Cellular calcium transport in fish: Unique and universal mechanisms

The tilapia, Oreochromis mossambicus, is a truly euryhaline species in that it lives, grows, and reproduces in freshwater as well as in full-strength seawater. The gills, intestine, and kidneys show ionoregulatory adaptations fundamental for the calcium balance of this fish in these vastly different ionic media. This review focuses on calcium flows in these ionoregulatory organs and the changes that occur in the Ca²⁺-transporting mechanisms in the basolateral plasma membrane compartment of the cells that make up their ion-transporting epithelia. Influx of Ca²⁺ via the gills is comparable in freshwater and seawater; also, the Ca²⁺-ATPase and Na⁺/Ca²⁺ exchanger in branchial epithelial plasma membranes have comparable activities in fish adapted to freshwater and in those adapted to seawater. Ussing chamber experiments with isolated opercular membranes (a flat epithelium with chloride cells) suggest that chloride-cell-mediated, inward Ca²⁺ transport is largely dependent on Na⁺-dependent mechanisms. The Ca²⁺-ATPase is thought to play a "housekeeping" role in cellular Ca²⁺ regulation. Intestinal epithelial Ca²⁺ flux is lower in seawater fish than in freshwater fish, and this may reflect adaptation to the imminent overload of calcium in seawater, where for the uptake of water the fish drinks a 10-millimolar Ca solution. Intestinal Ca²⁺ transport is fully dependent on serosal Na⁺. Accordingly, a powerful Na⁺/Ca²⁺ exchanger operates in the basolateral plasma membrane of the enterocyte, and in particular the capacity of this transporter decreases in seawater fish. The kidney of freshwater fishes produces a typical dilute and hypocalcic urine; in seawater, urine production decreases and the urine calcium concentration is always higher than that of the plasma. Exchange activity of Na⁺ and Ca²⁺ is undetectably low or absent in renal tissue plasma membranes. However, a high-affinity, high-capacity Ca²⁺-ATPase activity appears to correlate with Ca²⁺ reabsorption, as its activity significantly decreases after transfer of the fish to seawater. It thus appears that ATP- and Na⁺-dependent Ca²⁺ pumps are differentially expressed in gills, intestine, and kidney. Their activity may explain an ATP- or Na⁺-dependence of Ca²⁺ flow in the pertinent epithelium.