Skip to main content
SpringerLink
Log in

Theory of cation-phospholipid-induced shape changes in a lipid bilayer couple

  • Published:
Bulletin of Mathematical Biology Aims and scope Submit manuscript

Abstract

A quantitative model of ion binding and molecular interactions in the lipid bilayer membrane is proposed and found to be useful in examining the factors underlying such membrane characteristics as shape, sidedness, stability and vesicle size at various cation concentrations. The lipid membrane behaves as a bilayer couple whose preferential radius of curvature depends on the expansion or contraction of one monolayer relative to the other. It is proposed that molecular packing may be altered by electrostatic repulsion of adjacent like-charged phospholipid headgroups, or by bringing two headgroups closer together by divalent cation crossbridging. The surface concentrations of each type of cation-phospholipid complex can be described by simple binding equilibria and the Gouy-Chapman-Stern formulation for the surface potential in a diffuse double layer. The asymmetric distribution of acidic phospholipids in most biological membranes can account for the differential effects of identical ionic environments on either side of the bilayer. The fraction of vesicle material which tends to have a right-side-out orientation may be approximated by a normal distribution about the mean curvature. The theory generates vesicle sidedness distributions that, when fitted to experimental results from human erythrocyte membranes, provide an alternative method of estimating intrinsic cationphospholipid dissociation constants and other molecular parameters of the bilayer. The results also corroborate earlier suggestions that the Gouy-Chapman theory tends to overestimate free counter-ion concentrations at the surface under large surface potentials.

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

Similar content being viewed by others

Literature

  • Babcock, K. L. 1963. “Theory of Chemical Properties of Soil Colloidal Systems at Equilibrium.”Hilgardia,34, 417–542.

    Google Scholar 

  • Barlow, Jr., C.A. 1970. “The Electrical Double Layer.” InPhysical Chemistry: An Advanced Treatise. (Eds. H. Eyring, D. Henderson and W. Jost), Vol. 9A, pp. 167–246. New York: Academic Press.

    Google Scholar 

  • Bockris, J. O’M. and A. K. N. Reddy. 1970.Modern Electrochemistry. Vol. 2, p. 722–728. New York: Plenum Press.

    Google Scholar 

  • Bolt, G. H. 1955. “Analysis of the Validity of the Guoy-Chapman Theory of the Electrical Double Layer.”J. Colloid Sci.,10, 206–208.

    Article  Google Scholar 

  • Carvalho, A. P., H. Sanui and N. Pace. 1963. “Calcium and Magnesium Binding Properties of Cell Membrane Materials.”J. Cell. Comp. Physiol.,62, 311–317.

    Article  Google Scholar 

  • Chrzeszczyk, A., A. Wishnia and C. S. Springer. 1977. “The Intrinsic Structural Asymmetry of Highly Curved Phospholipid Bilayer Membranes.”Biochim. Biophys. Acta,470, 161–169.

    Article  Google Scholar 

  • Demel, R. A., W. S. M. G. van Kessel, R. F. A. Zwaal, B. Roelofsen and L. L. M. van Deenen. 1975. “Relationship Between Various Phospholipase Actions on Human Red Cell Membranes and the Interfacial Phospholipid Pressure in Monolayers.”Biochim. Biophys. Acta,406, 97–107.

    Article  Google Scholar 

  • Fisher, K. A. 1976. “Analysis of Membranes Halves: Cholesterol.”Proc. nat. Acad. Sci. U.S.A.,73, 173–177.

    Article  Google Scholar 

  • Gent, W. L. G., J. R. Trounce and M. Walser. 1964. “The Binding of Calcium Ions by the Human Erythrocyte Membrane.”Archs. biochem. Biophys.,105, 582–589.

    Article  Google Scholar 

  • Glaser, R., H. Wolf and S. Blottner. 1974. “The Behavior of Univalent Ions in the Membrane-Near Space of Human Erythrocytes.”Bioelectrochem. Bioenerg.,1, 343–349.

