Skip to main content

Ultrastructural Localization of Na++K+-ATPase in Specialized Membranes of Salt Transporting Cells in Marine Vertebrates

  • Chapter
Osmoregulation in Estuarine and Marine Animals

Part of the book series: Lecture Notes on Coastal and Estuarine Studies ((COASTAL,volume 9))

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.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bulger RE (1963) Fine structure of the rectal (salt-secreting) gland of the spiny dogfish Squalus acanthias. Anat. Rec. 147: 95–127.

    Article  PubMed  CAS  Google Scholar 

  • Burger JW and Hess WN (1960) Function of the rectal gland in the spiny dogfish. Science 131: 670–671.

    Article  PubMed  CAS  Google Scholar 

  • Dahl JL and Hokin LE (1974) The sodium-potassium adenosinetriphosphatase. Ann. Rev. Biochem. 43: 327–356.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ellis RA, Goertemiller CC Jr, and Stetson DL (1977) Significance of extensive ‘leaky’ cell junctions in the avian salt gland. Nature 268: 555–556.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ernst SA and Hootman SR (1981) Microscopical methods for the localization of Na+, K+-ATPase. Histochem. J. 13: 397–418.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Ernst SA and Schreiber JH (1981) Ultrastructural localization of Na+, K-ATPase in rat and rabbit kidney medulla. J. Cell Biol. 91: 803–813.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Foskett JK and Scheffey C (1982) The chloride cell: definitive identification as the salt-secretory cell in teleosts. Science 215: 164–166.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hootman SR and Ernst SA (1980) Dissociation of avian salt gland: separation procedures and characterization of dissociated cells. Am. J. Physiol. 238: C184–C195.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Hootman SR and Philpott CW (1978) Rapid isolation of chloride cells from pinfish gills. Anat. Rec. 190: 687–702.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Hootman SR and Philpott CW (1980) Accessory cells in teleost branchial epithelium. Am. J. Physiol. 238: R199–R206.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Keys AB (1931) Chloride and water secretion and absorption by the gills of the eel. Z. Vgl. Physiol. 15: 364–388.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Philpott CW and Copeland DE (1963) Fine structure of chloride cells from three species of Fundulus. J. Cell Biol. 18: 389–404.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Ritch R and Philpott CW (1969) Repeating particles associated with an electrolyte-transporting membrane. Exp. Cell Res. 55: 17–24.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Stirling CE (1976) High resolution autoradiography of 3H-ouabain binding in salt transporting epithelia. J. Microscopy 106: 145–157.

    Article  CAS  Google Scholar 

Download references

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1984 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

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

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-45574-2_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-540-13353-7

  • Online ISBN: 978-3-642-45574-2

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics