IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/3001593.html
   My bibliography  Save this article

Cortical softening elicits zygotic contractility during mouse preimplantation development

Author

Listed:
  • Özge Özgüç
  • Ludmilla de Plater
  • Varun Kapoor
  • Anna Francesca Tortorelli
  • Andrew G Clark
  • Jean-Léon Maître

Abstract

Actomyosin contractility is a major engine of preimplantation morphogenesis, which starts at the 8-cell stage during mouse embryonic development. Contractility becomes first visible with the appearance of periodic cortical waves of contraction (PeCoWaCo), which travel around blastomeres in an oscillatory fashion. How contractility of the mouse embryo becomes active remains unknown. We have taken advantage of PeCoWaCo to study the awakening of contractility during preimplantation development. We find that PeCoWaCo become detectable in most embryos only after the second cleavage and gradually increase their oscillation frequency with each successive cleavage. To test the influence of cell size reduction during cleavage divisions, we use cell fusion and fragmentation to manipulate cell size across a 20- to 60-μm range. We find that the stepwise reduction in cell size caused by cleavage divisions does not explain the presence of PeCoWaCo or their accelerating rhythm. Instead, we discover that blastomeres gradually decrease their surface tensions until the 8-cell stage and that artificially softening cells enhances PeCoWaCo prematurely. We further identify the programmed down-regulation of the formin Fmnl3 as a required event to soften the cortex and expose PeCoWaCo. Therefore, during cleavage stages, cortical softening, mediated by Fmnl3 down-regulation, awakens zygotic contractility before preimplantation morphogenesis.During preimplantation morphogenesis, the mouse embryo relies on forces generated by the actomyosin cytoskeleton. This study uncovers how periodic actomyosin contractions increase in frequency during cleavage stages as blastomeres soften with each cleavage division.