    Article  Google Scholar 

  • Gordesky, S. E. and G. V. Marinetti. 1973. “The Asymmetric Arrangement of Phospholipids in the Human Erythrocyte Membrane.”Biochem. biophys. Res. Commun.,50, 1027–1031.

    Article  Google Scholar 

  • Gur, Y., I. Ravina and A. J. Babchin. 1978. “On the Electrical Double Layer Theory.”J. Colloid Interface Sci.,64, 333–341.

    Article  Google Scholar 

  • Hall, J. E. and S. A. Simon. 1976. “A Simple Model for Calcium Induced Exocytosis.”Biochim. biophys. Acta,536, 613–616.

    Google Scholar 

  • Hauser, H., A. Darke and M. C. Phillips. 1976. “Ion-Binding to Phospholipids: Interaction of Calcium With Phosphatidylserine.”Eur. J. Biochem.,62, 335–344.

    Article  Google Scholar 

  • Haydon, D. A. 1964. “The Electrical Double Layer and Electrokinetic Phenomena.” InRecent Progress in Surface Science (Eds. J. F. Danielli, K. G. A. Pankhurst and A. C. Riddiford). Vol. 1, pp. 94–158. New York: Academic Press.

    Google Scholar 

  • Hendrickson, H. S. and J. G. Fullington. 1965. “Stabilities of Metal Complexes of Phospholipids: Ca(II), Mg(II) and Ni(II) Complexes of Phosphatidylserine and Triphosphoinositide.”Biochemistry,4, 1599–1605.

    Article  Google Scholar 

  • Huang, C. and J. P. Charlton. 1971. “Studies on Phosphatidylcholine Vesicles. Determination of Partial Specific Volumes by Sedimentation Velocity Method.”J. biol. Chem.,246, 2555–2560.

    Google Scholar 

  • — and J. T. Mason. 1978. “Geometric Packing Constraints in Egg Phosphatidylcholine Vesicles.”Proc. nat. Acad. Sci. U.S.A.,75, 308–310.

    Article  Google Scholar 

  • Johnson, R. M. and J. Robinson. 1976. “Morphological Changes in Asymmetric Erythrocyte Membranes Induced by Electrolytes.”Biochem. biophys. Res. Commun.,70, 925–931.

    Article  Google Scholar 

  • Joos, R. W. and C. W. Carr. 1967. “The Binding of Calcium Mixtures of Phospholipids.”Proc. soc. exp. biol. Med.,124, 1268–1272.

    Google Scholar 

  • Kwant, W. O. and P. Seeman. 1969. “The Displacement of Membrane Calcium by a Local Anesthetic (Chlorpromazine)”Biochim. biophys. Acta,193, 338–349.

    Article  Google Scholar 

  • Lecuyer, H. and D. G. Dervichian. 1969. “Structure of Aqueous Mixtures of Lecithin and Cholesterol.”J. mol. Biol.,45, 39–57.

    Article  Google Scholar 

  • Lin, G. S. B. and R. I. Macey. 1978. “Shape and Stability Changes in Human Erythrocyte Membranes Induced by Metal Cation.”Biochim. biophys. Acta,512, 270–283.

    Article  Google Scholar 

  • Ohki, S. 1970. “Properties of Lipid Bilayer Membranes. Membrane Thickness.”J. Theor. Biol.,26, 277–287.

    Article  Google Scholar 

  • Papahadjopoulos, D. 1968. “Surface Properties of Acidic Phospholipids: Interaction of Monolayer and Hydrated Liquid Crystals with Uni- and Bivalent Metal Ions.”Biochim. biophys. Acta,163, 240–264.

    Article  Google Scholar 

  • Poznansky, M. and Y. Lange. 1976. “Translayer Movement of Cholesterol in Dipalmitoyllecithin-cholesterol Vesicles.”Nature,259, 420–421.

    Article  Google Scholar 

  • Puskin, J. S. 1977. “Divalent Cation Binding to Phospholipids: An EPR Study.”J. Membr. Biol.,35, 39–55.

