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An in vitro model of early anteroposterior organization during human development

Author

Listed:
  • Naomi Moris

    (University of Cambridge)

  • Kerim Anlas

    (University of Cambridge
    European Molecular Biology Laboratory (EMBL) Barcelona)

  • Susanne C. van den Brink

    (Oncode Institute, Hubrecht Institute-KNAW (Royal Netherlands Academy of Arts and Sciences) and University Medical Center Utrecht)

  • Anna Alemany

    (Oncode Institute, Hubrecht Institute-KNAW (Royal Netherlands Academy of Arts and Sciences) and University Medical Center Utrecht)

  • Julia Schröder

    (University of Cambridge
    Heidelberg University)

  • Sabitri Ghimire

    (University of Cambridge)

  • Tina Balayo

    (University of Cambridge
    Universidad de las Palmas de Gran Canaria (ULPGC))

  • Alexander van Oudenaarden

    (Oncode Institute, Hubrecht Institute-KNAW (Royal Netherlands Academy of Arts and Sciences) and University Medical Center Utrecht)

  • Alfonso Martinez Arias

    (University of Cambridge)

Abstract

The body plan of the mammalian embryo is shaped through the process of gastrulation, an early developmental event that transforms an isotropic group of cells into an ensemble of tissues that is ordered with reference to three orthogonal axes1. Although model organisms have provided much insight into this process, we know very little about gastrulation in humans, owing to the difficulty of obtaining embryos at such early stages of development and the ethical and technical restrictions that limit the feasibility of observing gastrulation ex vivo2. Here we show that human embryonic stem cells can be used to generate gastruloids—three-dimensional multicellular aggregates that differentiate to form derivatives of the three germ layers organized spatiotemporally, without additional extra-embryonic tissues. Human gastruloids undergo elongation along an anteroposterior axis, and we use spatial transcriptomics to show that they exhibit patterned gene expression. This includes a signature of somitogenesis that suggests that 72-h human gastruloids show some features of Carnegie-stage-9 embryos3. Our study represents an experimentally tractable model system to reveal and examine human-specific regulatory processes that occur during axial organization in early development.

Suggested Citation

  • Naomi Moris & Kerim Anlas & Susanne C. van den Brink & Anna Alemany & Julia Schröder & Sabitri Ghimire & Tina Balayo & Alexander van Oudenaarden & Alfonso Martinez Arias, 2020. "An in vitro model of early anteroposterior organization during human development," Nature, Nature, vol. 582(7812), pages 410-415, June.
  • Handle: RePEc:nat:nature:v:582:y:2020:i:7812:d:10.1038_s41586-020-2383-9
    DOI: 10.1038/s41586-020-2383-9
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    Citations

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    Cited by:

    1. Ana Sousa-Ortega & Javier Vázquez-Marín & Estefanía Sanabria-Reinoso & Jorge Corbacho & Rocío Polvillo & Alejandro Campoy-López & Lorena Buono & Felix Loosli & María Almuedo-Castillo & Juan R. Martíne, 2023. "A Yap-dependent mechanoregulatory program sustains cell migration for embryo axis assembly," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Anchel de Jaime-Soguero & Janina Hattemer & Anja Bufe & Alexander Haas & Jeroen Berg & Vincent Batenburg & Biswajit Das & Barbara Marco & Stefania Androulaki & Nicolas Böhly & Jonathan J. M. Landry & , 2024. "Developmental signals control chromosome segregation fidelity during pluripotency and neurogenesis by modulating replicative stress," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    3. Daniele Kunz & Anfu Wang & Chon U Chan & Robyn H. Pritchard & Wenyu Wang & Filomena Gallo & Charles R. Bradshaw & Elisa Terenzani & Karin H. Müller & Yan Yan Shery Huang & Fengzhu Xiong, 2023. "Downregulation of extraembryonic tension controls body axis formation in avian embryos," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Marina Sanaki-Matsumiya & Mitsuhiro Matsuda & Nicola Gritti & Fumio Nakaki & James Sharpe & Vikas Trivedi & Miki Ebisuya, 2022. "Periodic formation of epithelial somites from human pluripotent stem cells," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Cassie L. Kemmler & Jana Smolikova & Hannah R. Moran & Brandon J. Mannion & Dunja Knapp & Fabian Lim & Anna Czarkwiani & Viviana Hermosilla Aguayo & Vincent Rapp & Olivia E. Fitch & Seraina Bötschi & , 2023. "Conserved enhancers control notochord expression of vertebrate Brachyury," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. 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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