Summary
Tissue from the digitiform rectal gland of the spiny dogfish, Squalus acanthias, was fixed briefly by formaldehyde perfusion and studied for the specificity and localization of p-nitrophenyl phosphatase (NPP'ase) activity. The enzymatic activity was K+-dependent (56%) and ouabain-sensitive (67% inhibition). The electron-dense reaction product (SrPO4) of the cytochemical reaction (Ernst, 1972b) was localized along the inner surfaces of the basolateral membranes of the secretory cells. It was absent from mitochondria, nuclei, vesicles, and other organelles. The luminal surface of the secretory cells was slightly reactive. On the basis of (1) this pattern of localization for the sodium transport system, (2) the presence of extensive intercellular labyrinthine channels (Bulger, 1963) that would facilitate “standing gradients” (Diamond and Bossert, 1968), and (3) the specific distribution of the energy-providing mitochondria, we conclude that the concentration and electrochemical gradients recorded from the secreting gland (Hayslett et al., 1974) are maintained across the domains of the basolateral surfaces of the secretory cells.
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References
Berridge, M.J., Oschman, J.L.: Transporting epithelia, p. 4. New York: Academic Press 1972
Bonting, S.L.: Studies on sodium-potassium-activated adenosine triphosphatase. XV. The rectal gland of the elasmobranch. Comp. Biochem. Physiol. 17, 953–966 (1966)
Bulger, R.E.: Fine structure of the rectal (salt-secreting) gland of the spiny dogfish, Squalus acanthias. Anat. Rec. 147, 95–127 (1963)
Bulger, R.E.: Electron microscopy of the stratified epithelium lining the excretory canal of the dogfish rectal gland. Anat. Rec. 151, 589–607 (1965)
Burger, J.W.: Further studies of the rectal gland in the spiny dogfish. Physiol. Zool. 35, 205–217 (1962)
Burger, J.W., Hess, W.N.: Function of the rectal gland in the spiny dogfish. Science 131, 670–671 (1960)
Diamond, J., Bessert, W.H.: Functional consequences of ultrastructural geometry in backwards fluid transporting epithelia. J. Cell Biol. 37, 694–702 (1968)
Doyle, W.L., Secretory cells of the rectal salt-gland of an elasmobranch, Urolophus. Anat. Rec. 142, 228 (1962a)
Doyle, W.L.: Tubule cells of the rectal salt-gland of Urolophus. Amer. J. Anat. 111, 223–238 (1962b)
Ellis, R.A., Goertemiller, Jr., C.C.: Cytological effects of salt-stress and localization of transport adenosine triphosphatase in the lateral nasal glands of the desert iguana, Dipsosaurus dorsalis. Anat. Rec. 180, 285–297 (1974)
Ellis, R.A., Goertemiller, Jr., C.C.: Scanning electron microscopy of intercellular channels and the localization of ouabain-sensitive p-nitrophenyl phosphatase activity in the salt-secreting lacrymal glands of the marine turtle, Chelonia mydas. Cytobiologie 13, 1–12 (1976)
Ernst, S.A.: 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 (1972a)
Ernst, S.A.: 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 (1972b)
Ernst, S.A., Ellis, R.A.: 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 (1969)
Ernst, S.A., Goertemiller, Jr., C.C., Ellis, R.A.: The effect of salt regimens on the development of (Na+-K+)-dependent ATP'ase activity during the growth of salt glands of domestic ducklings. Biochim. biophys. Acta (Amst.) 135, 682–692 (1967)
Ernst, S.A., Mills, J.W.: Basolateral localization of 3H-ouabain binding sites in avian salt gland. J. Cell Biol. 67, 111a (1975)
