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Abstract
Mammalian embryos have an intimate relationship with their mothers, particularly with
the placental vasculature from which embryos obtain nutrients essential for growth.
It is an interesting vascular bed because maternal vessel number and diameter change
dramatically during gestation and, in rodents and primates, the terminal blood space
becomes lined by placental trophoblast cells rather than endothelial cells. Molecular
genetic studies in mice aimed at identifying potential regulators of these processes
have been hampered by lack of understanding of the anatomy of the vascular spaces
in the placenta and the general nature of maternal-fetal vascular interactions. To
address this problem, we examined the anatomy of the mouse placenta by preparing plastic
vascular casts and serial histological sections of implantation sites from embryonic
day (E) 10.5 to term. We found that each radial artery carrying maternal blood into
the uterus branched into 5-10 dilated spiral arteries located within the metrial triangle,
populated by uterine natural killer (uNK) cells, and the decidua basalis. The endothelial-lined
spiral arteries converged together at the trophoblast giant cell layer and emptied
into a few straight, trophoblast-lined "canals" that carried maternal blood to the
base of the placenta. Maternal blood then percolated back through the intervillous
space of the labyrinth toward the maternal side of the placenta in a direction that
is countercurrent to the direction of the fetal capillary blood flow. Trophoblast
cells were found invading the uterus in two patterns. Large cells that expressed the
trophoblast giant cell-specific gene Plf (encoding Proliferin) invaded during the
early postimplantation period in a pattern tightly associated with spiral arteries.
These peri/endovascular trophoblast were detected only approximately 150-300 microm
upstream of the main giant cell layer. A second type of widespread interstitial invasion
in the decidua basalis by glycogen trophoblast cells was detected after E12.5. These
cells did not express Plf, but rather expressed the spongiotrophoblast-specific gene
Tpbp. Dilation of the spiral arteries was obvious between E10.5 and E14.5 and was
associated with a lack of elastic lamina and smooth muscle cells. These features were
apparent even in the metrial triangle, a site far away from the invading trophoblast
cells. By contrast, the transition from endothelium-lined artery to trophoblast-lined
(hemochorial) blood space was associated with trophoblast giant cells. Moreover, the
shaping of the maternal blood spaces within the labyrinth was dependent on chorioallantoic
morphogenesis and therefore disrupted in Gcm1 mutants. These studies provide important
insights into how the fetoplacental unit interacts with the maternal intrauterine
vascular system during pregnancy in mice.