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Balancing competing effects of tissue growth and cytoskeletal regulation during Drosophila wing disc development

Author

Listed:
  • Nilay Kumar

    (University of Notre Dame)

  • Jennifer Rangel Ambriz

    (University of California
    University of California)

  • Kevin Tsai

    (University of California
    University of California)

  • Mayesha Sahir Mim

    (University of Notre Dame)

  • Marycruz Flores-Flores

    (University of Notre Dame)

  • Weitao Chen

    (University of California
    University of California)

  • Jeremiah J. Zartman

    (University of Notre Dame
    University of Notre Dame)

  • Mark Alber

    (University of California
    University of California)

Abstract

How a developing organ robustly coordinates the cellular mechanics and growth to reach a final size and shape remains poorly understood. Through iterations between experiments and model simulations that include a mechanistic description of interkinetic nuclear migration, we show that the local curvature, height, and nuclear positioning of cells in the Drosophila wing imaginal disc are defined by the concurrent patterning of actomyosin contractility, cell-ECM adhesion, ECM stiffness, and interfacial membrane tension. We show that increasing cell proliferation via different growth-promoting pathways results in two distinct phenotypes. Triggering proliferation through insulin signaling increases basal curvature, but an increase in growth through Dpp signaling and Myc causes tissue flattening. These distinct phenotypic outcomes arise from differences in how each growth pathway regulates the cellular cytoskeleton, including contractility and cell-ECM adhesion. The coupled regulation of proliferation and cytoskeletal regulators is a general strategy to meet the multiple context-dependent criteria defining tissue morphogenesis.

Suggested Citation

  • Nilay Kumar & Jennifer Rangel Ambriz & Kevin Tsai & Mayesha Sahir Mim & Marycruz Flores-Flores & Weitao Chen & Jeremiah J. Zartman & Mark Alber, 2024. "Balancing competing effects of tissue growth and cytoskeletal regulation during Drosophila wing disc development," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46698-7
    DOI: 10.1038/s41467-024-46698-7
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    References listed on IDEAS

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    1. Mototsugu Eiraku & Nozomu Takata & Hiroki Ishibashi & Masako Kawada & Eriko Sakakura & Satoru Okuda & Kiyotoshi Sekiguchi & Taiji Adachi & Yoshiki Sasai, 2011. "Self-organizing optic-cup morphogenesis in three-dimensional culture," Nature, Nature, vol. 472(7341), pages 51-56, April.
    2. Silvia Aldaz & Luis M. Escudero & Matthew Freeman, 2013. "Dual role of myosin II during Drosophila imaginal disc metamorphosis," Nature Communications, Nature, vol. 4(1), pages 1-10, June.
    3. Sebastian A Sandersius & Manli Chuai & Cornelis J Weijer & Timothy J Newman, 2011. "Correlating Cell Behavior with Tissue Topology in Embryonic Epithelia," PLOS ONE, Public Library of Science, vol. 6(4), pages 1-11, April.
    4. Stefan Harmansa & Alexander Erlich & Christophe Eloy & Giuseppe Zurlo & Thomas Lecuit, 2023. "Growth anisotropy of the extracellular matrix shapes a developing organ," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Fisun Hamaratoglu & Aitana Morton de Lachapelle & George Pyrowolakis & Sven Bergmann & Markus Affolter, 2011. "Dpp Signaling Activity Requires Pentagone to Scale with Tissue Size in the Growing Drosophila Wing Imaginal Disc," PLOS Biology, Public Library of Science, vol. 9(10), pages 1-17, October.
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