Endothelial cell hyperproliferation and stratification in uteroplacental blood vessels of the black mastiff bat, Molossus rufus

Abstract

Placentation was studied histologically and immunocytochemically in black mastiff bats obtained at frequent intervals throughout pregnancy. These were bred in a captive colony or collected from a reproductively-synchronized wild population. During late pregnancy, the single fetus was largely sustained by a discoidal, hemochorial placenta located at the cranial end of the right uterine horn. This invariant positioning was determined by a vascular tuft that developed there both during early pregnancy and non-pregnant cycles. This provided a scaffold for early placental morphogenesis. As development proceeded, small arterioles and venules serving the tuft were converted to large uteroplacental vessels. Within the base of the placenta, these became lined by an unusual vascular epithelium composed of intermingled patches of multilayered endothelial cells and cytotrophoblast. Initially, the endothelium became multilayered by hypertrophy, proliferation, and infolding of its basal lamina. These created endothelial bilayers usually insinuated between basal laminae. The development of temporary gaps in the laminae then permitted further enlargement of the vessels and proliferation of the endothelial cells as monolayer sheets or chains. The latter were interconnected, forming a complex, stratified, cellular network associated with a prominent meshwork of basal laminae. Throughout much of pregnancy, these endothelial cells were cuboidal to columnar and possessed an abundance of basal glycoprotein granules presumably containing basal lamina precursors. The cells also expressed vimentin and frequently von Willebrand factor, but not cytokeratins or desmin. Pronounced thickening of the endothelia and amplification of their basal laminae likely evolved to greatly strengthen the walls of the uteroplacental vessels.