Skip to main content
SpringerLink
Log in

Sulfatide and Na+-K+-ATPase: A Salinity-sensitive Relationship in the Gill Basolateral Membrane of Rainbow Trout

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

We investigated the effect of salinity on the relationship between Na+-K+-ATPase and sulfogalactosyl ceramide (SGC) in the basolateral membrane of rainbow trout (Oncorhynchus mykiss) gill epithelium. SGC has been implicated as a cofactor in Na+-K+-ATPase activity, especially in Na+-K+-ATPase rich tissues. However, whole-tissue studies have questioned this role in the fish gill. We re-examined SGC cofactor function from a gill basolateral membrane perspective. Nine SGC fatty acid species were quantified by tandem mass spectrometry (MS/MS) and related to Na+-K+-ATPase activity in trout acclimated to freshwater or brackish water (20 ppt). While Na+-K+-ATPase activity increased, the total concentration and relative proportion of SGC isoforms remained constant between salinities. However, we noted a negative correlation between SGC concentration and Na+-K+-ATPase activity in fish exposed to brackish water, whereas no correlation existed in fish acclimated to freshwater. Differential Na+-K+-ATPase/SGC sensitivity is discussed in relation to enzyme isoform switching, the SGC cofactor site model and saltwater adaptation.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  • M.B. Abramson R. Katzman R. Curci C.E. Wilson (1967) ArticleTitleThe reactions of sulfatide with metallic cations in aqueous systems Biochemistry 6 295–304 Occurrence Handle10.1021/bi00853a046 Occurrence Handle6030326

    Article  PubMed  Google Scholar 

  • M.B. Abramson R. Katzman (1968) ArticleTitleIonic interaction of sulphatide with choline lipids Science 161 576–577 Occurrence Handle4298707

    PubMed  Google Scholar 

  • P.J. Bentley L. Feeney A.N. Hanson R.N. Mixon (1976) ArticleTitleSulfated glycolipids in ciliary body epithelium Invest. Ophthalmol 15 575–579 Occurrence Handle931709

    PubMed  Google Scholar 

  • A.R. Borgatti A. Paliarani U. Ventrella (1992) ArticleTitleGill (Na+-K+)-ATPase involvement and regulation during Salmonid adaptation to salt water Comp. Biochem. Physiol 102A 637–643 Occurrence Handle10.1016/0300-9629(92)90717-5

    Article  Google Scholar 

  • W.D. Comper T.C. Laurent (1978) ArticleTitlePhysiological function of connective tissue polysaccharides Physiol. Rev. 58 255–315 Occurrence Handle414242

    PubMed  Google Scholar 

  • E.L. Crockett (1999) ArticleTitleLipid restructuring does not contribute to elevated activities of Na+/K+-ATPase in basolateral membranes from the gill of seawater acclimated eel (Anguillia rostrata) J. Exp. Biol. 202 2385–2392 Occurrence Handle10441089

    PubMed  Google Scholar 

  • F.H. Epstein A.I. Katz G.E. Pickford (1967) ArticleTitleSodium- and potassium-activated adenosine triphosphate of gills: role in adaptation of teleosts to salt water Science 156 1245–1247 Occurrence Handle4225898

    PubMed  Google Scholar 

  • L. Feeney R.N. Mixon (1974) ArticleTitleLocalization of 35sulfated macromolecules at the site of active transport in the ciliary processes Invest. Ophthalmol. 13 882 Occurrence Handle4279344

    PubMed  Google Scholar 

  • P. Fredman L. Mattsson K. Andersson P. Davidsson I. Ishizuka S. Jeansson J.E. Mansson L. Svennerholm (1988) ArticleTitleCharacterization of the binding epitope of a monoclonal antibody to sulphatide Biochem. J. 251 17–22 Occurrence Handle2455508

    PubMed  Google Scholar 

  • H. Fujimoto K. Tadano-Aritomi A. Tokumasu K. Ito T. Hikita K. Suzuki I. Ishizuka (2000) ArticleTitleRequirement of seminolipid in spermatogenesis revealed by UDP-galactose: ceramide galactosyltransferase-deficient mice J. Biol. Chem. 275 22623–22626 Occurrence Handle10.1074/jbc.C000200200 Occurrence Handle10801776

