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Amnion signals are essential for mesoderm formation in primates

Author

Listed:
  • Ran Yang

    (Karolinska Institutet)

  • Alexander Goedel

    (Karolinska Institutet)

  • Yu Kang

    (Kunming University of Science and Technology)

  • Chenyang Si

    (Kunming University of Science and Technology)

  • Chu Chu

    (Kunming University of Science and Technology)

  • Yi Zheng

    (University of Michigan)

  • Zhenzhen Chen

    (Kunming University of Science and Technology)

  • Peter J. Gruber

    (Karolinska Institutet
    Yale University)

  • Yao Xiao

    (Karolinska Institutet)

  • Chikai Zhou

    (Karolinska Institutet)

  • Nevin Witman

    (Karolinska Institutet)

  • Elif Eroglu

    (Karolinska Institutet)

  • Chuen-Yan Leung

    (Karolinska Institutet)

  • Yongchang Chen

    (Kunming University of Science and Technology)

  • Jianping Fu

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

  • Weizhi Ji

    (Kunming University of Science and Technology)

  • Fredrik Lanner

    (Karolinska Institutet
    Karolinska Universitetssjukhuset
    Karolinska Institutet)

  • Yuyu Niu

    (Kunming University of Science and Technology
    Kunming University of Science and Technology)

  • Kenneth R. Chien

    (Karolinska Institutet)

Abstract

Embryonic development is largely conserved among mammals. However, certain genes show divergent functions. By generating a transcriptional atlas containing >30,000 cells from post-implantation non-human primate embryos, we uncover that ISL1, a gene with a well-established role in cardiogenesis, controls a gene regulatory network in primate amnion. CRISPR/Cas9-targeting of ISL1 results in non-human primate embryos which do not yield viable offspring, demonstrating that ISL1 is critically required in primate embryogenesis. On a cellular level, mutant ISL1 embryos display a failure in mesoderm formation due to reduced BMP4 signaling from the amnion. Via loss of function and rescue studies in human embryonic stem cells we confirm a similar role of ISL1 in human in vitro derived amnion. This study highlights the importance of the amnion as a signaling center during primate mesoderm formation and demonstrates the potential of in vitro primate model systems to dissect the genetics of early human embryonic development.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25186-2
    DOI: 10.1038/s41467-021-25186-2
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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. Nevin Witman & Chikai Zhou & Timm Häneke & Yao Xiao & Xiaoting Huang & Eduarde Rohner & Jesper Sohlmér & Niels Grote Beverborg & Miia L. Lehtinen & Kenneth R. Chien & Makoto Sahara, 2023. "Placental growth factor exerts a dual function for cardiomyogenesis and vasculogenesis during heart development," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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