The cerebral capillary bed consists of a dense network of vessels out of specialized brain microvascular endothelial cells (BMECs) that deliver essential nutrients to the brain. To form functionally branched vasculature, BMECs have to sense and adapt to site-specific shear stress, relayed by mechanosensory cell surface proteins (CSPs) presented on the BMEC surface. Previous research on the effect of physiological and pathological shear stress on large vessels has studied unidirectional and oscillatory flow as proxies for laminar and disturbed shear stress. However, the effect of shear stress on BMECs forming the luminally exposed part of the blood-brain barrier is less well understood. Inspired by preliminary findings in vivo, we set out to investigate the contradiction of string vessel formation at disturbed flow and the hypothesis that shear stress in the brain capillaries is inconsistent. We present a first discovery-driven surface proteotyping on primary murine BMECs, flow-conditioned in microfluidic devices. We describe the regulation of over 500 CSPs under unidirectional and oscillatory shear stress against a no-flow condition. We discuss the role of Tbhs1, Plvap, and Cd276 in BMEC mechanosensory adaptations, and their potential use as handles in targeted therapy. We complement our findings with proteomic data (of the whole cells) and validate selected de novo candidates with immuno-fluorescent stains. Our results advance existing data with CSP markers that extend the picture of the role of mechanical forces on the endothelium and may help to characterize adaptations to flow in brain capillaries.