Abstract
During embryonic development, sequential waves of hematopoiesis give rise to blood-forming cells with diverse lineage potentials and self-renewal properties. This process must accomplish two important yet divergent goals: the rapid generation of differentiated blood cells to meet the needs of the developing embryo and the production of a reservoir of hematopoietic stem cells to provide for life-long hematopoiesis in the adult. Vascular beds in distinct anatomical sites of extraembryonic tissues and the embryo proper provide the necessary conditions to support these divergent objectives, suggesting a critical role for specialized vascular niche cells in regulating disparate blood cell fates during development. In this review, we will examine the current understanding of how organ- and stage-specific vascular niche specialization contributes to the development of the hematopoietic system.
Highlights
The blood and the vascular systems are intimately connected in their evolutionary and developmental origins
We have described how specialization of the vascular niche, in the context of a variety of organs and tissues throughout development, plays a central role by orchestrating the sequential waves of developmental hematopoiesis necessary to carry out these diverse processes
A comprehensive review of the large and growing body of literature in this field is prohibitive, we have focused on studies highlighting several central and recurring concepts, as well as recent studies providing provocative new insights which open up novel questions for future exploration and offer pathways to clinical translation
Summary
The blood and the vascular systems are intimately connected in their evolutionary and developmental origins. The signaling pathways and the transcriptional programs that specify and distinguish endothelial and hematopoietic fates have been the subject of much study and are extensively reviewed elsewhere (Ciau-Uitz et al, 2014; Frame et al, 2017; Perlin et al, 2017a; Dzierzak and Bigas, 2018; Gao et al, 2018; Menegatti et al, 2019; Slukvin and Uenishi, 2019) Even once their fates are distinctly specified, endothelial and hematopoietic cells continue to share close spatial relationships, forming specialized microenvironments in which cross-communication is an essential aspect of hematopoietic maintenance and differentiation throughout the course of development and adulthood. In contrast to adult hematopoiesis, where essentially all circulating blood cells are derived from HSCs residing in the bone marrow niche, the first blood cells during embryonic development are generated without transitioning through an HSC state These initial phases are referred to as HSCindependent waves of hematopoiesis (Palis, 2016a; Dzierzak and Bigas, 2018; Hadland and Yoshimoto, 2018). Niche-derived signals have been shown to support the sequential aspects of the primitive wave of hematopoiesis in the yolk sac, coordinating its rapid onset
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