IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43996-4.html
   My bibliography  Save this article

Contractile ring mechanosensation and its anillin-dependent tuning during early embryogenesis

Author

Listed:
  • Christina Rou Hsu

    (The University of British Columbia, 2350 Health Sciences Mall
    The University of British Columbia, 2350 Health Sciences Mall)

  • Gaganpreet Sangha

    (The University of British Columbia, 2350 Health Sciences Mall
    The University of British Columbia, 2350 Health Sciences Mall)

  • Wayne Fan

    (The University of British Columbia, 2350 Health Sciences Mall
    The University of British Columbia, 2350 Health Sciences Mall)

  • Joey Zheng

    (The University of British Columbia, 2350 Health Sciences Mall
    The University of British Columbia, 2350 Health Sciences Mall)

  • Kenji Sugioka

    (The University of British Columbia, 2350 Health Sciences Mall
    The University of British Columbia, 2350 Health Sciences Mall)

Abstract

Cytokinesis plays crucial roles in morphogenesis. Previous studies have examined how tissue mechanics influences the position and closure direction of the contractile ring. However, the mechanisms by which the ring senses tissue mechanics remain largely elusive. Here, we show the mechanism of contractile ring mechanosensation and its tuning during asymmetric ring closure of Caenorhabditis elegans embryos. Integrative analysis of ring closure and cell cortex dynamics revealed that mechanical suppression of the ring-directed cortical flow is associated with asymmetric ring closure. Consistently, artificial obstruction of ring-directed cortical flow induces asymmetric ring closure in otherwise symmetrically dividing cells. Anillin is vital for mechanosensation. Our genetic analysis suggests that the positive feedback loop among ring-directed cortical flow, myosin enrichment, and ring constriction constitutes a mechanosensitive pathway driving asymmetric ring closure. These findings and developed tools should advance the 4D mechanobiology of cytokinesis in more complex tissues.

