Shear stress-induced restoration of pulmonary microvascular endothelial barrier function following ischaemia reperfusion injury requires VEGFR2 signalling

Am J Physiol Lung Cell Mol Physiol. 2024 Dec 19. doi: 10.1152/ajplung.00200.2024. Online ahead of print.

Abstract

Normal shear stress produced by blood flow is sensed by the vascular endothelium and required for maintenance of the homeostatic functions of the endothelium in systemic conduit and resistance vessels. Many critical illnesses are characterised by periods of abnormally reduced or absent shear stress in the lung (e.g. haemorrhagic shock, embolism, ischaemia reperfusion injury and lung transplantation) and are complicated by pulmonary oedema following reperfusion due to microvascular leak. The role of shear stress in regulating the pulmonary microvascular endothelial barrier in the intact vascular bed has not been previously examined. We tested the hypothesis that, in lungs injured by a period of ischaemia and reperfusion (IRI), reduced shear stress contributes to increased pulmonary microvascular endothelial barrier permeability and oedema formation. Furthermore, we examined the role of VEGFR2 as a mechanosensor mediating the endothelial response to this altered shear stress. Following IRI, we perfused isolated ventilated mouse lungs with a low viscosity solution (LVS) or a higher, physiological viscosity solution (PVS) at constant flow to produce differing endothelial shear stresses in of the intact microcirculation. Lungs perfused with LVS developed pulmonary oedema due to increased endothelial permeability whereas those perfused with PVS were protected from oedema formation by reduced endothelial permeability. This effect of PVS required normal VEGFR2 mechanoreceptor function. These data show for the first time that shear stress has an important role in restoring endothelial barrier function in the intact pulmonary microcirculation following injury and have important implications for the treatment of pulmonary oedema in critically ill patients.

Keywords: endothelial permeability; microvascular circulation; non-cardiogenic pulmonary edema; pulmonary circulation; shear stress.