    Article  Google Scholar 

  • Rojas, E. and J. M. Tobias. 1965. “Membrane Model: Association of Inorganic Cations with Phospholipid Monolayers.”Biochim. biophys. Acta,94, 394–404.

    Google Scholar 

  • Rothman, J. E. and E. A. Dawidowicz. 1975. “Asymmetric Exchange of Vesicle Phospholipids Catalyzed by the Phosphatidylcholine Exchange Protein. Measurement of Inside-Outside Transitions.”Biochemistry,14, 2809–2816.

    Article  Google Scholar 

  • Rouser, G., G. K. Nelson, S. Fleischer and G. Simon. 1968. “Lipid Composition of Animal Cell Membranes, Organelles and Organs.” InBiological Membranes: Physical Fact and Function. (Ed. D. Chapman), pp. 5–69. London: Academic Press.

    Google Scholar 

  • Sanui, H., A. P. Carvalho and N. Pace. 1962. “Relationship of Hydrogen Ion Binding to Sodium and Potassium Binding by Rat Liver Cell Microsomes and Human Erythrocyte Ghosts.”J. cell. comp. Physiol.,59, 241–250.

    Article  Google Scholar 

  • — and N. Pace. 1962. “Sodium and Potassium Binding by Human Erythrocyte Ghosts.”J. cell. comp. Physiol.,59, 251–257.

    Article  Google Scholar 

  • Shah, D. O. and J. H. Schulman. 1967. “Influence of Calcium, Cholesterol and Unsaturation on Lecithin Monolayers.”J. Lipid. Res.,8, 215–226.

    Google Scholar 

  • Sheetz, M. P. and S. J. Singer. 1974. “Biological Membranes as Bilayer Couples. A Molecular Mechanism of Drug-Erythrocyte Interactions.”Proc. natl. Acad. Sci. U.S.A.,71, 4457–4461.

    Article  Google Scholar 

  • Tanford, C. and J. A. Reynolds. 1976. “Characterization of Membrane Proteins in Detergent Solutions.”Biochim. biophys. Acta,457, 133–170.

    Google Scholar 

  • Tien, H. T. and E. A. Dawidowicz. 1966. “Black Lipid Films in Aqueous Media: A New Type of Interfacial Phenomenon.”J. Colloid Interface Sci.,22, 438–453.

    Article  Google Scholar 

  • Tolberg, A. B. and R. I. Macey. 1972. “The Release of Membrane-Bound Calcium by Radiation and Sulfhydryl Reagents.”J. cell. Physiol. 79, 43–52.

    Article  Google Scholar 

  • Turner, J. D. and G. Rouser. 1970. “Precise Quantitative Determination of Human Blood Lipids by Thin-layer and Triethylaminoethylcellulose Column Chromatography.”Analyt. Biochem.,38, 423–436.

    Article  Google Scholar 

  • Vandenheuvel, F. A. 1963. “Study of Biological Structure at the Molecular Level with Stereomodel Projections: I. The Lipids in the Myelin Sheath of Nerve.”J. Am. Oil Chem. Soc.,40, 455–471.

    Google Scholar 

  • Verkleij, A. J., R. F. A. Zwaal, B. Roelofsen, P. Comfurius, D. Kastelijn and L. L. M. van Deenen. 1973. “The Asymmetric Distribution of Phospholipids in the Human Red Cell Membrane.”Biochem. biophys. Acta,323, 178–193.

    Google Scholar 

  • Weed, R. I. and B. Chailley. 1972. “Calcium-pH Interactions in the Production of Shape Change in Erythrocytes.”Nouv. Rev. Fr. Hémat. 12, 775–788.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Physiology-Anatomy, and Group in Biophysics and Medical Physics, University of California, 94720, Berkeley, CA, USA

    Gregory S. B. Lin

Authors
  1. Gregory S. B. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lin, G.S.B. Theory of cation-phospholipid-induced shape changes in a lipid bilayer couple. Bltn Mathcal Biology 42, 601–625 (1980). https://doi.org/10.1007/BF02460983

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02460983

Keywords

Search

Navigation