The Ruminant Placental Trophoblast Binucleate cell – an evolutionary breakthrough.

Abstract

ABSTRACT

Viviparity and the development of a placenta are two of the major reasons for the success of the mammals in colonising all habitats, both terrestrial and aquatic. The placenta is an apposition of fetal to maternal tissue which serves two main, but competing functions: to maximise oxygen transfer and the acquisition of nutrients from the mother, but to minimise immunological rejection by the maternal immune system. This has resulted in the evolution of four main types differing in the degree of loss of the maternal uterine epithelial (UE) barrier: epitheliochorial, synepitheliochorial, endotheliochorial and hemochorial, all providing a successful safe balance between the needs of mother and fetus. Epitheliochorial is the least invasive, a simple apposition and microvillar interdigitation of the apices of uterine epithelium and trophoblast. It is suggested to have evolved as response to the increase in size of the animal to provide a sufficiently long gestation to produce a single altricial (run/swim- soon- as- born) neonate as in the Cetartiodactyla. The mother needs to have good control of the fetal demands so the uterine epithelial barrier is maintained. However in the synepitheliochorial placenta, characteristic of all ruminants, the fetus has evolved a means of increasing, or at least maintaining, demand without the need for invasion. This it has achieved by the development of the trophoblast binucleate cell (BNC) which, uniquely, can fuse with a uterine epithelial cell to form fetomaternal hybridtissue. This can maintain some maternal barrier function but also deliver fetally synthesised immunomodulatory and metabolic messages to the maternal circulation. This review provides the evidence for this remarkable evolutionary step and also considers an alternative explanation for the formation of the structure of the ruminant placenta.