    Article  PubMed  Google Scholar 

  • A. Gibbs G.N. Somero (1989) ArticleTitlePressure adaptation of Na+/K+-ATPase in gills of marine teleosts J. Exp. Biol. 143 475–92 Occurrence Handle2543729

    PubMed  Google Scholar 

  • S.M. Goldin S.W. Tong (1974) ArticleTitleReconstitution of active transport catalyzed by the purified sodium and potassium ion-stimulated adenosine triphosphatase from canine renal medulla J. Biol. Chem. 249 5907–5915 Occurrence Handle4278244

    PubMed  Google Scholar 

  • E. Gonzalez F. Zambrano (1983) ArticleTitlePossible role of sulphatide in the K+ activated phosphatase activity Biochim. Biophys. Acta 728 66–72 Occurrence Handle6299339

    PubMed  Google Scholar 

  • Y. Grimm-Jorgensen M.E. Ducor J. Piscatelli (1986) ArticleTitleSurface mucus production in gastropods is dependent on environmental salinity and humidity Comp. Biochem. Physiol 83A 415–419 Occurrence Handle10.1016/0300-9629(86)90125-8

    Article  Google Scholar 

  • C.G. Hansson K-A. Karlsson B.E. Samuelsson (1978) ArticleTitleIdentification of sulphatides in human erythrocyte membrane and their relation to sodium-potassium dependent adenosine triphosphate J. Biochem 83 813–819 Occurrence Handle147867

    PubMed  Google Scholar 

  • C.G. Hansson E. Heilbronn K-A. Karlsson Samuelsson (1979) ArticleTitleThe lipid composition of the electric organ of the ray, Torpedo marmorata, with specific reference to sulfatides and Na+-K+-ATPase J. Lipid Res 20 509–518 Occurrence Handle222858

    PubMed  Google Scholar 

  • L. Ishizuka T. Yamakawa (1985) Glycoglycerolipids H. Wiegandt (Eds) Glycolipids Elsevier Amsterdam 101–196

    Google Scholar 

  • I. Ishizuka M. Suzuki T. Yamakawa (1973) ArticleTitleIsolation and characterization of a novel sulfoglycolipid, ‘seminolipid’, from boar testis and spermatozoa J. Biochem. 73 77–87 Occurrence Handle4690236

    PubMed  Google Scholar 

  • A. Jedlicki F. Zambrano (1985) ArticleTitleRole of sulfatide on phosphoenzyme formation and ouabain binding of the (Na+ + K+) ATPase Arch. Biochem. Biophys. 238 558–564 Occurrence Handle10.1016/0003-9861(85)90200-0 Occurrence Handle2986554

    Article  PubMed  Google Scholar 

  • K. Jüress R. Bastrop (1995) ArticleTitleThe function of mitochondria-rich cells (chloride cells) in teleost gills Rev. Fish Biol. Fish 5 235–255

    Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1968) ArticleTitleSulfatides and sodium ion transport, sphingolipid composition of the rectal gland of spiny dogfish FEBS Lett. 2 4–6 Occurrence Handle10.1016/0014-5793(68)80084-5 Occurrence Handle11946252

    Article  PubMed  Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1969) ArticleTitleSphingolipid composition of the avian salt gland Biochim. Biophys. Acta 176 429–431 Occurrence Handle4237892

    PubMed  Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1971) ArticleTitleLipid pattern and Na+-K+-dependent adenosine triphosphatase activity in the salt gland of duck before and after adaptation to hypertonic saline J. Membrane Biol 5 169–184

    Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1973) ArticleTitleThe sphingolipid composition of bovine kidney cortex, medulla and papilla Biochim. Biophys. Acta 316 317–335 Occurrence Handle4356060

    PubMed  Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1974a) ArticleTitleThe lipid composition of the salt (rectal gland) of spiny dogfish Biochim. Biophys. Acta 337 356–376

    Google Scholar 

  • K.-A. Karlsson B.E. Samuelsson G.O. Steen (1974b) ArticleTitleThe lipid composition and Na+-K+- dependent adenosine-triphosphatase activity of the salt (nasal) gland of eider duck and herring gull Eur. J. Biochem 46 243–258 Occurrence Handle10.1111/j.1432-1033.1974.tb03617.x

    Article  Google Scholar 

  • K.A. Karlsson (1977) Aspects on structure and function of sphingolipids in cell surface membranes I. Abrahamsson S. Pascher (Eds) Structure of Biological Membranes Plenum Press New York 245–274

