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


When in freshwater, fish are subjected to an osmotic influx of water and efflux of ions across their skin and gills. This problem is overcome by an active uptake of monovalent ions across the gills and the excretion of a copious and dilute urine by the kidney (Fig. 1A; Smith, 1932Go; Krogh, 1939Go; Parry, 1966Go; Perry, 1997Go). The uptake of Na+ and Cl by various vertebrates in freshwater, i.e. under in vivo conditions, is stoichiometrically balanced and occurs independently by exchanging H+ for Na+ and HCO3 for Cl (Krogh, 1939Go; Kirschner, 1983Go). The models developed for these ion exchange mechanisms were derived mostly from the results of studies carried out in Ussing-like chambers. Since such studies require the use of flat sheets of tissues, they have been performed mainly on amphibian epidermis, which, in contrast to the fish gill, has a flat surface (Garcia-Romeu and Ehrenfeld, 1975Go; Kirschner, 1983Go; Larsen, 1988Go). The results of these studies have led to the general acceptance that the exchange of Na+ for H+ involves an active secretion of H+ by an electrogenic H+-ATPase and the uptake of Na+ through an epithelial Na+ channel (ENac), rather than occurring simply through an Na+/H+-antiport. This mechanism is dependent on the activities of both cytosolic carbonic anhydrase in the H+ secreting cell and Na+/K+-ATPase in the basolateral membrane of the cell whose apical membrane contains the ENac (Harvey and Ehrenfeld, 1986Go; Harvey et al., 1988Go; Nagel and Dörge, 1996Go; Ehrenfeld and Klein, 1997Go). Furthermore, the toad and turtle urinary bladders, in which the epithelium has a cellular composition comparable with that of amphibian skin and consists also of granular cells and mitochondria-rich (MR) cells (Wade et al., 1975Go; Wade, 1976Go; Rick et al., 1978Go; Durham and Nagel, 1986Go; Brown and Breton, 1996Go), employ essentially the same mechanisms for reabsorbing Na+ from the urine and for secreting H+ into that urine (Stetson and Steinmetz, 1985Go; Durham and Nagel, 1986Go; Lang, 1988Go). In addition, the immunocytochemical demonstration that H+-ATPase and ENac are present in the gill epithelium of teleosts (Sullivan et al., 1995Go; Wilson et al., 2000aGo; Marshall, 2002Go) is consistent with the hypothesis that this mechanism for taking up Na+ from a hypotonic environment is universal amongst vertebrates and invertebrates such as crustaceans, annelids and molluscs (Kirschner, 1983Go).

In contrast to the indirect coupling of Na+ uptake to H+ secretion, as described above, the uptake of Cl from an hypotonic environment by all epithelia studied thus far occurs directly by means of an HCO3/Cl antiport (Garcia-Romeu and Ehrenfeld, 1975Go; Larsen, 1991Go; Marshall et al., 1997Go). The cells engaged in Cl uptake are further characterised by the presence of cytosolic carbonic anhydrase and a Cl channel in their basolateral membrane (Larsen, 1991Go).

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