Plasma Membrane Potential of Animal Cells Generated by Ion Pumping, Not by Ion Gradients

  • C. L. Bashford
  • C. A. Pasternak

Abstract

The plasma membrane potential of animal cells is generally thought to be generated predominantly by the diffusion of K+ out of cells (Williams, 1970), with only very minor contributions from the diffusion of other ions or from an electrogenic Na+ pump (Thomas, 1972; Lew et al., 1979). The experiments to be described show that this view is no longer universally applicable, and that plasma membrane potential of at least two cell types, — a mouse tumour cell and human neutrophils, — arises predominantly from electrogenic pumping of Na+ and, to a lesser extent, of H+. In such cells electrical and osmotic stability are preserved by the operation of anion leak and electroneutral ion transport pathways (Bashford & Pasternak, 1984, 1985a,b).

Keywords

Permeability Lactate Carbonyl Iodide Cyanide 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bashford, C.L., Casey, R.P., Radda, G.K. and Ritchie, G.A., 1976, Energy-coupling in adrenal chromaffin granules, Neuroscience 1: 399.CrossRefGoogle Scholar
  2. Bashford, C.L., Chance, B. and Prince, R.C., 1979a, Oxonol dyes as monitors of membrane potential. Their behaviour in photosynthetic bacteria, Biochim.Biophys.Acta. 545: 46.CrossRefGoogle Scholar
  3. Bashford, C.L., Chance, B., Smith, J.C. and Yoshida, T., 1979b, The behaviour of oxonol dyes in phospholipid dispersions, Biophys.J., 25: 63.CrossRefGoogle Scholar
  4. Bashford, C.L. and Pasternak, C.A., 1984, Plasma membrane potential of Lettre cells does not depend on cation gradients but on pumps, J.Membr.Biol., 79: 275.CrossRefGoogle Scholar
  5. Bashford, C.L. and Pasternak, C.A., 1985a, Generation of plasma membrane potential by the Na+-pump coupled to proton extrusion, Eur.Biophys.J., in press.Google Scholar
  6. Bashford, C.L. and Pasternak, C.A., 1985b, Plasma membrane potential of neutrophils generated by the Na’ pump, Biochim.Biophys.Acta, in press.Google Scholar
  7. Bashford, C.L., Alder, G.M., Gray, M.A., Micklem, K.J., Taylor, C.C., Turek, P.J. and Pasternak, C.A., 1985, Oxonol dyes as monitors of membrane potential: The effect of viruses and toxins on the plasma membrane potential of animal cells in monolayer culture and in suspension, J.Cell.Physiol., 123: 326.CrossRefGoogle Scholar
  8. Galloway, C. J., Dean, G.E., Marsh, M., Rudnick, G. and Mellman, I., 1983, Acidification of macrophages and fibroblast endocytic vesicles in vitro, Proc.Natl.Acad.Sci.USA, 80: 33–34.CrossRefGoogle Scholar
  9. Harris, E.J. and Pressman, B.C., 1967, Obligate cation exchanges in red cells, Nature 216: 918.CrossRefGoogle Scholar
  10. Henderson, P.J.F., McGivan, J.D. and Chappell, J.B., 1969, The action of certain antibiotics on mitochondria’, erythrocyte and artificial phospholipid membranes. The role of induced proton permeability, Biochem.J., 111: 521.Google Scholar
  11. Hoffman, J.F. and Laris, P.C., 1974, Determination of membrane potentials in human and Amphiuma red blood cells by means of a fluorescence probe, J.Physiol. 239: 519.Google Scholar
  12. Hopkins, C.R., 1984, The importance of the endosome in intracellular traffic, Nature 304: 684.CrossRefGoogle Scholar
  13. Impraim, C.C., Foster, K.A., Micklem, K.J. and Pasternak, C.A., 1980, Nature of virally mediated changes in membrane permeability to small molecules, Biochem.J., 186: 847.Google Scholar
  14. Lew, V.L., Ferreira, H.G. and Moura, T., 1979, The behaviour of transporting epithelial cells. I. Computer analysis of a basic model. Proc.R.Soc.Lond.B., 206: 53.CrossRefGoogle Scholar
  15. Linnett, P.E. and Beechey, R.B., 1979, Inhibitors of the ATP synthetase system, Meth.Enzymol. 55: 472.CrossRefGoogle Scholar
  16. Mehta, S., Bashford, C.L., Knox, P. and Pasternak, C.A., 1985, Chemiluminescence in neutrophils and Lettre cells induced by myxoviruses, Biochem.J. 227: 99.Google Scholar
  17. Segal, A.W., Dorling, J. and Coade, S., 1980, Kinetics of fusion of the cytoplasmic granules with phagocytic vacuoles in human polymorphonuclear leukocytes, J.Cell.Biol., 85: 42.CrossRefGoogle Scholar
  18. Smith, J.C., Russ, P., Cooperman, B.S. and Chance, B., 1976, Synthesis, structure determination, spectral properties and energy-linked spectral responses of the extrinsic probe oxonol-V in membranes, Biochemistry, 15: 5094.CrossRefGoogle Scholar
  19. Tatham, P.E.R., Delves, P.J., Shen, L. and Roitt, I.M., 1980, Chemotactic factor-induced membrane potential changes in rabbit neutrophils monitored by the fluorescent dye 3,3’-dipropylthiadicarbocyanine iodide, Biochim.Biophys.Acta, 602: 285.CrossRefGoogle Scholar
  20. Thomas, R.C., 1972, Electrogenic sodium pump in nerve and muscle cells, Physiol.Rev., 52: 563.Google Scholar
  21. Williams, J.A., 1970, Origin of transmembrane potentials in non-excitable cells, J.theor.Biol., 28: 287.CrossRefGoogle Scholar
  22. Yamoshiro, D.J., Fluss, S.R. and Maxfield, F.R., 1983, Acidification of endocytic vesicles by an ATP-dependent pump, J.Cell Biol., 97: 929.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1986

Authors and Affiliations

  • C. L. Bashford
    • 1
  • C. A. Pasternak
    • 1
  1. 1.Department of BiochemistrySt George’s Hospital Medical SchoolCranmer Terrace, LondonUK

Personalised recommendations