Skip to main content
Log in

Sodium- and potassium-activated adenosine triphosphatase in the excretory organs of Sepia officinalis (Cephalopoda)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Sodium- and potassium-activated ATPase (Na+−K+-ATPase) has been demonstrated in excretory organs of Sepia officinalis, using a cytochemical procedure. In the renal appendages, both epithelia of the pancreatic appendages, the folded epithelium of the branchial heart appendage and the transport-active epithelium of the gill, the enzyme is localized exclusively in the basolateral cell membranes, i.e., the membranes of the basal labyrinth and the lateral plasma membranes. In addition, Na+−K+-ATPase is also located in the sarcolemma of the muscle fibres of the branchial heart. Distribution and localization of the enzyme is further substantiated by [3H]-ouabain autoradiography. The possible involvement of Na+−K+-ATPase in the excretion of ammonia and in ionic regulation in dibranchiate cephalopods is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Akera, T. and T. M. Brody: The role of Na, K-ATPase in the intotropic action of digitalis. Pharmacol. Rev. 29, 187–220 (1978)

    Google Scholar 

  • Amlacher, E.: Autoradiographie in Histologie und Cytologie. 48 pp. Stuttgart: Gustav Fisher 1974

    Google Scholar 

  • Berridge, M. J. and J. L. Oschman: Transporting epithelia, pp 1–72, New York, London: Academic Press 1972

    Google Scholar 

  • Bidder, A. M.: Feeding and digestion in cephalopods. In: Physiology of mollusca, Vol 2. pp 97–124, Ed. by K. M. Wilbur and C. M. Yonge. New York, London: Academic Press 1966

    Google Scholar 

  • Blaustein, M. P.: The interrelationship between sodium and calcium fluxes across cell membranes. Rev. Physiol. Biochem. Pharmacol. 70, 33–82 (1974)

    PubMed  Google Scholar 

  • Boucaud-Camou, E.: Etude histologique et histochimique de l'appareil digestif de Sepiola atlantica D'Orbigny et Sepia officinalis L. Bull. Soc. Linnéenne de Normandie 10 Serie, Vol 9, 220–243 (1968)

    Google Scholar 

  • Boucaud-Camou, E.: Etude infrastructurale du pancréas de Sepia officinalis. Bull. Soc. Zool. France 97, 197–203 (1972)

    Google Scholar 

  • Boucaud-Camou, E.: Localisation d'activités enzymatiques impliquées dans Ia digestion chez Sepia officinalis L. Arch. Zool. Exp. Gen. 115, 5–27 (1974)

    Google Scholar 

  • Boucaud-Camou, E. et E. Pequignat: Etude experimentale de l'absorption digestive chez Sepia officinalis L. Forma et Functio Vol 6, 93–112 (1973)

    Google Scholar 

  • Castaldi, L. e Z. Musio: Osservazioni sul cosi detto pancreas di Sepia officinalis. Mon. Zool. Ital. 39, 137–150 (1928)

    Google Scholar 

  • Dahl, J. C. and L. E. Hokin: The sodium-potassium adenosine triphosphatase. Ann. Rev. Biochem. 43, 327–356 (1974)

    Article  PubMed  Google Scholar 

  • DiBona, D. R. and J. W. Mills. Distribution of Na+-pump sites in transporting epithelia. Fedn. Proc. 38, 134–143 (1979)

    Google Scholar 

  • Donaubauer, H. H.: Adenosine triphosphatase localization in the branchial heart appendage of Sepia officinalis L. (Cephalopoda). Histochem. 65, 17–30 (1979)

    Google Scholar 

  • Donaubauer, H. H.: Adenosine triphosphatase localization in the branchial heart of Sepia officinalis L. (Cephalopoda). Histochem. 69, 27–37 (1980)

    Google Scholar 

  • Donaubauer, H. H. and R. Schipp: Localization of enzyme activities in the pancreatic appendages of Sepia officinalis L. (Cephalopoda). Histochem. 59, 29–44 (1978)

