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Bidirectional Wnt signaling between endoderm and mesoderm confers tracheal identity in mouse and human cells

Author

Listed:
  • Keishi Kishimoto

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

  • Kana T. Furukawa

    (Riken Center for Biosystems Dynamics Research (BDR))

  • Agustin Luz-Madrigal

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center)

  • Akira Yamaoka

    (Riken Center for Biosystems Dynamics Research (BDR))

  • Chisa Matsuoka

    (Riken Center for Biosystems Dynamics Research (BDR))

  • Masanobu Habu

    (Kyoto University)

  • Cantas Alev

    (Kyoto University
    Kyoto University)

  • Aaron M. Zorn

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center)

  • Mitsuru Morimoto

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

Abstract

The periodic cartilage and smooth muscle structures in mammalian trachea are derived from tracheal mesoderm, and tracheal malformations result in serious respiratory defects in neonates. Here we show that canonical Wnt signaling in mesoderm is critical to confer trachea mesenchymal identity in human and mouse. At the initiation of tracheal development, endoderm begins to express Nkx2.1, and then mesoderm expresses the Tbx4 gene. Loss of β-catenin in fetal mouse mesoderm causes loss of Tbx4+ tracheal mesoderm and tracheal cartilage agenesis. The mesenchymal Tbx4 expression relies on endodermal Wnt activation and Wnt ligand secretion but is independent of known Nkx2.1-mediated respiratory development, suggesting that bidirectional Wnt signaling between endoderm and mesoderm promotes trachea development. Activating Wnt, Bmp signaling in mouse embryonic stem cell (ESC)-derived lateral plate mesoderm (LPM) generates tracheal mesoderm containing chondrocytes and smooth muscle cells. For human ESC-derived LPM, SHH activation is required along with WNT to generate proper tracheal mesoderm. Together, these findings may contribute to developing applications for human tracheal tissue repair.

Suggested Citation

  • Keishi Kishimoto & Kana T. Furukawa & Agustin Luz-Madrigal & Akira Yamaoka & Chisa Matsuoka & Masanobu Habu & Cantas Alev & Aaron M. Zorn & Mitsuru Morimoto, 2020. "Bidirectional Wnt signaling between endoderm and mesoderm confers tracheal identity in mouse and human cells," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17969-w
    DOI: 10.1038/s41467-020-17969-w
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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. 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.

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