Suggested Citation

  • Christina Rou Hsu & Gaganpreet Sangha & Wayne Fan & Joey Zheng & Kenji Sugioka, 2023. "Contractile ring mechanosensation and its anillin-dependent tuning during early embryogenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43996-4
    DOI: 10.1038/s41467-023-43996-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43996-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43996-4?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. Diana Pinheiro & Edouard Hannezo & Sophie Herszterg & Floris Bosveld & Isabelle Gaugue & Maria Balakireva & Zhimin Wang & Inês Cristo & Stéphane U. Rigaud & Olga Markova & Yohanns Bellaïche, 2017. "Transmission of cytokinesis forces via E-cadherin dilution and actomyosin flows," Nature, Nature, vol. 545(7652), pages 103-107, May.
    2. Anan Chen & Luisa Ulloa Severino & Thomas C. Panagiotou & Trevor F. Moraes & Darren A. Yuen & Brigitte D. Lavoie & Andrew Wilde, 2021. "Inhibition of polar actin assembly by astral microtubules is required for cytokinesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Ravi S. Kamath & Andrew G. Fraser & Yan Dong & Gino Poulin & Richard Durbin & Monica Gotta & Alexander Kanapin & Nathalie Le Bot & Sergio Moreno & Marc Sohrmann & David P. Welchman & Peder Zipperlen &, 2003. "Systematic functional analysis of the Caenorhabditis elegans genome using RNAi," Nature, Nature, vol. 421(6920), pages 231-237, January.
    4. Mirjam Mayer & Martin Depken & Justin S. Bois & Frank Jülicher & Stephan W. Grill, 2010. "Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows," Nature, Nature, vol. 467(7315), pages 617-621, September.
    5. Charles R. Harris & K. Jarrod Millman & Stéfan J. Walt & Ralf Gommers & Pauli Virtanen & David Cournapeau & Eric Wieser & Julian Taylor & Sebastian Berg & Nathaniel J. Smith & Robert Kern & Matti Picu, 2020. "Array programming with NumPy," Nature, Nature, vol. 585(7825), pages 357-362, September.
    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. Furqan Dar & Samuel R. Cohen & Diana M. Mitrea & Aaron H. Phillips & Gergely Nagy & Wellington C. Leite & Christopher B. Stanley & Jeong-Mo Choi & Richard W. Kriwacki & Rohit V. Pappu, 2024. "Biomolecular condensates form spatially inhomogeneous network fluids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. López Pérez, Mario & Mansilla Corona, Ricardo, 2022. "Ordinal synchronization and typical states in high-frequency digital markets," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 598(C).
    3. Jessica M. Vanslambrouck & Sean B. Wilson & Ker Sin Tan & Ella Groenewegen & Rajeev Rudraraju & Jessica Neil & Kynan T. Lawlor & Sophia Mah & Michelle Scurr & Sara E. Howden & Kanta Subbarao & Melissa, 2022. "Enhanced metanephric specification to functional proximal tubule enables toxicity screening and infectious disease modelling in kidney organoids," Nature Communications, Nature, vol. 13(1), pages 1-23, December.
    4. Lauren L. Porter & Allen K. Kim & Swechha Rimal & Loren L. Looger & Ananya Majumdar & Brett D. Mensh & Mary R. Starich & Marie-Paule Strub, 2022. "Many dissimilar NusG protein domains switch between α-helix and β-sheet folds," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Ichiro Kawasaki & Kenta Sugiura & Taeko Sasaki & Noriyuki Matsuda & Miyuki Sato & Ken Sato, 2024. "MARC-3, a membrane-associated ubiquitin ligase, is required for fast polyspermy block in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    6. Matthew Rosenblatt & Link Tejavibulya & Rongtao Jiang & Stephanie Noble & Dustin Scheinost, 2024. "Data leakage inflates prediction performance in connectome-based machine learning models," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    7. Hope Dang & Raul Castro-Portuguez & Luis Espejo & Grant Backer & Samuel Freitas & Erica Spence & Jeremy Meyers & Karissa Shuck & Emily A. Gardea & Leah M. Chang & Jonah Balsa & Niall Thorns & Caroline, 2023. "On the benefits of the tryptophan metabolite 3-hydroxyanthranilic acid in Caenorhabditis elegans and mouse aging," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Sayedali Shetab Boushehri & Katharina Essig & Nikolaos-Kosmas Chlis & Sylvia Herter & Marina Bacac & Fabian J. Theis & Elke Glasmacher & Carsten Marr & Fabian Schmich, 2023. "Explainable machine learning for profiling the immunological synapse and functional characterization of therapeutic antibodies," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Arles Urrutia & Víctor A García-Angulo & Andrés Fuentes & Mauricio Caneo & Marcela Legüe & Sebastián Urquiza & Scarlett E Delgado & Juan Ugalde & Paula Burdisso & Andrea Calixto, 2020. "Bacterially produced metabolites protect C. elegans neurons from degeneration," PLOS Biology, Public Library of Science, vol. 18(3), pages 1-31, March.
    10. Khaled Akkad & David He, 2023. "A dynamic mode decomposition based deep learning technique for prognostics," Journal of Intelligent Manufacturing, Springer, vol. 34(5), pages 2207-2224, June.
    11. Romain Fournier & Zoi Tsangalidou & David Reich & Pier Francesco Palamara, 2023. "Haplotype-based inference of recent effective population size in modern and ancient DNA samples," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    12. Laura Portell & Sergi Morera & Helena Ramalhinho, 2022. "Door-to-Door Transportation Services for Reduced Mobility Population: A Descriptive Analytics of the City of Barcelona," IJERPH, MDPI, vol. 19(8), pages 1-20, April.
    13. Caroline Haimerl & Douglas A. Ruff & Marlene R. Cohen & Cristina Savin & Eero P. Simoncelli, 2023. "Targeted V1 comodulation supports task-adaptive sensory decisions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. Binh An Truong Quang & Ruby Peters & Davide A. D. Cassani & Priyamvada Chugh & Andrew G. Clark & Meghan Agnew & Guillaume Charras & Ewa K. Paluch, 2021. "Extent of myosin penetration within the actin cortex regulates cell surface mechanics," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    15. Matthias Wagener & Andriette Bekker & Mohammad Arashi, 2021. "Mastering the Body and Tail Shape of a Distribution," Mathematics, MDPI, vol. 9(21), pages 1-22, October.
    16. Gallo Cassarino, Tiziano & Barrett, Mark, 2022. "Meeting UK heat demands in zero emission renewable energy systems using storage and interconnectors," Applied Energy, Elsevier, vol. 306(PB).
    17. Maren Schnieder, 2023. "Ebike Sharing vs. Bike Sharing: Demand Prediction Using Deep Neural Networks and Random Forests," Sustainability, MDPI, vol. 15(18), pages 1-15, September.
    18. Klement Stojanovski & Ioana Gheorghe & Peter Lenart & Anne Lanjuin & William B. Mair & Benjamin D. Towbin, 2023. "Maintenance of appropriate size scaling of the C. elegans pharynx by YAP-1," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    19. Gabriele Orlando & Daniele Raimondi & Ramon Duran-Romaña & Yves Moreau & Joost Schymkowitz & Frederic Rousseau, 2022. "PyUUL provides an interface between biological structures and deep learning algorithms," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    20. Hazal Colak Oz & Çiçek Güven & Gonzalo Nápoles, 2023. "School dropout prediction and feature importance exploration in Malawi using household panel data: machine learning approach," Journal of Computational Social Science, Springer, vol. 6(1), pages 245-287, April.

    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_s41467-023-43996-4. 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.