    Google Scholar 

  • Ellis, R. A. and C. C. Goertemiller: Cytological effects of salt stress and localization of transport adenosine triphosphatase in the lateral nasal gland of the desert iguana Dipsosaurus dorsalis. Anat. Rec. 180, 285–298 (1974)

    PubMed  Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • 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)

    PubMed  Google Scholar 

  • Ernst, S. A.: Transport ATPase cytochemistry: Ultrastructural localization of potassium-dependent and potassium-independent phosphatase activities in rat kidney cortex. J. Cell Biol. 66, 586–608 (1975)

    Article  PubMed  Google Scholar 

  • Ernst, S. A. and J. W. Mills: 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 (1977)

    PubMed  Google Scholar 

  • Farquhar, M. G. and G. E. Palade: Adenosine triphosphatase localization in amphibian epidermis. J. Cell Biol. 30, 359–379 (1966)

    Article  PubMed  Google Scholar 

  • Glynn, I. M. and S. J. D. Karlish: The sodium pump. Ann. Rev. Physiol. 37, 13–55 (1975)

    Article  Google Scholar 

  • Goertemiller, C. C. and R. A. Ellis: Localization of ouabain-sensitive, potassium-dependent nitrophenyl phosphatase in the rectal gland of the spiny dogfish, Squalus acanthias. Cell Tiss. Res. 175, 101–112 (1976)

    Google Scholar 

  • Harrison, F. M. and A. W. Martin: Excretion in the cephalopod Octopus dofleini. J. exp. Biol. 42, 71–98 (1965)

    PubMed  Google Scholar 

  • Hobbs, A. S. and P. DeWeer: Transport adenosine triphosphatase: Absence of ATP: p-nitrophenol phosphotransferase activity. Arch. Biochem. Biophys. 173, 386–388 (1976)

    PubMed  Google Scholar 

  • Höfer, M.: Transport durch biologische Membranen. Das Konzept der Trägerkatalyse. pp 46–51. Weinheim, New York: Verlag Chemie 1977

    Google Scholar 

  • Hokin, L. E.: The molecular machine for driving the coupled transports of Na+ and K+ is a Na+−K+-activated ATPase. TIBS 1, 233–237 (1976)

    Google Scholar 

  • Hossler, F. E., J. R. Ruby and T. D. Mcllwain: The gill arch of the mullet (Mugil cephalus) II. Modification in surface ultrastructure and Na+−K+-ATPase content during adaption to various salinities. J. exp. Zool. 208, 399–406 (1979)

    Google Scholar 

  • Johnson, M. P. and F. B. P. Wooding: Adenosine triphosphatase distribution in mammary tissue. Histochem. J. 10, 171–183 (1978)

    PubMed  Google Scholar 

  • Kaplan, J. G.: Membrane cation transport and the control of proliferation of mammalian cells. Ann. Rev. Physiol. 40, 19–41 (1978)

    Article  Google Scholar 

  • Karnaky, K. J., S. A. Ernst and C. W. Philpott: Teleost chloride cell. I. Response of pupfish Cyprinodon varegatus gill Na+−K+-ATPase and chloride cell fine structure to various high salinity environments. J. Cell Biol. 70, 144–156 (1976)

    Article  PubMed  Google Scholar 

  • Koefoed-Johnson, V. and H. H. Ussing: The nature of the frog skin potential. Acta Physiol. Scand. 42, 298–308 (1958)

    PubMed  Google Scholar 

  • Kyte, J.: Immunoferritin determination of the distribution of Na+−K+-ATPase over the plasma membranes of renal convoluted tubules. I. Distal segment. J. Cell Biol. 68, 287–303 (1976a)

    Article  PubMed  Google Scholar 

  • Kyte, J.: Immunoferritin determination of the distribution of Na+−K+-ATPase over the plasma membranes of renal convoluted tubules. II. Proximal segment. J. Cell Biol. 68, 304–318 (1976b)

    Article  PubMed  Google Scholar 

  • Lindenmayer, G. E. and A. Schwartz: A kinetic characterization on Na+−K+-ATPase and its potential role as a link between extracellular and intracellular events: Hypothesis for digitalis induced inotropism. J. Mol Cell. Cardiol. 7, 591–612 (1975)

