Abstract
All marine vertebrates regulate the salt concentration of their body fluids to levels far below those found in the marine environment. In addition to renal mechanisms, osmotic homeostasis is maintained by the active excretion of NaCl from specialized organs, the location and structure of which varies considerably among the classes of vertebrates. Thus in marine teleosts, the gill is the primary site of extra-renal salt secretion, while in elasmobranch fish the rectal gland fulfills this role. In marine birds, paired glands located just above the orbits of the eyes are responsible for salt secretion. Considering the phylogenetic diversity and varied anatomical location of these organs, one might expect that the secretory cells that comprise each of these glands would exhibit a comparable diversity of structure. This, however, is not the case. Rather, the commonality of function shared by these cells is mirrored in the underlying similarity of their cytoarchitectural design. The most salient features shared by these epithelial cells are an extensive elaboration of basolateral plasma membranes and an abundant supply of mitochondria, the mitochondria generally in close proximity to the amplified basal and lateral cell surfaces. Other structural features, such as specific modifications of the occluding junctions that unite adjacent secretory cells, also exhibit marked similarities in these salt secretory tissues.
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References
Bonting SL, Caravaggio LL, Canady MR, and Hawkins NM (1964) Studies on sodium-potassium activated adenosinetriphosphatase XI. The salt gland of the herring gull. Arch. Biochem. Biophys. 106: 49–56.
Bradley TJ (1981) Improved visualization of apical vesicles in chloride cells of fish gills using an osmium quick-fix technique. J. Exp. Zool. 217: 185–198.
Bulger RE (1963) Fine structure of the rectal (salt-secreting) gland of the spiny dogfish Squalus acanthias. Anat. Rec. 147: 95–127.
Burger JW and Hess WN (1960) Function of the rectal gland in the spiny dogfish. Science 131: 670–671.
Dahl JL and Hokin LE (1974) The sodium-potassium adenosinetriphosphatase. Ann. Rev. Biochem. 43: 327–356.
Degnan KJ, Karnaky KJ Jr, and Zadunaisky JA (1977) Active chloride transport in the iri vitro opercular skin of a teleost (Fundulus heteroclitus), a gill-like epithelium rich in chloride cells. J. Physiol. (Lond.) 271: 155–191.
Dunel-Erb S and Laurent P (1980) Ultrastructure of marine teleost gill epithelia: SEM and TEM study of the chloride cell apical membrane. J. Morphol. 165: 175–186.
Ellis RA, Goertemiller CC Jr, and Stetson DL (1977) Significance of extensive ‘leaky’ cell junctions in the avian salt gland. Nature 268: 555–556.
Ernst SA (1972a) Transport adenosine triphosphatase cytochemistry. I. Biochemical characterization of a cytochemical medium for the ultrastructural localization of ouabain-sensitive, potassium-dependent phosphatase activity in the avian salt gland. J. Histochem. Cytochem. 20: 13–22.
Ernst SA (1972b) Transport adenosine triphosphatase cytochemistry. II. Cytochemical localization of ouabain-sensitive, potassium-dependent phosphatase activity in the secretory epithelium of the avian salt gland. J. Histochem. Cytochem. 20: 23–38.
Ernst SA (1975) Transport ATPase cytochemistry: ultrastructural localization of potassium-dependent and potassium-independent phosphatase activities in the rat kidney cortex. J. Cell Biol. 66: 586–608.
Ernst SA, Dodson WC, and Karnaky KJ Jr (1980) Structural diversity of occluding junctions in the low-resistance chloride-secreting opercular epithelium of seawater-adapted killifish (Fundulus heteroclitus). J. Cell Biol. 87: 488–497.
Ernst SA and Ellis RA (1969) The development of surface specialization in the secretory epithelium of the avian salt gland in response to osmotic stress. J. Cell Biol. 40: 305–321.
Ernst SA, Goertemiller CC Jr, and Ellis RA (1967) The effect of salt regimens on the development of (Na+-K+)-dependent ATPase activity during the growth of salt glands of ducklings. Biochim. Biophys. Acta 135: 682–692.
Ernst SA and Hootman SR (1981) Microscopical methods for the localization of Na+, K+-ATPase. Histochem. J. 13: 397–418.
Ernst SA, Hootman SR, Schreiber JH, and Riddle CV (1981) Freeze-fracture and morphometric analysis of occluding junctions in rectal glands of elasmobranch fish. J. Membrane Biol. 58: 101–114.
Ernst SA and Mills JW (1977) Basolateral plasma membrane localization of ouabain-sensitive sodium transport sites in the secretory epithelium of the avian salt gland. J. Cell Biol. 75: 74–94.
Ernst SA and Mills JW (1980) Autoradiographic localization of tritiated ouabain-sensitive sodium pump sites in ion transporting epithelia. J. Histochem. Cytochem. 28: 72–77.
Ernst SA, Riddle CV, and Karnaky KJ Jr (1980) Relationship between localization of Na+-K+-ATPase, cellular fine structure, and reabsorptive and secretory electrolyte transport. In: Bronner F and Kleinzeller A (eds.) Current Topics in Membranes and Transport, vol. 13. Academic Press, New York, pp. 355–385.
Ernst SA and Schreiber JH (1981) Ultrastructural localization of Na+, K-ATPase in rat and rabbit kidney medulla. J. Cell Biol. 91: 803–813.
Ernst SA and Van Rossum GDV (1982) Ions and energy metabolism in duck salt gland: possible role of furosemide-sensitive co-transport of sodium and chloride. J. Physiol. (Lond.) 325: 333–352.
