The ultrastructure of oral (buccopharyngeal) membrane formation and rupture in the anuran embryo

Abstract

The ultrastructure of the oral (buccopharyngeal) membrane was examined by transmission and electron microscopy in the anuran, Rana japonica, embryo. The stomodeum is recognizable on the ventral surface anterior to the neural folds as the neural folds are beginning to close (neural tube stage). The stomodeum is gradually enlarged and deepened as development proceeds. At the neural tube stage, the oral membrane is 5-7 cell layers thick and the stomodeal ectodermal cells are cuboidal and the foregut endodermal cells are cuboidal or columnar. Desmosomes and basal lamina could not be found between the ectodermal and endodermal epithelia. The oral membrane gradually thins between the neural tube and hatching stages. At the hatching stage, the oral membrane becomes two or three cell layers thick and each cell is flattened. Many perforations of the oral membrane after hatching and the oral membrane appears "net-like." Necrotic cells occur in the oral membrane and these cells contain many autophagic vacuoles. ACPase-positive lysosomes, Golgi regions, and autophagic vacuoles were present in the oral membrane. At the asymmetrical trunk stage, a large part of the oral membrane disappears and only remnants are left.

Hedgehog activity controls opening of the primary mouth

“…Anatomical characterization in diverse systems including sea urchins, urodeles, Xenopus , and mouse have suggested that interactions between foregut and stomodeal ectoderm are important for oral perforation (Dickinson and Sive, 2006; Hardin and Armstrong, 1997; McClay et al, 1992; Poelmann et al, 1985; Soukup et al, 2013; Takahama et al, 1988; Theiler, 1969; Watanabe et al, 1984; Waterman, 1977). However, molecular regulation of primary mouth opening is largely untested, especially as perforation occurs early in development and perturbation of major signaling cascades results in broad cranial defects.…”

“…The primary mouth marks the location of this interface, and perforation is essential (Dickinson and Sive, 2006; Hardin and Armstrong, 1997; McClay et al, 1992; Poelmann et al, 1985; Soukup et al, 2013; Takahama et al, 1988; Watanabe et al, 1984). Despite the fundamental importance of the primary mouth, little is known about the molecular control of its development.…”

Tissue fusion and cell sorting in embryonic development and disease: biomedical implications

“…(26) However, we propose that, in many cases, the possibility of partial intercalation has simply not been studied, and the occurrence of cell intercalation seems evident in mesenchymal fusion. Furthermore, this could be an alternative mechanism accounting for the perforation of epithelial membranes to connect different cavities as occurs in opening of the oral membrane in Rana japonica, (29) in the urogenital and the anal membranes during cloacal/anorectal morphogenesis in chick, mouse, rat and human embryos. (30)(31)(32)(33) Cellular rearrangements resulting in the incorporation of transient epithelial cells into adjacent epithelia represents another possible mechanism for the perforation of membranes.…”

Using frogs faces to dissect the mechanisms underlying human orofacial defects

“…This is especially evident when the buccopharyngeal membrane is fluorescently labeled for actin in Xenopus (Fig 2C–E). The “stretching” of cells as the buccopharyngeal membrane ruptures can also be observed in mammals (including humans) [26, 27] and other frog species [28, 29]. Based on this stretched appearance of the cells, we have formulated the hypothesis that the process of buccopharyngeal perforation is mediated by biomechanical forces (Fig.…”