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Emergence of periodic circumferential actin cables from the anisotropic fusion of actin nanoclusters during tubulogenesis

Author

Listed:
  • Sayaka Sekine

    (RIKEN Center for Biosystems Dynamics Research
    Tohoku University)

  • Mitsusuke Tarama

    (RIKEN Center for Biosystems Dynamics Research
    Kyushu University)

  • Housei Wada

    (RIKEN Center for Biosystems Dynamics Research)

  • Mustafa M. Sami

    (RIKEN Center for Biosystems Dynamics Research
    Okinawa Institute of Science and Technology Graduate University)

  • Tatsuo Shibata

    (RIKEN Center for Biosystems Dynamics Research)

  • Shigeo Hayashi

    (RIKEN Center for Biosystems Dynamics Research
    Kobe University Graduate School of Science)

Abstract

The periodic circumferential cytoskeleton supports various tubular tissues. Radial expansion of the tube lumen causes anisotropic tensile stress, which can be exploited as a geometric cue. However, the molecular machinery linking anisotropy to robust circumferential patterning is poorly understood. Here, we aim to reveal the emergent process of circumferential actin cable formation in a Drosophila tracheal tube. During luminal expansion, sporadic actin nanoclusters emerge and exhibit circumferentially biased motion and fusion. RNAi screening reveals the formin family protein, DAAM, as an essential component responding to tissue anisotropy, and non-muscle myosin II as a component required for nanocluster fusion. An agent-based model simulation suggests that crosslinkers play a crucial role in nanocluster formation and cluster-to-cable transition occurs in response to mechanical anisotropy. Altogether, we propose that an actin nanocluster is an organizational unit that responds to stress in the cortical membrane and builds a higher-order cable structure.

Suggested Citation

  • Sayaka Sekine & Mitsusuke Tarama & Housei Wada & Mustafa M. Sami & Tatsuo Shibata & Shigeo Hayashi, 2024. "Emergence of periodic circumferential actin cables from the anisotropic fusion of actin nanoclusters during tubulogenesis," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44684-z
    DOI: 10.1038/s41467-023-44684-z
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    References listed on IDEAS

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    1. Daichi Kamiyama & Sayaka Sekine & Benjamin Barsi-Rhyne & Jeffrey Hu & Baohui Chen & Luke A. Gilbert & Hiroaki Ishikawa & Manuel D. Leonetti & Wallace F. Marshall & Jonathan S. Weissman & Bo Huang, 2016. "Versatile protein tagging in cells with split fluorescent protein," Nature Communications, Nature, vol. 7(1), pages 1-9, April.
    2. Victoria Tianjing Yan & Arjun Narayanan & Tina Wiegand & Frank Jülicher & Stephan W. Grill, 2022. "A condensate dynamic instability orchestrates actomyosin cortex activation," Nature, Nature, vol. 609(7927), pages 597-604, September.
    3. Dennis Zimmermann & Kaitlin E. Homa & Glen M. Hocky & Luther W. Pollard & Enrique M. De La Cruz & Gregory A. Voth & Kathleen M. Trybus & David R. Kovar, 2017. "Mechanoregulated inhibition of formin facilitates contractile actomyosin ring assembly," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
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