    Google Scholar 

  • K.J. Karnaky SuffixJr S.A. Ernst C.W. Philpott (1976) ArticleTitleTeleost chloride cell I. Response of pupfish Cyprinodon variegates gill Na,K-ATPase and chloride cell fine structure to various high salinity environments J. Cell. Biol. 70 144–156 Occurrence Handle10.1083/jcb.70.1.144 Occurrence Handle132450

    Article  PubMed  Google Scholar 

  • K.J. Karnaky SuffixJr L.B. Kinter C.E. Kinter W.B. Stirling (1976) ArticleTitleTeleost 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 Occurrence Handle10.1083/jcb.70.1.157 Occurrence Handle132451

    Article  PubMed  Google Scholar 

  • E.L. Kean (1968) ArticleTitleRapid, sensitive spectrophotometric method for quantitative determination of sulfatides J. Lipid. Res. 9 319–327 Occurrence Handle5646183

    PubMed  Google Scholar 

  • Y. Kushi M. Arita L. Ishizuka T. Kasama P. Friedman S. Handa (1996) ArticleTitleSulfatide is expressed in both erythrocytes and platelets of bovine origin Biochim. Biophys. Acta 1304 254–62 Occurrence Handle8982271

    PubMed  Google Scholar 

  • J. Kyte (1971) ArticleTitlePurification of the sodium- and potassium-dependent adenosine triphosphate from canine renal medulla J. Biol. Chem. 246 4157–4165 Occurrence Handle4253595

    PubMed  Google Scholar 

  • M. Levine J. Bain R. Narashimhan B. Palmer A.J. Yates R.K. Murray (1975) ArticleTitleA comparative study of the glycolipids of human, bird, and fish testis and of human sperm Biochim. Biophys. Acta 441 134–145

    Google Scholar 

  • C.A. Lingwood (1986) ArticleTitleColocalization of sulfogalactosylacylalkylglycerol (SGG) and its binding protein during spermatogenesis and sperm mutation. Topology of SGC defines a new testicular germ cell membrane domain Biochem. Cell. Biol. 64 984–992 Occurrence Handle3541976

    PubMed  Google Scholar 

  • S.D. McCormick (1993) ArticleTitleMethods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity Can. J. Fish. Aquat. Sci. 50 656–658

    Google Scholar 

  • H.B. Nader M.L. Medeiros J.F. Pavia V.M.P. Pavia S.M.B. Jeronimo M.P.C. Ferreira C.P. Dietrich (1983) ArticleTitleA correlation between the sulfated glycosaminoglycan concentration and degree of salinity of the “habitat” in fifteen species of the classes Crustacea, Pelecypoda and Gastropoda Comp. Biochem. Physiol. 766 433–436

    Google Scholar 

  • Y. Niimura I. Ishizuka (1990) ArticleTitleAdaptive changes in sulfoglycolipids of kidney cell lines by culture in anisosmotic media Biochim. Biophys. Acta 1052 248–254 Occurrence Handle10.1016/0167-4889(90)90218-3 Occurrence Handle2334735

    Article  PubMed  Google Scholar 

  • Y. Niimura I. Ishizuka (1991) ArticleTitleAccumulation of sulfoglycolipids in hyerosmosis-resistant clones derived from the renal epithelial cell line MDCK (Madin-Darby canine kidney cell) Comp. Biochem. Physiol. 100B 535–541

    Google Scholar 

  • P. Ottolenghi (1975) ArticleTitleThe reversible delipidation of a solubilized sodium-plus-potassium ion-dependent adenosine triphosphate from the salt gland of the spiny dogfish Biochem. J. 151 61–66 Occurrence Handle174557

    PubMed  Google Scholar 

  • A. Pagliarani V. Ventrella R. Ballestrazzi F. Trombetti M. Pirini G. Trigari (1991) ArticleTitleSalinity-dependence of the properties of gill (Na++K+)-ATPase in rainbow trout (Oncorhynchus mykiss) Comp. Biochem. Physiol 100B 229–236

    Google Scholar 

  • S.F. Perry G. Flik (1988) ArticleTitleCharacterization of branchial transepithelial calcium fluxes in freshwater trout, Salmo gairdneri Am. J. Physiol. 254 R491–R498 Occurrence Handle2831744