    Article  PubMed  Google Scholar 

  • Mangum, C. P., S. U. Silverthorn, J. L. Harris, D. W. Towle and A. R. Krall: The relationship between blood pH, ammonia excretion and adaption to low salinity in the blue crab, Callinectes sapidus (1). J. exp. Zool. 195, 129–136 (1976)

    Google Scholar 

  • Mangum, C. P., J. A. Dykens, R. P. Henry and G. Polites: The excretion of NH+ and its ouabain-sensitivity in aquatic annelids and molluscs. J. exp. Zool. 203, 151–159 (1978)

    Google Scholar 

  • Martin, A. W. and F. A. Aldrich: Comparison of hearts and branchial heart appendages in some cephalopods. Canad. J. Zool. 48, 751–756 (1970)

    Google Scholar 

  • Martin, A. W.: Physiology of the excretory organs of cephalopods. In: Excretion. pp 112–123. Ed. by A. Wessing. Stuttgart: Gustav Fischer 1975

    Google Scholar 

  • Mills, J. W. and S. A. Ernst: Localization of sodium pump sites in frog urinary bladder. Biochim. Biophys. Acta 375, 268–273 (1975)

    PubMed  Google Scholar 

  • Mills, J. W. and D. R. DiBona: Localization of Na+ pump sites in frog skin. J. Cell Biol. 73, 88–110 (1977)

    Article  PubMed  Google Scholar 

  • Philpott, C. W. and D. E. Copeland: Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18, 389–404 (1963)

    Article  PubMed  Google Scholar 

  • Portius, H. J. and K. R. H. Repke: Eigenschaften und Funktion des Na+, K+-aktivierten Mg2+-abhängigen Adenosintriphosphat Phosphohydrolase-Systems des Herzmuskels. Acta Biol. Med. Ger. 19, 907–938 (1967)

    Google Scholar 

  • Potts, W. T. W. and A. W. Martin: The process of ammonia excretion in an Octopus. Proc. Int. Congr. Zool. 1, 78 (1963)

    Google Scholar 

  • Potts, W. T. W.: Ammonia excretion in Octopus dofleini. Comp. Biochem. Physiol. 14, 339–355 (1965)

    Article  PubMed  Google Scholar 

  • Potts, W. T. W.: Excretion in the molluscs. Biol. Rev. 42, 1–41 (1967)

    Article  Google Scholar 

  • Potts, W. T. W.: Aspects of excretion in the molluses. Symp. Zool. Soc. London 22, 187–192 (1968)

    Google Scholar 

  • Potts, W. T. W. and M. Todd: Kidney function in the Octopus. Comp. Biochem. Physiol. 16, 479–489 (1965)

    Article  PubMed  Google Scholar 

  • Robertson, J. D.: Further studies on ionic regulation in marine invertebrates. J. exp. Biol. 30: 277–296 (1953)

    Google Scholar 

  • Russo, J. and P. Wells: Ultrastructural localization of ATPase activity in resting mammary gland. J. Histochem. Cytochem. 25, 135–148 (1977)

    PubMed  Google Scholar 

  • Schip, R. and F. Hevert: Ultrafiltration in the branchial heart appendage of dibranchiate cephalopods: Comparative ultrastructural and physiological study. J. exp. Biol. (In press)

  • Schipp, R. and A. Schäfer: Die Besonderheiten der Feinstruktur von Kiemenherz und Kiemengefäßen von Cephalopoden. Verh. Dtsch. Zool. Ges. Innsbruck, 1968 Zool. Anz. 32, 113–123 (1969a)

    Google Scholar 

  • Schipp, R. und A. Schäfer: Vergleichende elektronenmikroskopische Untersuchungen an den zentralen Herzorganen von Cephalopoden (Sepia officinalis). Feinstruktur und Funktion der Kiemenherzen. Z. Zellforsch. 101, 367–379 (1969b)

    PubMed  Google Scholar 

  • Schipp, R., P. Höhn und A. Schäfer: Elektronenmikroskopische und histochemische Untersuchungen zur Funktion des Kiemenherzanhangs (Pericardialdrüse) von Sepia officinalis. Z. Zellforsch. 117, 252–274 (1971)

