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Am J Physiol Cell Physiol (February 4, 2004). doi:10.1152/ajpcell.00243.2003
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Submitted on June 11, 2003
Accepted on January 30, 2004

Differential Membrane Potential and Ion Current Responses to Different Types of Shear Stress in Vascular Endothelial Cells

Deborah K Lieu1, Pamela A Pappone2, and Abdul I Barakat1*

1 Mechanical and Aeronautical Engineering, University of California, Davis, Davis, CA, USA
2 Section of Neurobiology, Physiology and Behavior, University of California, Davis, Davis, CA, USA

* To whom correspondence should be addressed. E-mail: abarakat{at}ucdavis.edu.

Vascular endothelial cells (ECs) distinguish among and respond differently to different types of fluid mechanical shear stress. Elucidating the mechanisms governing this differential responsiveness is key to understanding why early atherosclerotic lesions localize preferentially in arterial regions exposed to low and/or oscillatory flow. An early and very rapid endothelial response to flow is the activation of flow-sensitive K+ and Cl- channels that respectively hyperpolarize and depolarize the cell membrane and that regulate several important endothelial responses to flow. We have used whole-cell current- and voltage-clamp techniques to demonstrate that flow-sensitive hyperpolarizing and depolarizing currents respond differently to different types of shear stress in cultured bovine aortic ECs. A steady shear stress of 10 dyne/cm2 activated both currents leading to rapid membrane hyperpolarization that was subsequently reversed to depolarization. In contrast, a steady shear stress of 1 dyne/cm2 only activated the hyperpolarizing current. A purely oscillatory shear stress of 0±10 dyne/cm2 with an oscillation frequency of either 1 or 0.2 Hz activated the hyperpolarizing current but only minimally the depolarizing current, while a 5-Hz oscillation activated neither current. These results demonstrate for the first time that flow-activated ion currents exhibit different sensitivities to shear stress magnitude and oscillation frequency. We propose that flow-sensitive ion channels constitute components of an integrated mechanosensing system that, through the aggregate effect of ion channel activation on cell membrane potential, enables ECs to distinguish among different types of flow.




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