Freeze-fracture and morphometric analysis of occluding junctions in rectal glands of elasmobranch fish

Abstract

The structure of occluding junctions in secretory and ductal epithelium of salt-secreting rectal glands from two species of elasmobranch fish, the spiny dogfishSqualus acanthias and the stingrayDasyatis sabina, was examined by thin-section and freeze-fracture electron microscopy. In both species, occluding junctions between secretory cells are shallow in their apical to basal extent and are characterized by closely juxtaposed parallel strands. Average strand number in the dogfish was 3.5±0.2 with a mean depth of 56±5 nm; in the stingray a mean of 2.0±0.2 strands encompassed an average depth of 18±3 nm. In contrast, the linear extent of these junctions was remarkably large due to the intermeshing of the narrow apices of the secretory cells to form the tubular lumen. Morphometric analysis gave values of 66.8±2.5 and 74.9±4.6 m/cm² for the length of junction per unit of luminal surface area in the dogfish and stingray, respectively. This junctional morphology is similar to that generally described for “leaky” epithelia. In comparison, the stratified ductal epithelium which carries the NaCl-rich secretion to the intestine is characterized by extensive occluding junctions which extend 0.6–0.8 μm in depth and consist of a mean of 12 strands arranged in an anastomosing network, an architectural pattern typical of “tight” epithelia. The length density of these junctions in the dogfish rectal gland was 7.6±0.1 m/cm². The junctional architecture of the rectal gland secretory epithelium (few strands, large junctional length densities) is similar to that described for several other hypertonic secretory epithelia [20, 34] and is compatible with the recent model for salt secretion in rectal glands [39] and in other Cl⁻ secretory epithelia which posits a conductive paracellular pathway for transepithelial Na⁺ secretion from intercellular space to the lumen to form the NaCl-rich secretory product.