & Shinichiro Nakamura & Takuya Yamamoto & Mitinori Saitou, 2016. "A developmental coordinate of pluripotency among mice, monkeys and humans," Nature, Nature, vol. 537(7618), pages 57-62, September.
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