Development of structure and function in the mammalian yolk sac: I. Developmental morphology and vitamin B 12 uptake of the rat yolk sac

Abstract

Morphological and physiological aspects of differentiation have been analyzed in the visceral splanchnopleure of the inverted yolk sac placenta of the albino rat between 13 days and term. The visceral yolk sac is known to be involved in the transfer of antibodies from the maternal to the fetal blood. The absorptive cells of the visceral endoderm possess ultrastructural features characteristic of protein-absorbing cells. The appearance of the free surface of these simple columnar cells suggests motility. It is primarily modified to form long, branching microvilli that often seem to be fusing. Invaginations of the free surface originate between microvilli, and most probably connect with an extensive canalicular system of smooth membranes located in the superficial cytoplasm. The inner surface of both the invaginations and the canaliculi possesses a filamentous coat that may represent a vast internal surface for the attachment of proteins. Morphological and physiological evidence suggests that large absorptive vacuoles arise as dilatations of the canaliculi. The content of the more deeply located vacuoles is more condensed, and they may be called absorptive droplets. Thus, a superficial system of smooth membranes is directly involved in the uptake of macromolecules, such as antibodies and other proteins. During this period of gestation various morphological changes occur that may affect absorptive activity considerably. As gestation proceeds, the microvilli become shorter and less branched; the smooth membrane system is altered; and intercellular associations change as large dilatations appear in the intercellular space of the absorptive epithelium. In addition, there is a thickening of the placental barrier that intervenes between the yolk sac (or uterine cavity) and the vitelline circulation. The present findings indicate that the visceral yolk sac possesses a highly specific mechanism for accumulating considerable vitamin B 12 and B 12-intrinsic factor complex in vitro. The parietal wall lacks this mechanism. The capacity to concentrate vitamin B 12 and B 12-intrinsic factor both in vivo and in vitro is greater at 13 days than near term when determined on the basis of radioactivity per unit weight. This suggests a decrease in absorptive capacity per cell as gestation proceeds. The reduced absorptive activity of each cell is, however, more than counterbalanced by a seventyfold increase in the mass of this placental membrane. Microscopic examination revealed that the morphology of the visceral yolk sac is well preserved during a 60-minute period of in vitro incubation. Experimental findings in vitro indicate that although the visceral splanchnopleure can accumulate a large macromolecular complex, such as vitamin B 12-IF, it lacks the capacity to concentrate small molecules, such as l-valine and α-methylglucoside, against a concentration gradient. This evidence suggests that this placental membrane in the rat may be highly specialized for the transfer of macromolecules.