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Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis

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  • Lu Han

    (University of Cincinnati, College of Medicine)

  • Praneet Chaturvedi

    (University of Cincinnati, College of Medicine)

  • Keishi Kishimoto

    (University of Cincinnati, College of Medicine
    RIKEN Center for Biosystems Dynamics Research (BDR)
    Cincinnati Children’s Hospital)

  • Hiroyuki Koike

    (University of Cincinnati, College of Medicine)

  • Talia Nasr

    (University of Cincinnati, College of Medicine)

  • Kentaro Iwasawa

    (University of Cincinnati, College of Medicine)

  • Kirsten Giesbrecht

    (University of Cincinnati, College of Medicine)

  • Phillip C. Witcher

    (University of Cincinnati, College of Medicine)

  • Alexandra Eicher

    (University of Cincinnati, College of Medicine)

  • Lauren Haines

    (University of Cincinnati, College of Medicine)

  • Yarim Lee

    (University of Cincinnati, College of Medicine)

  • John M. Shannon

    (University of Cincinnati, College of Medicine)

  • Mitsuru Morimoto

    (RIKEN Center for Biosystems Dynamics Research (BDR)
    Cincinnati Children’s Hospital)

  • James M. Wells

    (University of Cincinnati, College of Medicine)

  • Takanori Takebe

    (University of Cincinnati, College of Medicine)

  • Aaron M. Zorn

    (University of Cincinnati, College of Medicine
    Cincinnati Children’s Hospital)

Abstract

Visceral organs, such as the lungs, stomach and liver, are derived from the fetal foregut through a series of inductive interactions between the definitive endoderm (DE) and the surrounding splanchnic mesoderm (SM). While DE patterning is fairly well studied, the paracrine signaling controlling SM regionalization and how this is coordinated with epithelial identity is obscure. Here, we use single cell transcriptomics to generate a high-resolution cell state map of the embryonic mouse foregut. This identifies a diversity of SM cell types that develop in close register with the organ-specific epithelium. We infer a spatiotemporal signaling network of endoderm-mesoderm interactions that orchestrate foregut organogenesis. We validate key predictions with mouse genetics, showing the importance of endoderm-derived signals in mesoderm patterning. Finally, leveraging these signaling interactions, we generate different SM subtypes from human pluripotent stem cells (hPSCs), which previously have been elusive. The single cell data can be explored at: https://research.cchmc.org/ZornLab-singlecell .

Suggested Citation

  • Lu Han & Praneet Chaturvedi & Keishi Kishimoto & Hiroyuki Koike & Talia Nasr & Kentaro Iwasawa & Kirsten Giesbrecht & Phillip C. Witcher & Alexandra Eicher & Lauren Haines & Yarim Lee & John M. Shanno, 2020. "Single cell transcriptomics identifies a signaling network coordinating endoderm and mesoderm diversification during foregut organogenesis," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17968-x
    DOI: 10.1038/s41467-020-17968-x
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    Cited by:

    1. Karin D. Prummel & Helena L. Crowell & Susan Nieuwenhuize & Eline C. Brombacher & Stephan Daetwyler & Charlotte Soneson & Jelena Kresoja-Rakic & Agnese Kocere & Manuel Ronner & Alexander Ernst & Zahra, 2022. "Hand2 delineates mesothelium progenitors and is reactivated in mesothelioma," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Lu Han & Yongxia Wu & Kun Fang & Sean Sweeney & Ulyss K. Roesner & Melodie Parrish & Khushbu Patel & Tom Walter & Julia Piermattei & Anthony Trimboli & Julia Lefler & Cynthia D. Timmers & Xue-Zhong Yu, 2023. "The splanchnic mesenchyme is the tissue of origin for pancreatic fibroblasts during homeostasis and tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    3. Andrea B. Alber & Hector A. Marquez & Liang Ma & George Kwong & Bibek R. Thapa & Carlos Villacorta-Martin & Jonathan Lindstrom-Vautrin & Pushpinder Bawa & Feiya Wang & Yongfeng Luo & Laertis Ikonomou , 2023. "Directed differentiation of mouse pluripotent stem cells into functional lung-specific mesenchyme," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Ryan J. Smith & Hongpan Zhang & Shengen Shawn Hu & Theodora Yung & Roshane Francis & Lilian Lee & Mark W. Onaitis & Peter B. Dirks & Chongzhi Zang & Tae-Hee Kim, 2022. "Single-cell chromatin profiling of the primitive gut tube reveals regulatory dynamics underlying lineage fate decisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Shunsuke Tanigawa & Etsuko Tanaka & Koichiro Miike & Tomoko Ohmori & Daisuke Inoue & Chen-Leng Cai & Atsuhiro Taguchi & Akio Kobayashi & Ryuichi Nishinakamura, 2022. "Generation of the organotypic kidney structure by integrating pluripotent stem cell-derived renal stroma," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Andrea Toth & Paranthaman Kannan & John Snowball & Matthew Kofron & Joseph A. Wayman & James P. Bridges & Emily R. Miraldi & Daniel Swarr & William J. Zacharias, 2023. "Alveolar epithelial progenitor cells require Nkx2-1 to maintain progenitor-specific epigenomic state during lung homeostasis and regeneration," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    7. Mariana A. Branco & Tiago P. Dias & Joaquim M. S. Cabral & Perpetua Pinto-do-Ó & Maria Margarida Diogo, 2022. "Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid," Nature Communications, Nature, vol. 13(1), pages 1-18, December.

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