Endothelial Piezo1 channel mediates mechano-feedback control of brain blood flow

Xin Rui Lim, Mohammad M. Abd-Alhaseeb, Michael Ippolito, Masayo Koide, Amanda J. Senatore, Curtis Plante, Ashwini Hariharan, Nick Weir, Thomas A. Longden, Kathryn A. Laprade, James M. Stafford, Dorothea Ziemens, Markus Schwaninger, Jan Wenzel, Dmitry D. Postnov and Osama F. Harraz ()
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Xin Rui Lim: University of Vermont
Mohammad M. Abd-Alhaseeb: University of Vermont
Michael Ippolito: University of Vermont
Masayo Koide: University of Vermont
Amanda J. Senatore: University of Vermont
Curtis Plante: University of Vermont
Ashwini Hariharan: University of Maryland
Nick Weir: University of Maryland
Thomas A. Longden: University of Maryland
Kathryn A. Laprade: University of Vermont
James M. Stafford: University of Vermont
Dorothea Ziemens: University of Lübeck
Markus Schwaninger: University of Lübeck
Jan Wenzel: University of Lübeck
Dmitry D. Postnov: Aarhus University
Osama F. Harraz: University of Vermont

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Hyperemia in response to neural activity is essential for brain health. A hyperemic response delivers O2 and nutrients, clears metabolic waste, and concomitantly exposes cerebrovascular endothelial cells to hemodynamic forces. While neurovascular research has primarily centered on the front end of hyperemia—neuronal activity-to-vascular response—the mechanical consequences of hyperemia have gone largely unexplored. Piezo1 is an endothelial mechanosensor that senses hyperemia-associated forces. Using genetic mouse models and pharmacologic approaches to manipulate endothelial Piezo1 function, we evaluated its role in blood flow control and whether it impacts cognition. We provide evidence of a built-in brake system that sculpts hyperemia, and specifically show that Piezo1 activation triggers a mechano-feedback system that promotes blood flow recovery to baseline. Further, genetic Piezo1 modification led to deficits in complementary memory tasks. Collectively, our findings establish a role for endothelial Piezo1 in cerebral blood flow regulation and a role in its behavioral sequelae.

Date: 2024
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DOI: 10.1038/s41467-024-52969-0

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