Firth, J.A.: Problems of specificity in the use of a strontium capture technique for cytochemical localization of ouabain-sensitive, potassium-dependent phosphatase in mammalian renal tubules. J. Histochem. Cytochem. 22, 1163–1168 (1974)
Fletcher, G.L., Stainer, I.M., Holmes, W.N.: Sequential changes in the adenosine triphosphatase activity and the electrolyte excretory capacity of the nasal glands of ducks (Anas platyrhynchos) during the period of adaptation to hypertonic saline. J. exp. Biol. 47, 375–391 (1967)
Hayslett, J.P., Schon, D.A., Epstein, M., Hogben, A.M.: In vitro perfusion of the dogfish rectal gland. Amer. J. Physiol. 226, 1188–1192 (1974)
Hokin, L.E.: Purification and properties of the sodium-potassium transport adenosinetriphosphatase from the rectal gland of the spiny dogfish, Squalus acanthias. J. Supramolec. Struct. 1, 336–347 (1973)
Jampol, L.M., Epstein, F.H.: Role of Na-K-ATP'ase in osmotic regulation by marine vertebrates. Bull. Mt. Desert Biol. Lab. 8, 32–34 (1968)
Katz, A.I., Epstein, F.H.: The physiological role of sodium-potassium activated adenosine triphosphatase in the active transport of cations across biological membranes. Israeli J. med. Sci. 3, 155–166 (1967)
Komnick, H., Komnick, U.: Electronenmikroskopische Untersuchungen zur funktionellen Morphologie des Ionentransportes in der Salzdrüse von Larus argentatus. V. Experimenteller Nachweis der Transportwege Z. Zellforsch. 60, 163–203 (1963)
Kominick, H., Wohlfarth-Bottermann, K.E.: Zur Cytologie der Rectaldrüsen von Knorpelfischen. I. Die Feinstruktur der Tubulusepithelzellen. Z. Zellforsch. 74, 123–144 (1966)
Lennep, E.W. van: Electron microscopic histochemical studies on salt-excreting glands in elasmobranchs and marine catfish. J. Ultrastruct. Res. 25, 94–108 (1967)
Mazurkiewicz, J.E., Hossler, F.E., Barrnett, R.J.: A new method for localization of Na+, K+ ATP'ase for the study of membrane biogenesis in the salt gland. J. Cell Biol. 63, 213a (1974)
Mills, J.W., Ernst, S.A.: Localization of sodium pump sites in frog urinary bladder. Biochim. biophys. Acta (Amst.) 375, 268–273 (1975a)
Mills, J.W., Ernst, S.A.: Localization of 3H-ouabain binding sites in frog skin. J. Cell. Biol. 67, 287a (1975b)
Peaker, M., Linzell, J.L.: Salt gland in birds and reptiles. Cambridge, England: Cambridge University Press 1975
Pitts, R.F.: Mechanisms of reabsorption and excretion of ions and water. Physiology of the kidney and body fluids, Chap. 7, p. 91. Chicago: Year Book Medical Publishers, Inc. 1963
Skou, J.C.: The (Na -K+) activated enzyme system and its relationship to transport of sodium and potassium. Quart. Rev. Biophys. 7, 401–434 (1975)
Stockem, W., Komnick, H., Wohlfarth-Bottermann, K.E.: Zur Cytologie der Rectaldrüsen von Knorpelfischen. II. Die Mikromorphologie des zentralen Sammelkanals. Helgoländer wiss. Meeresunters. 18, 424–452 (1968)
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This research was supported by NIH Research Grant AM 13455 from the Institute of Arthritis and Metabolic Diseases. The authors thank Mrs. Julia Gross for her excellent technical assistance and Mrs. Jean Waage for transcribing the manuscript
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Goertemiller, C.C., Ellis, R.A. Localization of ouabain-sensitive, potassium-dependent nitrophenyl phosphatase in the rectal gland of the spiny dogfish, Squalus acanthias . Cell Tissue Res. 175, 101–112 (1976). https://doi.org/10.1007/BF00220826
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DOI: https://doi.org/10.1007/BF00220826