We investigated the origin of the apical transcytic membrane system in jejunal absorptive cells of neonatal rats using light, electron, and immunofluorescence microscopy. In rats just after birth, intraluminally injected horseradish peroxidase (HRP), used as a macromolecular tracer, was observed only in the apical endocytic membrane system including the lysosomes, of jejunal absorptive cells in vivo. No tracer, however, was found in the intercellular space between the jejunal absorptive cells and the submucosa. Immunoreactive neonatal Fc receptor (FcRn) was localized in the perinuclear region of these absorptive cells whereas immunoglobulin G (IgG) was not found in these absorptive cells. In contrast, in rats 2 h after breast-feeding, intraluminally injected HRP was observed in the apical endocytic membrane system and in the apical transcytic membrane system of the absorptive cells. Moreover, HRP was found in the intercellular space between the jejunal absorptive cells and the submucosa. Furthermore, FcRn and IgG were widely distributed throughout the absorptive cells, and IgG was detected in both the intercellular space and the submucosa. These data suggest that initiation of breast-feeding induces the transportation of membrane-incorporated FcRn from its perinuclear localization to the apical plasma membrane domain. This transportation is achieved through the membrane system, which mediates apical receptor-mediated transcytosis via the trans-Golgi network. Subsequently, the apical plasma membrane containing the FcRn binds to maternal IgG, is endocytosed into the absorptive cells, and is transported to the basolateral membrane domain.