IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41178-w.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41178-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41178-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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. 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.
    3. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Shun Li & Zong-Yuan Liu & Hao Li & Sijia Zhou & Jiaying Liu & Ningwei Sun & Kai-Fu Yang & Vanessa Dougados & Thomas Mangeat & Karine Belguise & Xi-Qiao Feng & Yiyao Liu & Xiaobo Wang, 2024. "Basal actomyosin pulses expand epithelium coordinating cell flattening and tissue elongation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Hiroyuki Uechi & Kazuki Fukushima & Ryota Shirasawa & Sayaka Sekine & Erina Kuranaga, 2022. "Inhibition of negative feedback for persistent epithelial cell–cell junction contraction by p21-activated kinase 3," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Hannah J. Gustafson & Nikolas Claussen & Stefano Renzis & Sebastian J. Streichan, 2022. "Patterned mechanical feedback establishes a global myosin gradient," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. João Firmino & Jean-Yves Tinevez & Elisabeth Knust, 2013. "Crumbs Affects Protein Dynamics In Anterior Regions Of The Developing Drosophila Embryo," PLOS ONE, Public Library of Science, vol. 8(3), pages 1-10, March.
    5. Özge Özgüç & Ludmilla de Plater & Varun Kapoor & Anna Francesca Tortorelli & Andrew G Clark & Jean-Léon Maître, 2022. "Cortical softening elicits zygotic contractility during mouse preimplantation development," PLOS Biology, Public Library of Science, vol. 20(3), pages 1-23, March.
    6. Alexis Villars & Alexis Matamoro-Vidal & Florence Levillayer & Romain Levayer, 2022. "Microtubule disassembly by caspases is an important rate-limiting step of cell extrusion," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    7. Daniel Sánchez-Gutiérrez & Aurora Sáez & Alberto Pascual & Luis M Escudero, 2013. "Topological Progression in Proliferating Epithelia Is Driven by a Unique Variation in Polygon Distribution," PLOS ONE, Public Library of Science, vol. 8(11), pages 1-8, November.
    8. Sijia Zhou & Peng Li & Jiaying Liu & Juan Liao & Hao Li & Lin Chen & Zhihua Li & Qiongyu Guo & Karine Belguise & Bin Yi & Xiaobo Wang, 2022. "Two Rac1 pools integrate the direction and coordination of collective cell migration," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    9. K. Sri-Ranjan & J. L. Sanchez-Alonso & P. Swiatlowska & S. Rothery & P. Novak & S. Gerlach & D. Koeninger & B. Hoffmann & R. Merkel & M. M. Stevens & S. X. Sun & J. Gorelik & Vania M. M. Braga, 2022. "Intrinsic cell rheology drives junction maturation," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    10. R. Allena & J. Muñoz & D. Aubry, 2013. "Diffusion-reaction model for embryo development," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 16(3), pages 235-248.
    11. Tomer Stern & Stanislav Y Shvartsman & Eric F Wieschaus, 2020. "Template-based mapping of dynamic motifs in tissue morphogenesis," PLOS Computational Biology, Public Library of Science, vol. 16(8), pages 1-20, August.
    12. Guilherme Ventura & Aboutaleb Amiri & Raghavan Thiagarajan & Mari Tolonen & Amin Doostmohammadi & Jakub Sedzinski, 2022. "Multiciliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Eoin McEvoy & Tal Sneh & Emad Moeendarbary & Yousef Javanmardi & Nadia Efimova & Changsong Yang & Gloria E. Marino-Bravante & Xingyu Chen & Jorge Escribano & Fabian Spill & José Manuel Garcia-Aznar & , 2022. "Feedback between mechanosensitive signaling and active forces governs endothelial junction integrity," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    14. Julia Eckert & Benoît Ladoux & René-Marc Mège & Luca Giomi & Thomas Schmidt, 2023. "Hexanematic crossover in epithelial monolayers depends on cell adhesion and cell density," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    15. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41178-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.