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Osmoregulatory mechanisms in seawater
- Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys : Implications for osmoregulation in fresh and seawater


When in seawater, teleosts and lampreys are confronted with the reverse situation to that in freshwater, i.e. they experience an osmotic loss of water to the environment. The further loss of water through the kidneys is minimised by reducing excretion from this source to just a small amount of concentrated urine. The osmotic loss of water is overcome by swallowing seawater, resorbing monovalent ions and water from the gut and retaining the `free' water that remains following the secretion of an hypertonic solution of Na+ and Cl across the gills (Fig. 1B; Smith, 1930Go; Karnaky, 1980Go, 1986Go; Loretz, 1995Go). As long ago as 1932, Keys and Willmer considered that Cl is secreted by the gill epithelium through a large eosinophilic cell that resembles the parietal cell in the gastric mucosa of mammals and which was consequently termed the `chloride secreting cell' (Keys and Willmer, 1932Go). The cytoplasm of this cell contains numerous mitochondria and a system of membranous tubules (Philpott and Copeland, 1963Go; Karnaky et al., 1976aGo; Pisam and Rambourg, 1991Go). This membranous tubular system, which represents a vast intracellular amplification of the basolateral cell membrane, is the site of Na+/K+-ATPase activity and an Na+/K+/2Cl cotransport system (Karnaky et al., 1976bGo; Karnaky, 1980Go, 1986Go; Eriksson et al., 1985Go). The mechanism by which Na+ and Cl are transported by the gill epithelium of marine teleosts has been resolved through work on the opercular epithelium, which, in some teleost species, contains numerous chloride cells and, in contrast to the gill surface, is flat and thus suitable for studies in an Ussing-like chamber (Karnaky and Kinter, 1977Go).

Concomitant morphological and electrophysiological studies using the opercular epithelium have confirmed that, when teleosts are in seawater, Cl is secreted by this cell type through a secondary active transport that provides the driving force for the passive transport of Na+ through leaky pathways between adjacent chloride cells (Karnaky et al., 1977Go; Ernst et al., 1980Go; Foskett and Scheffey, 1982Go; Foskett and Machen, 1985Go). The channel through which Cl is secreted by the teleost chloride cell has now been identified as a homologue of the mammalian cystic fibrosis transmembrane conductance regulator (CFTR; Singer et al., 1998Go; Wilson et al., 2000bGo; Marshall et al., 2002Go). Identical mechanisms for hypertonic salt secretion are also present in the secretory cells of both the rectal gland of elasmobranch fishes and the nasal salt gland of some species of marine birds (Kirschner, 1977Go, 1980Go; Riddle and Ernst, 1979Go; Ernst et al., 1981Go). It is thus assumed that this mechanism is universally employed by vertebrates for osmoregulation in hypertonic environments.

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