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Tissue fluidity mediated by adherens junction dynamics promotes planar cell polarity-driven ommatidial rotation

Author

Listed:
  • Nabila Founounou

    (Icahn School of Medicine at Mount Sinai)

  • Reza Farhadifar

    (Flatiron Institute, Simons Foundation
    Harvard University)

  • Giovanna M. Collu

    (Icahn School of Medicine at Mount Sinai)

  • Ursula Weber

    (Icahn School of Medicine at Mount Sinai)

  • Michael J. Shelley

    (Flatiron Institute, Simons Foundation
    New York University)

  • Marek Mlodzik

    (Icahn School of Medicine at Mount Sinai)

Abstract

The phenomenon of tissue fluidity—cells’ ability to rearrange relative to each other in confluent tissues—has been linked to several morphogenetic processes and diseases, yet few molecular regulators of tissue fluidity are known. Ommatidial rotation (OR), directed by planar cell polarity signaling, occurs during Drosophila eye morphogenesis and shares many features with polarized cellular migration in vertebrates. We utilize in vivo live imaging analysis tools to quantify dynamic cellular morphologies during OR, revealing that OR is driven autonomously by ommatidial cell clusters rotating in successive pulses within a permissive substrate. Through analysis of a rotation-specific nemo mutant, we demonstrate that precise regulation of junctional E-cadherin levels is critical for modulating the mechanical properties of the tissue to allow rotation to progress. Our study defines Nemo as a molecular tool to induce a transition from solid-like tissues to more viscoelastic tissues broadening our molecular understanding of tissue fluidity.

Suggested Citation

  • Nabila Founounou & Reza Farhadifar & Giovanna M. Collu & Ursula Weber & Michael J. Shelley & Marek Mlodzik, 2021. "Tissue fluidity mediated by adherens junction dynamics promotes planar cell polarity-driven ommatidial rotation," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27253-0
    DOI: 10.1038/s41467-021-27253-0
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    References listed on IDEAS

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    1. 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.
    2. Alessandro Mongera & Payam Rowghanian & Hannah J. Gustafson & Elijah Shelton & David A. Kealhofer & Emmet K. Carn & Friedhelm Serwane & Adam A. Lucio & James Giammona & Otger Campàs, 2018. "A fluid-to-solid jamming transition underlies vertebrate body axis elongation," Nature, Nature, vol. 561(7723), pages 401-405, September.
    3. Jennifer A. Mitchel & Amit Das & Michael J. O’Sullivan & Ian T. Stancil & Stephen J. DeCamp & Stephan Koehler & Oscar H. Ocaña & James P. Butler & Jeffrey J. Fredberg & M. Angela Nieto & Dapeng Bi & J, 2020. "In primary airway epithelial cells, the unjamming transition is distinct from the epithelial-to-mesenchymal transition," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. Cayla E. Jewett & Timothy E. Vanderleest & Hui Miao & Yi Xie & Roopa Madhu & Dinah Loerke & J. Todd Blankenship, 2017. "Planar polarized Rab35 functions as an oscillatory ratchet during cell intercalation in the Drosophila epithelium," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    5. Innokenty Woichansky & Carlo Antonio Beretta & Nicola Berns & Veit Riechmann, 2016. "Three mechanisms control E-cadherin localization to the zonula adherens," Nature Communications, Nature, vol. 7(1), pages 1-11, April.
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