1. Developmental Biology

The cardiopharyngeal mesoderm contributes to lymphatic vessel development in mouse

  1. Kazuaki Maruyama  Is a corresponding author
  2. Sachiko Miyagawa-Tomita
  3. Yuka Haneda
  4. Mayuko Kida
  5. Fumio Matsuzaki
  6. Kyoko Imanaka-Yoshida
  7. Hiroki Kurihara  Is a corresponding author
  1. University of Tokyo, Japan
  2. Yamazaki University of Animal Health Technology, Japan
  3. RIKEN Center for Biosystems Dynamics Research, Japan
  4. Mie University, Japan
https://doi.org/10.7554/eLife.81515
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Cite this article
  1. Kazuaki Maruyama
  2. Sachiko Miyagawa-Tomita
  3. Yuka Haneda
  4. Mayuko Kida
  5. Fumio Matsuzaki
  6. Kyoko Imanaka-Yoshida
  7. Hiroki Kurihara
(2022)
The cardiopharyngeal mesoderm contributes to lymphatic vessel development in mouse
eLife 11:e81515.
https://doi.org/10.7554/eLife.81515
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Abstract

Lymphatic vessels are crucial for tissue homeostasis and immune responses in vertebrates. Recent studies have demonstrated that lymphatic endothelial cells (LECs) arise from both venous sprouting (lymphangiogenesis) and de novo production from non-venous origins (lymphvasculogenesis), which is similar to blood vessel formation through angiogenesis and vasculogenesis. However, the contribution of LECs from non-venous origins to lymphatic networks is considered to be relatively small. Here, we identify the Islet1 (Isl1)-expressing cardiopharyngeal mesoderm (CPM) as a non-venous origin of craniofacial and cardiac LECs. Genetic lineage tracing with Isl1Cre/+ and Isl1CreERT2/+ mice suggested that a subset of CPM cells gives rise to LECs. These CPM-derived LECs are distinct from venous-derived LECs in terms of their developmental processes and anatomical locations. Later, they form the craniofacial and cardiac lymphatic vascular networks in collaboration with venous-derived LECs. Collectively, our results demonstrate that there are two major sources of LECs, the cardinal vein and the CPM. As the CPM is evolutionarily conserved, these findings may improve our understanding of the evolution of lymphatic vessel development across species. Most importantly, our findings may provide clues to the pathogenesis of lymphatic malformations, which most often develop in the craniofacial and mediastinal regions.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figure 1H-source data 1, Figure 2 - Figure supplement 1I-source data 1, Figure 2H-source data 1, Figure 2P-source data 1, Figure 4O-source data 1, Figure 5 - Figure supplement 1A-F-source data 1, Figure 5 - Figure supplement 1O and P-source data 1, Figure 5K-R-source data 1, and Figure 6-Figure supplement 2-source data1.

Article and author information

Author details

  1. Kazuaki Maruyama

    Department of Physiological Chemistry and Metabolism, University of Tokyo, Bunkyo-ku, Japan
    For correspondence
    k.maruyama0608@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3935-328X

  2. Sachiko Miyagawa-Tomita

    Department of Animal Nursing Science, Yamazaki University of Animal Health Technology, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.

  3. Yuka Haneda

    Department of Physiological Chemistry and Metabolism, University of Tokyo, Bunkyo-ku, Japan
    Competing interests
    The authors declare that no competing interests exist.

  4. Mayuko Kida

    Department of Physiological Chemistry and Metabolism, University of Tokyo, Bunkyo-ku, Japan
    Competing interests
    The authors declare that no competing interests exist.

  5. Fumio Matsuzaki

    Laboratory for Cell Asymmetry, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7902-4520

  6. Kyoko Imanaka-Yoshida

    Department of Pathology and Matrix Biology, Mie University, Mie, Japan
    Competing interests
    The authors declare that no competing interests exist.

  7. Hiroki Kurihara

    Department of Physiological Chemistry and Metabolism, University of Tokyo, Bunkyo-ku, Japan
    For correspondence
    kuri-tky@umin.net
    Competing interests
    The authors declare that no competing interests exist.

Funding

Core Research for Evolutional Science and Technology (JPMJCR13W2)

  • Hiroki Kurihara

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Oliver A Stone, University of Oxford, United Kingdom

Ethics

Animal experimentation: All animal experiments were approved by the University of Tokyo (ethical approval number: H17-250) and Mie University (ethical approval number: 728) animal care and use committee, and were performed in accordance with institutional guidelines.

Version history

  1. Preprint posted: April 1, 2022 (view preprint)
  2. Received: July 4, 2022
  3. Accepted: October 3, 2022
  4. Accepted Manuscript published: October 5, 2022 (version 1)
  5. Version of Record published: October 13, 2022 (version 2)

Copyright

© 2022, Maruyama et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Kazuaki Maruyama
  2. Sachiko Miyagawa-Tomita
  3. Yuka Haneda
  4. Mayuko Kida
  5. Fumio Matsuzaki
  6. Kyoko Imanaka-Yoshida
  7. Hiroki Kurihara
(2022)
The cardiopharyngeal mesoderm contributes to lymphatic vessel development in mouse
eLife 11:e81515.
https://doi.org/10.7554/eLife.81515

Share this article

https://doi.org/10.7554/eLife.81515

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