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Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation

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  • Maureen Cetera

    (The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA
    Committee on Development, Regeneration and Stem Cell Biology, The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA)

  • Guillermina R. Ramirez-San Juan

    (The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA
    Institute for Biophysical Dynamics, The University of Chicago, 929 East 57th Street, Chicago, Illinois 60637, USA)

  • Patrick W. Oakes

    (Institute for Biophysical Dynamics, The University of Chicago, 929 East 57th Street, Chicago, Illinois 60637, USA)

  • Lindsay Lewellyn

    (The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA
    Butler University, 4600 Sunset Boulevard, Indianapolis, Indiana 46208, USA)

  • Michael J. Fairchild

    (Life Sciences Centre, University of British Columbia)

  • Guy Tanentzapf

    (Life Sciences Centre, University of British Columbia)

  • Margaret L. Gardel

    (Institute for Biophysical Dynamics, The University of Chicago, 929 East 57th Street, Chicago, Illinois 60637, USA)

  • Sally Horne-Badovinac

    (The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA
    Committee on Development, Regeneration and Stem Cell Biology, The University of Chicago, 920 East 58th Street, Chicago, Illinois 60637, USA)

Abstract

Tissues use numerous mechanisms to change shape during development. The Drosophila egg chamber is an organ-like structure that elongates to form an elliptical egg. During elongation the follicular epithelial cells undergo a collective migration that causes the egg chamber to rotate within its surrounding basement membrane. Rotation coincides with the formation of a ‘molecular corset’, in which actin bundles in the epithelium and fibrils in the basement membrane are all aligned perpendicular to the elongation axis. Here we show that rotation plays a critical role in building the actin-based component of the corset. Rotation begins shortly after egg chamber formation and requires lamellipodial protrusions at each follicle cell’s leading edge. During early stages, rotation is necessary for tissue-level actin bundle alignment, but it becomes dispensable after the basement membrane is polarized. This work highlights how collective cell migration can be used to build a polarized tissue organization for organ morphogenesis.

Suggested Citation

  • Maureen Cetera & Guillermina R. Ramirez-San Juan & Patrick W. Oakes & Lindsay Lewellyn & Michael J. Fairchild & Guy Tanentzapf & Margaret L. Gardel & Sally Horne-Badovinac, 2014. "Epithelial rotation promotes the global alignment of contractile actin bundles during Drosophila egg chamber elongation," Nature Communications, Nature, vol. 5(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms6511
    DOI: 10.1038/ncomms6511
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    Cited by:

    1. 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.
    2. Tom Brandstätter & David B. Brückner & Yu Long Han & Ricard Alert & Ming Guo & Chase P. Broedersz, 2023. "Curvature induces active velocity waves in rotating spherical tissues," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Chiao-Peng Hsu & Alfredo Sciortino & Yu Alice Trobe & Andreas R. Bausch, 2022. "Activity-induced polar patterns of filaments gliding on a sphere," Nature Communications, Nature, vol. 13(1), pages 1-8, December.

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