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Controlled modelling of human epiblast and amnion development using stem cells

Author

Listed:
  • Yi Zheng

    (University of Michigan)

  • Xufeng Xue

    (University of Michigan)

  • Yue Shao

    (University of Michigan)

  • Sicong Wang

    (University of Michigan)

  • Sajedeh Nasr Esfahani

    (University of Michigan)

  • Zida Li

    (University of Michigan)

  • Jonathon M. Muncie

    (University of California, San Francisco
    University of California, San Francisco and University of California, Berkeley)

  • Johnathon N. Lakins

    (University of California, San Francisco)

  • Valerie M. Weaver

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Deborah L. Gumucio

    (University of Michigan Medical School)

  • Jianping Fu

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

Abstract

Early human embryonic development involves extensive lineage diversification, cell-fate specification and tissue patterning1. Despite its basic and clinical importance, early human embryonic development remains relatively unexplained owing to interspecies divergence2,3 and limited accessibility to human embryo samples. Here we report that human pluripotent stem cells (hPSCs) in a microfluidic device recapitulate, in a highly controllable and scalable fashion, landmarks of the development of the epiblast and amniotic ectoderm parts of the conceptus, including lumenogenesis of the epiblast and the resultant pro-amniotic cavity, formation of a bipolar embryonic sac, and specification of primordial germ cells and primitive streak cells. We further show that amniotic ectoderm-like cells function as a signalling centre to trigger the onset of gastrulation-like events in hPSCs. Given its controllability and scalability, the microfluidic model provides a powerful experimental system to advance knowledge of human embryology and reproduction. This model could assist in the rational design of differentiation protocols of hPSCs for disease modelling and cell therapy, and in high-throughput drug and toxicity screens to prevent pregnancy failure and birth defects.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:573:y:2019:i:7774:d:10.1038_s41586-019-1535-2
    DOI: 10.1038/s41586-019-1535-2
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    Citations

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    Cited by:

    1. 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.
    2. Norio Kobayashi & Hiroaki Okae & Hitoshi Hiura & Naoto Kubota & Eri H. Kobayashi & Shun Shibata & Akira Oike & Takeshi Hori & Chie Kikutake & Hirotaka Hamada & Hirokazu Kaji & Mikita Suyama & Marie-Li, 2022. "The microRNA cluster C19MC confers differentiation potential into trophoblast lineages upon human pluripotent stem cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Mingyue Guo & Jinyi Wu & Chuanxin Chen & Xinggu Wang & An Gong & Wei Guan & Rowan M. Karvas & Kexin Wang & Mingwei Min & Yixuan Wang & Thorold W. Theunissen & Shaorong Gao & José C. R. Silva, 2024. "Self-renewing human naïve pluripotent stem cells dedifferentiate in 3D culture and form blastoids spontaneously," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Gawoon Shim & Isaac B. Breinyn & Alejandro Martínez-Calvo & Sameeksha Rao & Daniel J. Cohen, 2024. "Bioelectric stimulation controls tissue shape and size," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Hyung Chul Lee & Nidia M. M. Oliveira & Cato Hastings & Peter Baillie-Benson & Adam A. Moverley & Hui-Chun Lu & Yi Zheng & Elise L. Wilby & Timothy T. Weil & Karen M. Page & Jianping Fu & Naomi Moris , 2024. "Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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