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First published online 30 April 2008
doi: 10.1242/dev.020099

Development 135, 2083-2091 (2008)
Published by The Company of Biologists 2008
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Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth

David G. Simmons1,*, David R. C. Natale1,*, Valerie Begay2, Martha Hughes1, Achim Leutz2 and James C. Cross1,{dagger}

1 Department of Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, The University of Calgary, 3330 Hospital Drive NW, Calgary, AB, T2N 4N1, Canada.
2 Max Delbrueck Center for Molecular Medicine, Robert-Roessle-Str. 10, 13092 Berlin, Germany.

{dagger} Author for correspondence (e-mail: jcross{at}ucalgary.ca)

Accepted 31 March 2008

The labyrinth of the rodent placenta contains villi that are the site of nutrient exchange between mother and fetus. They are covered by three trophoblast cell types that separate the maternal blood sinusoids from fetal capillaries - a single mononuclear cell that is a subtype of trophoblast giant cell (sinusoidal or S-TGC) with endocrine function and two multinucleated syncytiotrophoblast layers, each resulting from cell-cell fusion, that function in nutrient transport. The developmental origins of these cell types have not previously been elucidated. We report here the discovery of cell-layer-restricted genes in the mid-gestation labyrinth (E12.5-14.5) including Ctsq in S-TGCs (also Hand1-positive), Syna in syncytiotrophoblast layer I (SynT-I), and Gcm1, Cebpa and Synb in syncytiotrophoblast layer II (SynT-II). These genes were also expressed in distinct layers in the chorion as early as E8.5, prior to villous formation. Specifically, Hand1 was expressed in apical cells lining maternal blood spaces (Ctsq is not expressed until E12.5), Syna in a layer immediately below, and Gcm1, Cebpa and Synb in basal cells in contact with the allantois. Cebpa and Synb were co-expressed with Gcm1 and were reduced in Gcm1 mutants. By contrast, Hand1 and Syna expression was unaltered in Gcm1 mutants, suggesting that Gcm1-positive cells are not required for the induction of the other chorion layers. These data indicate that the three differentiated trophoblast cell types in the labyrinth arise from distinct and autonomous precursors in the chorion that are patterned before morphogenesis begins.

Key words: Chorion, Gcm1, Labyrinth, Placenta, Syncytin, Syncytiotrophoblast, Trophoblast, Mouse


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