Morphogenesis of the horny jaws of Rana pipiens larvae

Abstract Anuran larvae possess oral appendages, the horny teeth and jaws, for grasping and shearing food. Unlike true vertebrate teeth, the shearing organ of tadpoles is constructed from horny epidermal cells organized into a beak. After the initial differentiation of the horny jaws, basal epithelial cells continue to divide and differentiate into horny cells, a morphogenetic process comparable to that of other epidermal appendages such as claws. In the present study the morphogenesis of the horny jaws has been examined with the electron microscope. The sequence of cellular division and differentiation in the larval jaws has been confirmed by autoradiography. The horny jaws are composed of a core of palisaded columns of cells, and a sheath covering the core, tapered toward the cutting edge of the jaw. The apical horny cells of each column are arranged like a stack of hollow cones, tightly linked laterally by means of interdigitating membranes and desmosomes with the cells of adjacent columns. The most apical horny cells of each column comprise a rigid serrate cutting edge for the jaw. Each such cell is derived from the basal columnar epithelium in a series of cellular transformations. The basal cells first differentiate into cuboidal cells, then into precone cells flattened perpendicularly to the basal columnar cells. Each precone cell develops a hillock at its apical surface while its basal surface becomes concave. The hillock gradually becomes more pointed, the base more concave, until a stack of conical cytoplasmic shells is formed, each cone encasing the one proximal to it. Free ribosomes, endoplasmic reticulum, and Golgi membranes are abundant and nucleoli are prominent in all column cells, indicating a high degree of synthetic activity. Keratin fibrils appear in the basal cells of the column, becoming more numerous and electron dense in cone cells. The fine structure of individual fibrils and their rapid coalescence in horny cone cells indicate a fibrous, hard type of keratin. A horny sheath, composed of plate-shaped squamous epithelial cells covers the core of the jaw orally and labially. Plate cells buttress the columns, each forming a tongue-in-groove association with the base of a cone cell. Although derived from the basal epithelium, the plate cells differ from column cells in shape, orientation, and mode of keratinization. Bundles of tonofilaments are formed which retain their tonofilamentous substructure up to the final stages of keratinization. The horny plate cells have a mottled appearance, due to large, electron translucent vacuoles. Mucous granules also occur throughout the cells of the jaws, even in keratinizing cone and plate cells. Cellular renewal of the horny jaws occurs during larval stages. Following injection of stage VI larvae with tritiated thymidine, autoradiographs of sections through the head reveal heavy labeling of basal epithelial cell nuclei. Seven days after injection the label appears distally in the sheath, but only proximally in the columns, in precone cells. Heavy labeling is absent from all regions of the sheath by 21 days, whereas cone cells of the columns are labeled at that time. The difference in rate of movement of the label in the sheath and columns may reflect different rates of morphogenesis in these regions.