Modelling post-implantation human development to yolk sac blood emergence

Joshua Hislop, Qi Song, Kamyar Keshavarz F., Amir Alavi, Rayna Schoenberger, Ryan LeGraw, Jeremy J. Velazquez, Tahere Mokhtari, Mohammad Naser Taheri, Matthew Rytel, Susana M. Chuva de Sousa Lopes, Simon Watkins, Donna Stolz, Samira Kiani, Berna Sozen, Ziv Bar-Joseph and Mo R. Ebrahimkhani ()
Additional contact information
Joshua Hislop: University of Pittsburgh
Qi Song: Carnegie Mellon University
Kamyar Keshavarz F.: University of Pittsburgh
Amir Alavi: Carnegie Mellon University
Rayna Schoenberger: University of Pittsburgh
Ryan LeGraw: University of Pittsburgh
Jeremy J. Velazquez: University of Pittsburgh
Tahere Mokhtari: University of Pittsburgh
Mohammad Naser Taheri: University of Pittsburgh
Matthew Rytel: University of Pittsburgh
Susana M. Chuva de Sousa Lopes: Leiden University Medical Center, Einthovenweg
Simon Watkins: University of Pittsburgh
Donna Stolz: University of Pittsburgh
Samira Kiani: University of Pittsburgh
Berna Sozen: Yale University
Ziv Bar-Joseph: Carnegie Mellon University
Mo R. Ebrahimkhani: University of Pittsburgh

Nature, 2024, vol. 626, issue 7998, 367-376

Abstract: Abstract Implantation of the human embryo begins a critical developmental stage that comprises profound events including axis formation, gastrulation and the emergence of haematopoietic system1,2. Our mechanistic knowledge of this window of human life remains limited due to restricted access to in vivo samples for both technical and ethical reasons3–5. Stem cell models of human embryo have emerged to help unlock the mysteries of this stage6–16. Here we present a genetically inducible stem cell-derived embryoid model of early post-implantation human embryogenesis that captures the reciprocal codevelopment of embryonic tissue and the extra-embryonic endoderm and mesoderm niche with early haematopoiesis. This model is produced from induced pluripotent stem cells and shows unanticipated self-organizing cellular programmes similar to those that occur in embryogenesis, including the formation of amniotic cavity and bilaminar disc morphologies as well as the generation of an anterior hypoblast pole and posterior domain. The extra-embryonic layer in these embryoids lacks trophoblast and shows advanced multilineage yolk sac tissue-like morphogenesis that harbours a process similar to distinct waves of haematopoiesis, including the emergence of erythroid-, megakaryocyte-, myeloid- and lymphoid-like cells. This model presents an easy-to-use, high-throughput, reproducible and scalable platform to probe multifaceted aspects of human development and blood formation at the early post-implantation stage. It will provide a tractable human-based model for drug testing and disease modelling.

Date: 2024
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DOI: 10.1038/s41586-023-06914-8

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