    PubMed  Google Scholar 

  • J.G. Richards J.W. Semple J.S. Bystriansky P.M. Schulte (2003) ArticleTitleNa+-K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer J. Exp. Biol. 206 4475–4486 Occurrence Handle10.1242/jeb.00701 Occurrence Handle14610032

    Article  PubMed  Google Scholar 

  • R. Sandhoff S.T. Hepbildikler R. Jennemann R. Geyer V. Gieselmann R.L. Proia H. Wiegandt H-J. Gröne (2002) ArticleTitleKidney sulfatides in mouse models of inherited glycosphingolipid disorders J. Biol Chem. 277 20386–20398 Occurrence Handle10.1074/jbc.M110641200 Occurrence Handle11919180

    Article  PubMed  Google Scholar 

  • J.A. Shayman N.S. Radin (1991) ArticleTitleStructure and function of renal glycosphingolipids Am. J. Physiol. 260 F291–302 Occurrence Handle2000947

    PubMed  Google Scholar 

  • T. Umeda K. Egawa Y. Nagai (1976) ArticleTitleEnhancement of sulphatide metabolism in the hypertrophied kidney of C3H/He mouse with reference to (Na+, K+) dependent ATPase Jpn. J. Exp. Med 46 87–94 Occurrence Handle6813

    PubMed  Google Scholar 

  • P. Bijl Particlever der M. Lopes-Cardozo G. Meer Particlevan (1996) ArticleTitleSorting of newly synthesized galactosphingolipids to the two surface domains of epithelial cells J. Cell. Biol. 132 813–820 Occurrence Handle10.1083/jcb.132.5.813 Occurrence Handle8603914

    Article  PubMed  Google Scholar 

  • D. White W. Weerachatyanukul B. Gadella N. Kamolvarin M. Attar N. Tanphaichitr (2000) ArticleTitleRole of sperm sulfogalactosylglycerolipid in mouse sperm-zona pellucida binding Biol. Reprod. 63 147–155 Occurrence Handle10859254

    PubMed  Google Scholar 

  • P.D. Whitfield P.C. Sharp D.W. Johnson P. Nelson P.J. Meikle (2001) ArticleTitleCharacterization of urinary sulfatides in metachromatic leukodystrophy using electrospray ionization-tandem mass spectrometry Mol. Genet. Met. 73 30–37 Occurrence Handle10.1006/mgme.2001.3165

    Article  Google Scholar 

  • B. Zalc J.J. Helwig M.S. Ghandour L. Sarlieve (1978) ArticleTitleSulfatide in the kidney: How is this lipid involved in sodium chloride transport? FEBS Lett 2 92–96 Occurrence Handle10.1016/0014-5793(78)80729-7

    Article  Google Scholar 

  • G. Zwingelstein J. Portoukalian G. Rebel G. Brichon (1980) ArticleTitleGill sulfolipid synthesis and seawater adaptation in euryhaline fish, Anguilla anguilla Comp. Biochem. Physiol 65B 555–558

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Pam Fredman (Sahlgrenska Academy at Goteborg University, Sweden) for kindly donating the Sulph 1 antibody. Logistical support was provided by Marie-Anne Skomorowski, Beth Boyd, Ben Speers-Roesch, Jason Bystriansky and Shannon Costigan. This work was funded by a NSERC Discovery Grant to J.S. Ballantyne and an NSERC PGS A scholarship to Daniel Lingwood.

Author information

Authors and Affiliations

  1. Department of Zoology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    D. Lingwood & J.S. Ballantyne

  2. Genetic-Metabolic Laboratory, Department of Pediatric Laboratory Medicine, The Hospital for Sick Children, Toronto, ON, M5G 1X8, Canada

    L.J. Fisher & J.W. Callahan

  3. Departments of Pediatrics and Biochemistry, University of Toronto, Toronto, ON, M5G 1X8, Canada

    J.W. Callahan

Authors
  1. D. Lingwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L.J. Fisher
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J.W. Callahan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J.S. Ballantyne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Lingwood.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lingwood, D., Fisher, L., Callahan, J. et al. Sulfatide and Na+-K+-ATPase: A Salinity-sensitive Relationship in the Gill Basolateral Membrane of Rainbow Trout. J Membrane Biol 201, 77–84 (2004). https://doi.org/10.1007/s00232-004-0708-3

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-004-0708-3

Keywords

Search

Navigation