The Journal of Membrane Biology

, Volume 82, Issue 1, pp 15–23 | Cite as

Effect of gangliosides on phospholipid bilayers: A study with the lipophilic ions relaxation method

  • Cesare Usai
  • Mauro Robello
  • Franco Gambale
  • Carla Marchetti
Articles

Summary

The presence of monosialoganglioside GM1 in dioleoylphosphatidylcholine black lipid membranes modifies the transport properties of the hydrophobic ion tetraphenylborate and the kinetics of relaxation of this ion after the application of a voltage step. At zero applied voltage, the difference in the relaxation time constants between pure phospholipid and gangliosidephospholipid mixed membranes is large. This difference may possibly rise from changes in the membranes fluidity since it has been found that the two types of membranes do not show appreciable difference in thickness. A uniform distribution of GM1 in the membrane seems to be more probable than the presence of lateral phase separation phenomena. The partition coefficient of tetraphenylborate between the bathing NaCl solution and the membrane appears to depend on the ionic strength, which controls the screening effect of the Na+ ions on the COO charged groups of the sialic acid of the ganglioside polar heads. Effects of dipolar potentials on the partition coefficient can be excluded, being the absorption plane of tetraphenylborate probably located outside the dipolar layer of the membrane.

Key Words

gangliosides lipid bilayer membranes lipophilic ions ion transport 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Andersen, O.S., Feldberg, S., Nakadomari, H., Levy, S., McLaughlin, S. 1978. Electrostatic interactions among hydrophobic ions in lipid bilayer membranes.Biophys. J. 21:35–70PubMedGoogle Scholar
  2. Andersen, O.S., Fuchs, M. 1975. Potential energy barriers to ion transport within lipid bilayers. Studies with tetraphenylborate.Biophys. J. 15:795–930PubMedGoogle Scholar
  3. Bach, D., Chapman, D. 1980. Calorimetric studies of biomembranes and their molecular components.In: Biological Microcalorimetry. A.E. Beezer, editor. pp. 275–309. Academic, LondonGoogle Scholar
  4. Benz, R., Conti, F. 1981. Structure of the squid axon membrane as derived from charge-pulse relaxation studies in the presence of absorbed lipophilic ions.J. Membrane Biol. 59:91–104Google Scholar
  5. Benz, R., Cross, D. 1978. Influence of sterols on ion transport through lipid bilayer membranes.Biochim. Biophys. Acta 506:265–280Google Scholar
  6. Benz, R., Frölich, D., Läuger, P. 1976. Influence of membrane structure on the kinetics of carrier-mediated ion transport through lipid bilayers.Biochim. Biophys. Acta 464:465–481Google Scholar
  7. Benz, R., Gisin, B.F. 1978. Influence of membrane structure on ion transport through lipid bilayer membranes.J. Membrane Biol. 40:293–314Google Scholar
  8. Benz, R., Läuger, P. 1977. Transport kinetics of dipicrylamine through lipid bilayer membranes. Effects of membrane structure.Biochim. Biophys. Acta 468:245–258PubMedGoogle Scholar
  9. Benz, R., Läuger, P., Janko, K. 1976. Transport kinetics of hydrophobic ions in lipid bilayer membranes. Charge pulse relaxation studies.Biochim. Biophys. Acta 455:701–720PubMedGoogle Scholar
  10. Benz, R., Nonner, W. 1981. Structure of the axolemma of frog myelinated nerve: Relaxation experiments with a lipophilic probe ion.J. Membrane Biol. 59:127–134Google Scholar
  11. Bruner, L.J. 1975. The interaction of hydrophobic ions with lipid bilayer membranes.J. Membrane Biol. 22:125–141Google Scholar
