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Prepublished online as a Blood First Edition Paper on October 24, 2002; DOI 10.1182/blood-2002-08-2531.
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Blood, 1 March 2003, Vol. 101, No. 5, pp. 1669-1675
PLENARY PAPER
Circulation is established in a stepwise pattern in the mammalian
embryo
Kathleen E. McGrath,
Anne D. Koniski,
Jeffrey Malik, and
James Palis
From the Center for Human Genetics and Molecular
Pediatric Diseases, Department of Pediatrics, University of Rochester,
NY.
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 revealed 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), most red cells remained in the yolk sac.
Although the number of red cells expanded rapidly in the embryo proper,
a steady state of approximately 40% red cells was not reached until 26 to 30 sp (E10). Additionally, erythroblasts were unevenly distributed
within the embryo's vasculature before 35 sp. These data suggest that
fully functional circulation is established after E10. This timing
correlated with vascular remodeling, suggesting that vessel
arborization, smooth muscle recruitment, or both are required. We also
examined the distribution of committed hematopoietic progenitors during
early embryogenesis. Before 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 with the embryo proper from E9.5 to E10.5. These results
indicated that the yolk sac vascular network remains a site of
progenitor production and 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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