Microscale geometrical modulation of PIEZO1 mediated mechanosensing through cytoskeletal redistribution

Haoqing Jerry Wang, Yao Wang, Seyed Sajad Mirjavadi, Tomas Andersen, Laura Moldovan, Parham Vatankhah, Blake Russell, Jasmine Jin, Zijing Zhou, Qing Li, Charles D. Cox, Qian Peter Su () and Lining Arnold Ju ()
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Haoqing Jerry Wang: The University of Sydney
Yao Wang: The University of Sydney
Seyed Sajad Mirjavadi: The University of Sydney
Tomas Andersen: The University of Sydney
Laura Moldovan: The University of Sydney
Parham Vatankhah: The University of Sydney
Blake Russell: The University of Sydney
Jasmine Jin: The University of Sydney
Zijing Zhou: Victor Chang Cardiac Research Institute
Qing Li: The University of Sydney
Charles D. Cox: Victor Chang Cardiac Research Institute
Qian Peter Su: Camperdown
Lining Arnold Ju: The University of Sydney

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract The microgeometry of the cellular microenvironment profoundly impacts cellular behaviors, yet the link between it and the ubiquitously expressed mechanosensitive ion channel PIEZO1 remains unclear. Herein, we describe a fluorescent micropipette aspiration assay that allows for simultaneous visualization of intracellular calcium dynamics and cytoskeletal architecture in real-time, under varied micropipette geometries. By integrating elastic shell finite element analysis with fluorescent lifetime imaging microscopy and employing PIEZO1-specific transgenic red blood cells and HEK cell lines, we demonstrate a direct correlation between the microscale geometry of aspiration and PIEZO1-mediated calcium signaling. We reveal that increased micropipette tip angles and physical constrictions lead to a significant reorganization of F-actin, accumulation at the aspirated cell neck, and subsequently amplify the tension stress at the dome of the cell to induce more PIEZO1’s activity. Disruption of the F-actin network or inhibition of its mobility leads to a notable decline in PIEZO1 mediated calcium influx, underscoring its critical role in cellular mechanosensing amidst geometrical constraints.

Date: 2024
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DOI: 10.1038/s41467-024-49833-6

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