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Serotonin signaling regulates actomyosin contractility during morphogenesis in evolutionarily divergent lineages

Author

Listed:
  • Sanjay Karki

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Mehdi Saadaoui

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Valentin Dunsing

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Stephen Kerridge

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Elise Silva

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Jean-Marc Philippe

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Cédric Maurange

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems)

  • Thomas Lecuit

    (Aix-Marseille Université & CNRS, IBDM—UMR7288 & Turing Centre for Living Systems
    Collège de France)

Abstract

Serotonin is a neurotransmitter that signals through 5-HT receptors to control key functions in the nervous system. Serotonin receptors are also ubiquitously expressed in various organs and have been detected in embryos of different organisms. Potential morphogenetic functions of serotonin signaling have been proposed based on pharmacological studies but a mechanistic understanding is still lacking. Here, we uncover a role of serotonin signaling in axis extension of Drosophila embryos by regulating Myosin II (MyoII) activation, cell contractility and cell intercalation. We find that serotonin and serotonin receptors 5HT2A and 5HT2B form a signaling module that quantitatively regulates the amplitude of planar polarized MyoII contractility specified by Toll receptors and the GPCR Cirl. Remarkably, serotonin signaling also regulates actomyosin contractility at cell junctions, cellular flows and epiblast morphogenesis during chicken gastrulation. This phylogenetically conserved mechanical function of serotonin signaling in regulating actomyosin contractility and tissue flow reveals an ancestral role in morphogenesis of multicellular organisms.

Suggested Citation

  • Sanjay Karki & Mehdi Saadaoui & Valentin Dunsing & Stephen Kerridge & Elise Silva & Jean-Marc Philippe & Cédric Maurange & Thomas Lecuit, 2023. "Serotonin signaling regulates actomyosin contractility during morphogenesis in evolutionarily divergent lineages," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41178-w
    DOI: 10.1038/s41467-023-41178-w
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    References listed on IDEAS

    as
    1. Akankshi Munjal & Jean-Marc Philippe & Edwin Munro & Thomas Lecuit, 2015. "A self-organized biomechanical network drives shape changes during tissue morphogenesis," Nature, Nature, vol. 524(7565), pages 351-355, August.
    2. Claire Bertet & Lawrence Sulak & Thomas Lecuit, 2004. "Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation," Nature, Nature, vol. 429(6992), pages 667-671, June.
    3. Girish R. Kale & Xingbo Yang & Jean-Marc Philippe & Madhav Mani & Pierre-François Lenne & Thomas Lecuit, 2018. "Distinct contributions of tensile and shear stress on E-cadherin levels during morphogenesis," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    4. Matteo Rauzi & Pierre-François Lenne & Thomas Lecuit, 2010. "Planar polarized actomyosin contractile flows control epithelial junction remodelling," Nature, Nature, vol. 468(7327), pages 1110-1114, December.
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