  12. Cornell, B.A., Separovic, F. 1983. Membrane thickness and acyl chain length.Biochim. Biophys. Acta 733:189–193PubMedGoogle Scholar
  13. Cuatrecasas, P. 1973a. Interaction ofVibrio cholerae enterotoxin with cell membranes.Biochemistry 12:3547–3557PubMedGoogle Scholar
  14. Cuatrecasas, P. 1973b. Gangliosides and membrane receptors for cholera toxin.Biochemistry 12:3558–3566PubMedGoogle Scholar
  15. DeLevie, R., Seidah, N.G., Larkin, D. 1974. Tetraphenylborate adsorption into an artificial ultrathin membrane.Electroanal. Chem. Interf. Electrochem. 48:153–159Google Scholar
  16. Delmelle, M., Dufrane, S.P., Brasseur, R., Ruysschaert, J.M. 1980. Clustering of gangliosides in phospholipid bilayers.FEBS Lett. 121:11–14PubMedGoogle Scholar
  17. Edelman, G.M. 1976. Surface modulation in cell recognition and cell growth.Science 192:218–226PubMedGoogle Scholar
  18. Fishman, P.H., Brady, R.O. 1975. Modification of membrane glycolipids by oncogenic agents.In: Modification of Lipid Metabolism. E.G. Perkins and L.A. Witting, editors. pp. 105–117. Academic, New YorkGoogle Scholar
  19. Fishman, P.H., Brady, R.O. 1976. Biosynthesis and function of gangliosides.Science 194:906–915PubMedGoogle Scholar
  20. Gaines, G.L. 1966. Insoluble monolayers at liquid-gas interfaces.In: Interscience Monographs on Physical Chemistry. I. Prigogine, editor. J. Wiley, New YorkGoogle Scholar
  21. Gambale, F., Robello, M., Usai, C., Marchetti, C. 1982. Properties of ionic transport through phospholipid-glycolipid artificial bilayers.Biochim. Biophys. Acta 693:165–172PubMedGoogle Scholar
  22. Hakomori, S.I., Jeanloz, R.W. 1970. Glycolipids as membrane antigens.In: Blood and Tissue Antigens. D. Aminof, editor. pp. 149–161. Academic, New YorkGoogle Scholar
  23. Haydon, D.A. 1975. Functions of the lipid in bilayer ion permeability.Ann. N.Y. Acad. Sci. 264:2–16PubMedGoogle Scholar
  24. Haydon, D.A., Hladky, S.B. 1972. Ion transport across thin lipid membranes: A critical discussion of mechanisms in selected systems.Q. Rev. Biophys. 5:187–282PubMedGoogle Scholar
  25. Ketterer, B., Neumcke, B., Läuger, P. 1971. Transport mechanism of hydrophobic ions through lipid bilayer membranes.J. Membrane Biol. 5:225–245Google Scholar
  26. Klenk, E. 1942. Uber die Ganglioside, eine neue gruppe von zuckererhaltigen gehirnlipoiden.Hoppe-Seyler's Z. Physiol. Chem. 273:76–88Google Scholar
  27. Läuger, P., Benz, R., Stark, G., Bamberg, E., Jordan, P.C., Fahr, A., Brock, W. 1981. Relaxation studies of ion transport systems in lipid bilayer membranes.Q. Rev. Biophys. 14:513–598PubMedGoogle Scholar
  28. Läuger, P., Neumcke, B. 1973. Theoretical analysis of ion conductance in lipid bilayer membranes.In: Membranes. A Series of Advances. G. Eisenman, editor. Vol. 2, pp. 1–59. M. Dekker, New YorkGoogle Scholar
  29. LeBlanc, O.H., Jr. 1969. Tetraphenylborate conductance through lipid bilayer membranes.Biochim. Biophys. Acta 193:350–360PubMedGoogle Scholar
  30. Liberman, E.A., Topaly, V.P. 1968. Selective transport of ions through bimolecular phospholipid membranes.Biochim. Biophys. Acta 163:125–136PubMedGoogle Scholar
  31. Maggio, B., Cumar, F.A., Caputto, R. 1978. Surface behaviour of gangliosides and related glycosphingolipids.Biochem. J. 171:559–565PubMedGoogle Scholar
  32. Maggio, B., Cumar, F.A., Caputto, R. 1980. Configuration and interactions of the polar head group in gangliosides.Biochem. J. 189:435–440PubMedGoogle Scholar
  33. McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces.Curr. Top. Membr. Transp. 9:71–144Google Scholar