Eveloff J, Karnaky KJ Jr, Silva P, Epstein FH, and Kinter WB (1979) Elasmobranch rectal gland cell: autoradiographic localization of 3H-ouabain-sensitive Na, K-ATPase in rectal gland of dogfish, Squalusacanthias. J. Cell Biol. 83: 16–32.
Forrest JN Jr, Cohen AD, Schon DA, and Epstein FH (1973) Na transport and Na-K-ATPase in gills during adaptation to seawater: effects of cortisol. Am. J. Physiol. 224: 709–713.
Foskett JK and Scheffey C (1982) The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215: 164–166.
Goertemiller CC Jr and Ellis RA (1976) Localization of ouabain-sensitive, potassium dependent nitrophenyl phosphatase in the rectal gland of the spiny dogfish, Squalus acanthias. Cell Tissue Res. 175: 101–112.
Hannafin J, Kinne-Saffran E, Friedman D, and Kinne R (1983) Presence of a sodium-potassium chloride cotransport system in. the rectal gland of Squalus acanthias. J. Membrane Biol. 75: 73–83.
Hokin LE, Dahl JL, Deupree JD, Dixon JF, Hackney JF, and Perdue JF (1973) Studies on the characterization of the sodium-potassium transport adenosine triphosphatase. X. Purification of the enzyme from the rectal gland of Squalus acanthias. J. Biol. Chem. 248: 2593–2605.
Hootman SR and Ernst SA (1980) Dissociation of avian salt gland: separation procedures and characterization of dissociated cells. Am. J. Physiol. 238: C184–C195.
Hootman SR and Ernst SA (1981) Effect of methacholine on Na+ pump activity and ion content of dispersed avian salt gland cells. Am. J. Physiol. 241: R77–R86.
Hootman SR and Philpott CW (1978) Rapid isolation of chloride cells from pinfish gills. Anat. Rec. 190: 687–702.
Hootman SR and Philpott CW (1979) Ultracytochemical localization of Na+, K+-activated ATPase in chloride cells from the gills of a euryhaline teleost. Anat. Rec. 193: 99–130.
Hootman SR and Philpott CW (1980) Accessory cells in teleost branchial epithelium. Am. J. Physiol. 238: R199–R206.
Karnaky KJ Jr, Kinter LB, Kinter WB, and Stirling CE (1976) Teleost chloride cell. II. Autoradiographic localization of gill Na, K-ATPase in killifish Fundulus heteroclitus adapted to low and high salinity environments. J. Cell Biol. 70: 157–177.
Keys AB (1931) Chloride and water secretion and absorption by the gills of the eel. Z. Vgl. Physiol. 15: 364–388.
Keys AB and Willmer EN (1932) Chloride secreting cells in the gills of fishes with special reference to the common eel. J. Physiol. (Lond.) 76: 368–378.
Kyte J (1976a) Immunoferritin determination of distribution of (Na++K+) ATPase over the plasma membranes of renal convoluted tubules. I. Distal segment. J. Cell Biol. 68: 287–303.
Kyte J (1976b) Immunoferritin determination of distribution of (Na++K+)ATPase over the plasma membranes of renal convoluted tubules. II. Proximal segments. J. Cell Biol. 68: 304–318.
Martin BJ and Philpott CW (1973) The adaptive response of the salt glands of adult mallard ducks to a salt water regime: an ultrastructural and tracer study. J. Exp. Zool. 186: 111–122.
Mayahara H, Fujimoto K, Ando T, and Ogawa K (1980) A new one-step method for the cytochemical localization of ouabain-sensitive, potassium-dependent p-nitrophenylphosphatase activity. Histochemistry 67: 125–138.
Mayahara H and Ogawa K (1980) Ultracytochemical localization of ouabainsensitive, potassium-dependent p-nitrophenylphosphatase activity in the rat kidney. Acta Histochem. Cytochem. 13: 90–102.
Philpott CW and Copeland DE (1963) Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18: 389–404.
Pisam M (1981) Membranous systems in the chloride cell of teleostean fish gill; their modifications in response to the salinity of the environment. Anat. Rec. 200: 401–414.
Riddle CV and Ernst SA (1979) Structural simplicity of the zonula occludens in the electrolyte secreting epithelium of the avian salt gland. J. Membrane Biol. 45: 21–35.
Ritch R and Philpott CW (1969) Repeating particles associated with an electrolyte-transporting membrane. Exp. Cell Res. 55: 17–24.
Schwartz M, Ernst SA, Seigel GJ, and Agranoff BW (1981) Immunocytochemical localization of (Na+, K+)-ATPase in the goldfish optic nerve. J. Neurochem. 36: 107–115.
Silva P, Stoff J, Field M, Fine L, Forrest JN, and Epstein FH (1977) Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport. Am. J. Physiol. 233: F298–F306
Stewart DJ, Semple EW, Swart GT, and Sen AK (1976) Induction of the catalytic protein of (Na++K+)-ATPase in the salt gland of the duck. Biochim. Biophys. Acta 419: 150–163.
Stirling CE (1976) High resolution autoradiography of 3H-ouabain binding in salt transporting epithelia. J. Microscopy 106: 145–157.
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Hootman, S.R., Ernst, S.A. (1984). Ultrastructural Localization of Na++K+-ATPase in Specialized Membranes of Salt Transporting Cells in Marine Vertebrates. In: Pequeux, A., Gilles, R., Bolis, L. (eds) Osmoregulation in Estuarine and Marine Animals. Lecture Notes on Coastal and Estuarine Studies, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-45574-2_11
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DOI: https://doi.org/10.1007/978-3-642-45574-2_11
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