Raphaël Clément1,2, Benjamin Mauroy1, Annemiek J M Cornelissen3. 1. Laboratoire J.-A. Dieudonné, Université Côte d'Azur and CNRS UMR 7351, Parc Valrose, Nice, France. 2. Aix Marseille Univ, CNRS, IBDM, Marseille, France. 3. Laboratoire Matière et Systèmes Complexes (MSC), University Paris Diderot and CNRS UMR 7057, Paris, France.
Abstract
BACKGROUND: Understanding how molecular and physical cues orchestrate vascular morphogenesis is a challenge for developmental biology. Only little attention has been paid to the impact of mechanical stress caused by tissue growth on early blood distribution. Here we study the peripheral accumulation of blood in the chicken embryonic yolk sac, which precedes sinus vein formation. RESULTS: We report that blood accumulation starts before heart-induced blood circulation. We hypothesized that the driving force for the primitive blood flow is a growth-induced gradient of tissue pressure in the yolk sac mesoderm. Therefore, we studied embryos in which heart development was arrested after 2 days of incubation, and found that yolk sac growth and blood peripheral accumulation still occurred. This suggests that tissue growth is sufficient to initiate the flow and the formation of the sinus vein, whereas heart contractions are not required. We designed a simple mathematical model which makes explicit the growth-induced pressure gradient and the subsequent blood accumulation, and show that growth can indeed account for the observed blood accumulation. CONCLUSIONS: This study shows that tissue growth pressure can drive early blood flow, and suggests that the mechanical environment, beyond hemodynamics, can contribute to vascular morphogenesis. Developmental Dynamics 246:573-584, 2017.
BACKGROUND: Understanding how molecular and physical cues orchestrate vascular morphogenesis is a challenge for developmental biology. Only little attention has been paid to the impact of mechanical stress caused by tissue growth on early blood distribution. Here we study the peripheral accumulation of blood in the chicken embryonic yolk sac, which precedes sinus vein formation. RESULTS: We report that blood accumulation starts before heart-induced blood circulation. We hypothesized that the driving force for the primitive blood flow is a growth-induced gradient of tissue pressure in the yolk sac mesoderm. Therefore, we studied embryos in which heart development was arrested after 2 days of incubation, and found that yolk sac growth and blood peripheral accumulation still occurred. This suggests that tissue growth is sufficient to initiate the flow and the formation of the sinus vein, whereas heart contractions are not required. We designed a simple mathematical model which makes explicit the growth-induced pressure gradient and the subsequent blood accumulation, and show that growth can indeed account for the observed blood accumulation. CONCLUSIONS: This study shows that tissue growth pressure can drive early blood flow, and suggests that the mechanical environment, beyond hemodynamics, can contribute to vascular morphogenesis. Developmental Dynamics 246:573-584, 2017.
Authors: Sophie Richard; Amanda Brun; Antonio Tedesco; Benjamin Gallois; Naoual Taghi; Philippe Dantan; Johanne Seguin; Vincent Fleury Journal: Commun Biol Date: 2018-12-21