  34. Mueller, P., Rudin, D.O., Tien, H.T., Wescott, W.C. 1963. Methods for the formation of single bimolecular lipid membranes in aqueous solution.J. Phys. Chem. 67:534–535Google Scholar
  35. Mullin, B.R., Pacuszka, T., Lee, G., Kohn, L.D., Brady, R.O., Fishman, P.H. 1978. Thyroid gangliosides with high affinity for thyrotropin: Potential role in thyroid regulation.Science 199:77–79Google Scholar
  36. Parsegian, A. 1969. Energy of an ion crossing a low dielectric membrane: Solution of four relevant electrostatic problems.Nature (London) 221:844–845Google Scholar
  37. Pickar, A.D., Benz, R. 1978. Transport of oppositely charged lipophilic probe ions in lipid bilayer membranes having various structures.J. Membrane Biol. 44:353–376Google Scholar
  38. Porcellati, G., Ceccarelli B., Tettamanti, R.O., editors. 1976. Ganglioside function. Biochemical and pharmacological implications.Adv. Exp. Med. Biol. Vol. 71. Plenum, New YorkGoogle Scholar
  39. Poss, A., Deleers, M., Ruysschaert, J.M. 1978. Evidence for a specific interaction between GT ganglioside incorporated into bilayer membranes and thyrotropin.FEBS Lett. 86:160–162PubMedGoogle Scholar
  40. Redwood, W.R., Polefka, T.G. 1976. Lectin receptor interaction in liposomes. II. Interaction of wheat germ agglutinin with phosphatidylcholine liposomes containing incorporated monosialoganglioside.Biochim. Biophys. Acta 455:631–643PubMedGoogle Scholar
  41. Sharon, F.J., Grant, C.W.M. 1978. A model for ganglioside behavior in cell membranes.Biochim. Biophys. Acta 507:280–293PubMedGoogle Scholar
  42. Sinha, B.A., Smejtek, P. 1983. Effect of 3-phenylindole on lipophilic ion and carrier-mediated ion transport across bilayer lipid membranes.J. Membrane Biol. 71:119–130Google Scholar
  43. Szabo, G. 1976. The influence of dipole potentials on the magnitude and the kinetics of ion transport in lipid bilayer membranes.In: Extreme Environment: Mechanism of Microbial Adaptation. M.R. Heinrich, editor. pp. 321–348. Academic, New YorkGoogle Scholar
  44. Tumanova, R.Y., Badjinyan, S.A., Nalbandyan, R.M. 1978. Resistance of planar bilayers of gangliosides.Biochem. Biophys. Res. Commun. 84:520–526PubMedGoogle Scholar
  45. Uchida, T., Nagai, Y., Kawasaki, Y., Wakayama, N. 1981. Fluorospectroscopic studies of various ganglioside and ganglioside-lecithin dispersions. Steady-state and time-resolved fluorescence measurements with 1,6-diphenyl-1,3,5-hexatriene.Biochemistry 20:162–169PubMedGoogle Scholar
  46. Usai, C., Marchetti, C., Gambale, F., Robello, M., Gorio, A. 1983. Capacitance-voltage relationship in phospholipid bilayers containing gangliosides.FEBS Lett. 153:315–319PubMedGoogle Scholar
  47. Van Heyningen, W.E. 1974. Gangliosides as membrane receptors for tetanus toxin, cholera toxin and serotonin.Nature (London) 249:415–417Google Scholar
  48. Wiegandt, H. 1975. Glycoproteins and glycolipids of the cell surface.In: Biomembranes, Lipids, Proteins and Receptors. R.M. Burton and F.S. Esters, editors. pp. 51–64. NATO Advanced Study Institute, Bi-Science, Webster Groves, Mo.Google Scholar

Copyright information

© Springer-Verlag 1984

Authors and Affiliations

  • Cesare Usai
    • 1
  • Mauro Robello
    • 2
  • Franco Gambale
    • 1
  • Carla Marchetti
    • 3
  1. 1.Istituto di Cibernetica e BiofisicaConsiglio Nazionale delle RicercheGenovaItaly
  2. 2.Istituto di Scienze FisicheUniversità di GenovaGenovaItaly
  3. 3.FIDIA Research LaboratoriesPadovaItaly

Personalised recommendations