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Abstract Blood development has been highly conserved during evolution. Hematopoietic cells in amphibian and fish embryos, as in mammalian embryos, emerge and progressively differentiate in several locations. Hematopoiesis, including of the immune system, is similar in the amphibian, Xenopus, to mammals and the embryos are ideal for tissue transplantation and lineage labelling experiments, which have enabled the elucidation of the distinct origins of embryonic and adult hematopoietic cells, as well as their migration pathways and organ colonisation behaviours. The zebrafish hematopoietic system is less well understood, but these embryos have recently emerged as a powerful system for both genetic analysis and imaging. In this review, we summarise our current knowledge of the cellular and genetic basis of ontogeny of the hematopoietic system in Xenopus and zebrafish embryos.
Fig. 1. Ontogeny and hematopoietic potential of the anterior portion of the ventralblood island (aVBI). (A) The aVBI and its precursor, the embryonic hemangioblasts, derive from dorsal blastomeres of the 32-cell stage embryo. (B) Embryonic hemangioblast (red cells) are specified during gastrulation when their mesodermal precursors (blue cells) encounter BMP signalling during their migration from dorsal to ventral. (C) Erythroid (Runx1) and myeloid (SpiB) genes are co-expressed (red arrows) at the hemangioblast stage. (D) Numerous myeloid cells differentiate from the embryonic hemangioblast at tail bud stages. These myeloid cells are highly migratory and initiate migration at stage 22 (24 hpf arrowheads).
Fig. 2. Ontogeny and hematopoietic potential of the posterior portion of the ventralblood island (pVBI). (A) Ventralblastomere D4 gives rise to the pVBI. (B) At tail bud stages (stage 30, 35hpf) all differentiated myeloid cells (MPO, Elas1, L-plastin) derive from the dorsal marginal zone (DMZ) indicating their anteriorhemangioblast origin. At this stage, the ventral marginal zone (VMZ) contains myeloid precursors (SpiB) but no migrating mature myeloid cells. (C) At early larval stages (stage 40, 66hpf), myeloid cells are no longer produced by the DMZ while a second wave differentiating from the VMZ becomes abundant.
Fig. 4. Ontogeny of the dorsal aorta (DA) and hematopoietic stem cells (HSCs) in Xenopus. (A) Runx1 expression and HSC emergence is restricted to the DA encompassing the trunk. (B) The DA is anatomically subdivided into paired DA, trunk DA and tailartery. HSCs only emerge in the trunk DA. (C) Diagram summarizing the blastomere origins of the anatomical subdivision of the DA.
Fig. 5. Origins of hemangioblast and blood/endothelial cells in zebrafish embryos. (A,B) Expression patterns of
flk1 (blue) and gata1 (red) in a flat mounted 8-somite stage embryo, with myoD marking the somites. (A) Schematic diagram; (B) in situ hybridization. (C-E) Expression pattern of an established hemangioblast marker, scl, in zebrafish marks both the anteriorhemangioblast population (ALM) which will give rise to myeloid and endothelial cells, and the posteriorhemangioblast population (PLM) which will give rise to erythroid and endothelial cells.
Fig. 5. Origins of hemangioblast and blood/endothelial cells in zebrafish embryos. F,G) Lineage tracing shows that PLM cells labeled at 5s (F) by photo conversion of fluorescent protein (Hatta et al., 2006) in the confocal microscope, are found migrating to the midline at 18s (not shown) and differentiated into red blood cells and endothelial cells at 26 hpf (G), with arrow indicating endothelial cells. Flat mount view (A-D); lateral view (E-G).
Fig. 6. HSCs in association with the ventral wall of the dorsal aorta (DA). (A) scl:gfp transgenic embryos show GFP expression in the putative HSCs in the DA at 48 hpf. (B) In situ hybridization at 26hpf showing runx1 expressing cells (HSCs) associated with the ventral wall of the DA. (C) gata2 is expressed in primitive blood, vessels and spinal chord neurons at 26 hpf. Lateral views, anterior to the left.
