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Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ

Author

Listed:
  • Margherita Perillo

    (Cellular Biology and Biochemistry, BioMed Division, Brown University
    Marine Biological Laboratory)

  • S. Zachary Swartz

    (Whitehead Institute for Biomedical Research
    Marine Biological Laboratory)

  • Cosmo Pieplow

    (Cellular Biology and Biochemistry, BioMed Division, Brown University)

  • Gary M. Wessel

    (Cellular Biology and Biochemistry, BioMed Division, Brown University)

Abstract

A fundamental goal in the organogenesis field is to understand how cells organize into tubular shapes. Toward this aim, we have established the hydro-vascular organ in the sea star Patiria miniata as a model for tubulogenesis. In this animal, bilateral tubes grow out from the tip of the developing gut, and precisely extend to specific sites in the larva. This growth involves cell migration coupled with mitosis in distinct zones. Cell proliferation requires FGF signaling, whereas the three-dimensional orientation of the organ depends on Wnt signaling. Specification and maintenance of tube cell fate requires Delta/Notch signaling. Moreover, we identify target genes of the FGF pathway that contribute to tube morphology, revealing molecular mechanisms for tube outgrowth. Finally, we report that FGF activates the Six1/2 transcription factor, which serves as an evolutionarily ancient regulator of branching morphogenesis. This study uncovers distinct mechanisms of tubulogenesis in vivo and we propose that cellular dynamics in the sea star hydro-vascular organ represents a key comparison for understanding the evolution of vertebrate organs.

Suggested Citation

  • Margherita Perillo & S. Zachary Swartz & Cosmo Pieplow & Gary M. Wessel, 2023. "Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37947-2
    DOI: 10.1038/s41467-023-37947-2
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    References listed on IDEAS

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    1. Aleksandr Vasilyev & Yan Liu & Nathan Hellman & Narendra Pathak & Iain A Drummond, 2012. "Mechanical Stretch and PI3K Signaling Link Cell Migration and Proliferation to Coordinate Epithelial Tubule Morphogenesis in the Zebrafish Pronephros," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-11, July.
    2. Gregory A. Cary & Brenna S. McCauley & Olga Zueva & Joseph Pattinato & William Longabaugh & Veronica F. Hinman, 2020. "Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    3. Maik C. Bischoff & Sebastian Lieb & Renate Renkawitz-Pohl & Sven Bogdan, 2021. "Filopodia-based contact stimulation of cell migration drives tissue morphogenesis," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
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