Embryonic signals direct the formation of tight junctional permeability barrier in the decidualizing stroma during embryo implantation

The protection of the embryo from the maternal adverse environment during early pregnancy is considered to be achieved by the establishment of a transitory permeability barrier created by decidual cells immediately surrounding the implanting embryo. Normally, the polarized epithelium acts as a barrier by regulating paracellular passage of substances through tight junctions. The expression of tight junction proteins in the uterine luminal epithelium prior to implantation is consistent with this idea. However, limited information is available regarding the nature and regulation of the permeability barrier that is created by decidualizing stromal cells during implantation. We show here that the tight junction proteins, occludin, claudin-1, zonula occludens-1 and zonula occludens-2, are all expressed and physically associated in decidualizing stromal cells of the primary decidual zone forming a barrier surrounding the embryo with the loss of adjacent luminal epithelium. The blastocyst trophectoderm appears to be the stimulus for the creation of this barrier, since isolated inner cell mass or artificial stimuli failed to induce such a barrier. Furthermore, the primary decidual zone induced by the normal blastocyst is impermeable to immunoglobulin molecules. These findings suggest that trophoblast-induced expression of tight junctions forms a temporary barrier in cells of the primary decidual zone that restricts the passage of injurious stimuli such as maternal immunoglobulins to the embryo.