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Extracellular matrix stiffness cues junctional remodeling for 3D tissue elongation

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  • Dong-Yuan Chen

    (University of California, Berkeley)

  • Justin Crest

    (University of California, Berkeley)

  • Sebastian J. Streichan

    (University of California, Santa Barbara Santa)

  • David Bilder

    (University of California, Berkeley)

Abstract

Organs are sculpted by extracellular as well as cell-intrinsic forces, but how collective cell dynamics are orchestrated in response to environmental cues is poorly understood. Here we apply advanced image analysis to reveal extracellular matrix-responsive cell behaviors that drive elongation of the Drosophila follicle, a model system in which basement membrane stiffness instructs three-dimensional tissue morphogenesis. Through in toto morphometric analyses of wild type and round egg mutants, we find that neither changes in average cell shape nor oriented cell division are required for appropriate organ shape. Instead, a major element is the reorientation of elongated cells at the follicle anterior. Polarized reorientation is regulated by mechanical cues from the basement membrane, which are transduced by the Src tyrosine kinase to alter junctional E-cadherin trafficking. This mechanosensitive cellular behavior represents a conserved mechanism that can elongate edgeless tubular epithelia in a process distinct from those that elongate bounded, planar epithelia.

Suggested Citation

  • Dong-Yuan Chen & Justin Crest & Sebastian J. Streichan & David Bilder, 2019. "Extracellular matrix stiffness cues junctional remodeling for 3D tissue elongation," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-10874-x
    DOI: 10.1038/s41467-019-10874-x
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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. Dong-Yuan Chen & Nikolas H. Claussen & Shiny Titus & Wenqi Hu & Bailey A. T. Weatherbee & Rachel S. Mandelbaum & Richard T. Scott Jr & Emre Seli & Sebastian J. Streichan & Magdalena Zernicka-Goetz, 2025. "Basement membrane perforations guide anterior–posterior axis formation," Nature Communications, Nature, vol. 16(1), pages 1-19, December.
    3. Julia Eckert & Toby G. R. Andrews & Joseph Pollard & Yuan Shen & Patricia Essebier & Benoit Ladoux & Anne K. Lagendijk & Rashmi Priya & Alpha S. Yap & Richard G. Morris, 2025. "Capturing nematic order on tissue surfaces of arbitrary geometry," Nature Communications, Nature, vol. 16(1), pages 1-13, December.
    4. Haruko Watanabe-Takano & Katsuhiro Kato & Eri Oguri-Nakamura & Tomohiro Ishii & Koji Kobayashi & Takahisa Murata & Koichiro Tsujikawa & Takaki Miyata & Yoshiaki Kubota & Yasuyuki Hanada & Koichi Nishi, 2024. "Endothelial cells regulate alveolar morphogenesis by constructing basement membranes acting as a scaffold for myofibroblasts," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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