Suggested Citation

  • 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.
    • Handle: RePEc:plo:pbio00:3001593
    DOI: 10.1371/journal.pbio.3001593
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001593
    Download Restriction: no
    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001593&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pbio.3001593?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. A. Chaigne & C. Campillo & N. S. Gov & R. Voituriez & C. Sykes & M. H. Verlhac & M. E. Terret, 2015. "A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte," Nature Communications, Nature, vol. 6(1), pages 1-10, May.
    2. Hui Yi Grace Lim & Yanina D. Alvarez & Maxime Gasnier & Yiming Wang & Piotr Tetlak & Stephanie Bissiere & Hongmei Wang & Maté Biro & Nicolas Plachta, 2020. "Keratins are asymmetrically inherited fate determinants in the mammalian embryo," Nature, Nature, vol. 585(7825), pages 404-409, September.
    3. Johanna Bischof & Christoph A. Brand & Kálmán Somogyi & Imre Májer & Sarah Thome & Masashi Mori & Ulrich S. Schwarz & Péter Lénárt, 2017. "A cdk1 gradient guides surface contraction waves in oocytes," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    4. Adam C. Martin & Matthias Kaschube & Eric F. Wieschaus, 2009. "Pulsed contractions of an actin–myosin network drive apical constriction," Nature, Nature, vol. 457(7228), pages 495-499, January.
    5. Anaïs Bailles & Claudio Collinet & Jean-Marc Philippe & Pierre-François Lenne & Edwin Munro & Thomas Lecuit, 2019. "Genetic induction and mechanochemical propagation of a morphogenetic wave," Nature, Nature, vol. 572(7770), pages 467-473, August.
    6. Jean-Léon Maître & Hervé Turlier & Rukshala Illukkumbura & Björn Eismann & Ritsuya Niwayama & François Nédélec & Takashi Hiiragi, 2016. "Asymmetric division of contractile domains couples cell positioning and fate specification," Nature, Nature, vol. 536(7616), pages 344-348, August.
    7. Zhanghan Wu & Maohan Su & Cheesan Tong & Min Wu & Jian Liu, 2018. "Membrane shape-mediated wave propagation of cortical protein dynamics," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    8. 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.
    9. Kei Yamamoto & Haruko Miura & Motohiko Ishida & Yusuke Mii & Noriyuki Kinoshita & Shinji Takada & Naoto Ueno & Satoshi Sawai & Yohei Kondo & Kazuhiro Aoki, 2021. "Optogenetic relaxation of actomyosin contractility uncovers mechanistic roles of cortical tension during cytokinesis," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    10. 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.
    11. Jan Budczies & Frederick Klauschen & Bruno V Sinn & Balázs Győrffy & Wolfgang D Schmitt & Silvia Darb-Esfahani & Carsten Denkert, 2012. "Cutoff Finder: A Comprehensive and Straightforward Web Application Enabling Rapid Biomarker Cutoff Optimization," PLOS ONE, Public Library of Science, vol. 7(12), pages 1-7, 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. Ngoc Minh Nguyen & Emmanuel Farge, 2024. "Mechanical induction in metazoan development and evolution: from earliest multi-cellular organisms to modern animal embryos," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. Robin M. Skory & Adam A. Moverley & Goli Ardestani & Yanina Alvarez & Ana Domingo-Muelas & Oz Pomp & Blake Hernandez & Piotr Tetlak & Stephanie Bissiere & Claudio D. Stern & Denny Sakkas & Nicolas Pla, 2023. "The nuclear lamina couples mechanical forces to cell fate in the preimplantation embryo via actin organization," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. 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.
    8. 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.
    9. Owen Puls & Daniel Ruiz-Reynés & Franco Tavella & Minjun Jin & Yeonghoon Kim & Lendert Gelens & Qiong Yang, 2024. "Spatial heterogeneity accelerates phase-to-trigger wave transitions in frog egg extracts," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. Rayane Dibsy & Erwan Bremaud & Johnson Mak & Cyril Favard & Delphine Muriaux, 2023. "HIV-1 diverts cortical actin for particle assembly and release," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    11. 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.
    12. 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.
    13. 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.
    14. B Rey deCastro, 2019. "Cumulative ROC curves for discriminating three or more ordinal outcomes with cutpoints on a shared continuous measurement scale," PLOS ONE, Public Library of Science, vol. 14(8), pages 1-16, August.
    15. Hyungjin Kim & Chang Min Park & Bhumsuk Keam & Sang Joon Park & Miso Kim & Tae Min Kim & Dong-Wan Kim & Dae Seog Heo & Jin Mo Goo, 2017. "The prognostic value of CT radiomic features for patients with pulmonary adenocarcinoma treated with EGFR tyrosine kinase inhibitors," PLOS ONE, Public Library of Science, vol. 12(11), pages 1-13, November.
    16. 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.
    17. Julien Fierling & Alphy John & Barthélémy Delorme & Alexandre Torzynski & Guy B. Blanchard & Claire M. Lye & Anna Popkova & Grégoire Malandain & Bénédicte Sanson & Jocelyn Étienne & Philippe Marmottan, 2022. "Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    18. Junko Otsuki & Toshiroh Iwasaki & Noritoshi Enatsu & Yuya Katada & Kohyu Furuhashi & Masahide Shiotani, 2020. "The inclusion of blastomeres into the inner cell mass in early-stage human embryos depends on the sequence of cell cleavages during the fourth division," PLOS ONE, Public Library of Science, vol. 15(10), pages 1-7, October.
    19. Ryota Sakamoto & Michael P. Murrell, 2024. "Mechanical power is maximized during contractile ring-like formation in a biomimetic dividing cell model," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    20. Jessica E Forsyth & Ali H Al-Anbaki & Roberto de la Fuente & Nikkinder Modare & Diego Perez-Cortes & Isabel Rivera & Rowena Seaton Kelly & Simon Cotter & Berenika Plusa, 2021. "IVEN: A quantitative tool to describe 3D cell position and neighbourhood reveals architectural changes in FGF4-treated preimplantation embryos," PLOS Biology, Public Library of Science, vol. 19(7), pages 1-25, July.

    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:plo:pbio00:3001593. 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: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    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.