    PubMed  Google Scholar 

  • Schipp, R. and S. von Boletzky: Morphology and function of the excretory organs in dibranchiate cephalopods. Fortschr. Zool. 23, 89–110 (1975)

    Google Scholar 

  • Schipp, R., S. von Boletzky and G. Doell: Ultrastructural and cytochemical investigations on the renal appendages and their concrements in dibranchiate cephalopods (Mollusca, Cephalopoda) Z. Morph. Tiere 81, 279–304 (1975)

    Article  Google Scholar 

  • Schipp, R. and S. von Boletzky: The pancreatic appendages of dibranchiate cephalopods. I. The fine structure of the pancreas in Sepioidea. Zoomorph. 86, 81–98 (1976)

    Google Scholar 

  • Schipp, R., S. A. Mollenhauer and S. von Boletzky: Electron microscopical and histochemical studies of differentiation and function of the cephalopod gill (Sepia officinalis L.). Zoomorph. 93, 193–207 (1979)

    Google Scholar 

  • Schoffeniels, E. and R. Gilles: Ionoregulation and osmoregulation in mollusca. In: Chemical zoology. Vol VII, Mollusca. pp 393–420 Ed. by M. Florkin and T. Scheer, New York, London: Academic Press 1972

    Google Scholar 

  • Schwartz, A., G. E. Lindenmayer and J. C. Allen: The sodiumpotassium adenosine triphosphatase: Pharmacological, physiological and biochemical aspects. Pharmacol. Rev. 27, 3–134 (1975)

    PubMed  Google Scholar 

  • Silva, P., J. Stoff, M. Field, L. Fine, J. N. Forrest and F. H. Epstein: Mechanism of active chloride secretion by shark rectal gland: Role of Na+−K+-ATPase in chloride transport. Am. J. Physiol. 233, F298-F306 (1977)

    PubMed  Google Scholar 

  • Skou, J. C.: The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 23, 394–401 (1957)

    Article  PubMed  Google Scholar 

  • Stirling, C. E.: Radioautographic localization of sodium pump sites in rabbit intestine. J. Cell Biol. 53, 704–714 (1972)

    Article  PubMed  Google Scholar 

  • Thompson, I. G. and F. B. M. Cowan: Localization of K+-stimulated p-NPPase in the lachrymal “salt” gland of Malaclemys, using cytochemical and autoradiographical techniques. Cell Tiss. Res. 174, 417–426 (1976)

    Google Scholar 

  • Tiedemann, K. and J. Schlüns: Histochemical localization of Mg−Na−K-ATPase in different stages of the sheep mesonephros. Histochem. 45, 331–340 (1975)

    Google Scholar 

  • Towle, D. W., G. E. Palmer and J. L. Harris: Role of gill Na+−K+-dependent ATPase in acclimation of blue crabs (Callinectes sapidus) to low salinity. J. exp. Zool. 196, 315–322 (1976)

    Google Scholar 

  • Vigelius, W. J.: Über das Exkretionssystem der Cephalopoden. Niederl. Arch. Zool. 5, 115–184 (1880a)

    Google Scholar 

  • Vigelius, W. J.: Vergleichend-anatomische Untersuchungen über das sogenannte Pankreas der Cephalopoden. Natk. Verh. Koninkl. Akad. Deel XXII, 1–30 (1880b)

    Google Scholar 

  • Widdcombe, J. H., C. B. Basbaum and Y. J. Yee: Localization of Na+-pumps in the tracheal epithelium of the dog. J. Cell Biol. 82, 380–390 (1979)

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by O. Kinne, Hamburg

This study was supported by the “Deutsche Forschungsgemeinschaft” and is part of a doctoral dissertation

Rights and permissions

Reprints and permissions

About this article

Cite this article

Donaubauer, H.H. Sodium- and potassium-activated adenosine triphosphatase in the excretory organs of Sepia officinalis (Cephalopoda). Mar. Biol. 63, 143–150 (1981). https://doi.org/10.1007/BF00406822

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00406822

Keywords

Navigation