Abstract
The renal vasculature is required for blood filtration, blood pressure regulation, and pH maintenance, as well as other specialised kidney functions. Yet, despite its importance, many aspects of its development are poorly understood. To provide a detailed spatiotemporal analysis of kidney vascularisation, we collected images of embryonic mouse kidneys at various developmental time-points. Here we describe the first stages of kidney vascularisation and demonstrate that polygonal networks of vessels (endothelial plexuses) form in cycles at the periphery of the kidney. We show that kidney vascularisation initiates at E11, when vessels connected to the embryonic circulation form a ring around the ureteric bud. From E13.5, endothelial plexuses organise around populations of cap mesenchymal and ureteric bud cells in a cyclical, predictable manner. Specifically, as the ureteric bud bifurcates, endothelia form across the bifurcation site as the cap mesenchyme splits. The plexuses are vascular, carry erythrocytes, are enclosed within a basement membrane, and can always be traced back to the renal artery. Our results are a major step towards understanding how the global architecture of the renal vasculature is achieved.
Highlights
Adult mouse kidneys receive 9–22% of cardiac output[1,2,3]
Previous studies have investigated the initial phases of kidney vascularisation[21, 25,26,27,28], the precise spatiotemporal origin of the first renal blood vessels remains unknown
By taking confocal images of whole-mount kidneys at various developmental time points with anti-CD31 and anti-laminin, we have mapped the first steps of kidney vascularisation in the CD-1 mouse embryo
Summary
Adult mouse kidneys receive 9–22% of cardiac output[1,2,3]. Most of this blood travels into the glomerular capillaries in the renal cortex[4, 5] where small molecules are filtered from the plasma. A major concept proposed to explain kidney vascularisation purports that the kidney is vascularised via a combination of vasculogenic and angiogenic processes[14,15,16,17,18] According to this theory, blood vessels arise in situ via vasculogenesis around the periphery of the kidney from endogenous endothelial progenitors, whereas the endothelia of the major vessels and the medulla form via angiogenesis, by branching from extrinsic sources. We demonstrate that the early embryonic kidney initially becomes vascularised via systemically connected blood vessels and that endothelia are patterned at the border of the kidney in a cyclical, non-stochastic manner These data provide a new conceptual model to explain how the renal blood vessels develop
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