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Prepublished online as a Blood First Edition Paper on October 24, 2002; DOI 10.1182/blood-2002-08-2531.
Submitted August 16, 2002
Accepted October 1, 2002
Circulation is established in a step-wise pattern in the mammalian embryo
Kathleen E McGrath*, Anne D Koniski, Jeffrey Malik, and James Palis
Center for Human Genetics and Molecular Pediatric Disease, University of Rochester, Rochester, NY, USA
* Corresponding author; email: kathleene_mcgrath{at}URMC.rochester.edu.
To better understand the relationship between the embryonic hematopoietic and vascular systems, we investigated the establishment of circulation in mouse embryos by examining the redistribution of yolk sac-derived primitive erythroblasts and definitive hematopoietic progenitors. Our studies reveal that small numbers of erythroblasts first enter the embryo proper at 4 to 8 somite pairs (sp) (embryonic day 8.25 (E8.25)), concomitant with the proposed onset of cardiac function. Hours later (E8.5), the vast majority of red cells still remain in the yolk sac. While the number of red cells expands rapidly in the embryo proper, a steady state of approximately 40% red cells is not reached until 26-30 sp (E10). Additionally, erythroblasts are unevenly distributed within the embryo's vasculature before 35 sp. These data suggest that fully functional circulation is established after E10. This timing correlates with vascular remodeling, suggesting that vessel arborization and/or smooth muscle recruitment is required. We also examined the distribution of committed hematopoietic progenitors during early embryogenesis. Prior to E8.0, all progenitors were found in the yolk sac. When normalized to circulating erythroblasts, there was a significant enrichment (20 to 5-fold) of progenitors in the yolk sac compared to the embryo proper from E9.5 to E10.5. These results indicate that the yolk sac vascular network remains a site of progenitor production and/or preferential adhesion even as the fetal liver becomes a hematopoietic organ. We conclude that a functional vascular system develops gradually and that specialized vascular-hematopoietic environments exist after circulation becomes fully established.
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