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

Sayaka Sekine (), Mitsusuke Tarama (), Housei Wada, Mustafa M. Sami, Tatsuo Shibata and Shigeo Hayashi
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Sayaka Sekine: RIKEN Center for Biosystems Dynamics Research
Mitsusuke Tarama: RIKEN Center for Biosystems Dynamics Research
Housei Wada: RIKEN Center for Biosystems Dynamics Research
Mustafa M. Sami: RIKEN Center for Biosystems Dynamics Research
Tatsuo Shibata: RIKEN Center for Biosystems Dynamics Research
Shigeo Hayashi: RIKEN Center for Biosystems Dynamics Research

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-023-44684-z

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