Morphological and functional aspects of the canine placental barrier: Evidence supporting a deciduo-chorial model

Abstract The canine placenta, characterized by its deciduate and endotheliochorial nature, represents an intermediate placental type between non-invasive and highly invasive placentas. Decidual cells are involved in the prepartum parturition cascade. As they are the only cells expressing the nuclear progesterone receptor (PGR), they play a crucial role in luteal progesterone (P4)-dependent embryo-maternal communication and are essential for maintaining pregnancy. This study focuses on the quantity, morphology, and spatial arrangement of decidual cells. Immunohistochemistry (IHC) was used to localize and quantify PGR-expressing cells. Consecutive tissue sections were evaluated utilizing anti-PGR, -vimentin, and -pan-cytokeratin antibodies, providing insights into decidual cell morphology. This was followed by transmission electron microscopy (TEM) and serial section scanning electron microscopy (SEM) generating high-resolution 2D and 3D images, leading to reconstructions of decidual cells and their morphological interactions with neighboring cellular compartments. A significant reduction in PGR-expressing cells was observed at prepartum luteolysis. Decidual cells were found to be polymorph with extensive cytoplasmic branches, varying individually in their morphology. Further, for the first time, the 3D reconstructions highlighted the complex network of decidual cells, which were shown to form part of the feto-maternal barrier, supporting the existence of a deciduo-chorial interface in the canine placenta. Therefore, we propose a role for decidual cells as a morphological and biochemically active barrier between the fetal and maternal compartments. The decreasing P4/PGR signaling towards prepartum luteolysis is possibly associated with a reduction in the number of decidual cells during the progression of pregnancy as a sign of placental maturation toward parturition. Lay summary The dog has a deciduate placenta, meaning that specific maternal cells (decidual cells) form part of the placenta. This placenta shows restricted invasive behavior of fetal cells (trophoblast) into maternal uterine structures. Decidual cells are involved in the hormonal processes leading up to birth. They are the only placental cells expressing the nuclear progesterone receptor (PGR), which allows them to respond to progesterone, needed for the maintenance of pregnancy. This study focuses on the number, shape, and arrangement of decidual cells. We also found a significant reduction in PGR-expressing cells shortly before birth, when progesterone levels decrease. Interestingly, the drop in progesterone signaling is associated with a reduction in the number of decidual cells, indicating maturation of the placenta in preparation for delivery. Using electron microscopy, decidual cells were found to be irregularly shaped with long, branching extensions. For the first time, 3D reconstructions highlighted the complex network of decidual cells, which were shown to form part of the contact zone between mother and fetus - supporting the existence of a new type of interface in the canine placental labyrinth.