Abstract
In the first paper in this series (Stokke et al. Eur Biophys J 1986, 13:203–218) we developed the general theory of the mechanochemical properties and the elastic free energy of the protein gel — lipid bilayer membrane model. Here we report on an extensive numerical analysis of the human erythrocyte shapes and shape transformations predicted by this new cell membrane model. We have calculated the total elastic free energy of deformation of four different cell shape classes: disc-shaped cells, cup-shaped cells, crenated cells, and cells with membrane invaginations. We find that which of these shape classes is favoured depends strongly on the spectrin gel osmotic tension, ΠGu, and the surface tensions, ΠEu and ΠPu, of the extracellular and protoplasmic halves of the membrane lipid bilayer, respectively. For constant ratio ΠEu/ΠPu>0 large negative or positive values of ΠGu favour respectively the crenated and invaginated cell shape classes. For small absolute values of ΠGu, ΠEu, and ΠPu, biconcave or cup-shaped cells are the stable ones. Our numerical analysis shows that the higher the membrane skeleton compressibility is, the smaller are the values of ΠGu needed to induce cell shape transformation. We find that the stable and metastable shapes of discocytes and stomatocytes generally depend both on the shape of the stressfree membrane skeleton and the membrane skeleton compressibility.
Similar content being viewed by others
References
Bennet V (1982) The molecular basis for membrane — cytoskeleton association in human erythrocytes. J Cell Biochem 18:49–65
Brailsford JD, Bull BS (1973) The red cell. A macromodel simulating the hypotonic — sphere isotonic — disc transformation. J Theor Biol 39:325–332
Brailsford JD, Korpman RA, Bull BS (1976) The red cell shape from discocyte to hypotonic spherocyte. A mathematical delineation based on a uniform shell hypothesis. J Theor Biol 60:131–145
Brailsford JD, Korpman RA, Bull BS (1980a) Crenation and cupping of the red cell: A new theoretical approach. Part I. Crenation. J Theor Biol 86:513–529
Brailsford JD, Korpman RA, Bull BS (1980b) Crenation and cupping of the red cell: A new theoretical approach. Part II. Cupping. J Theor Biol 86:531–546
Branton D, Cohen CM, Tyler J (1981) Interaction of cytoskeletal proteins on the human erythrocyte membrane. Cell 24:24–32
Bull B (1972) The red cell biconcavity and deformability. A macromodel based on flow chamber observations. Nouv Rev Fr Hematol 12:835–844
Canham PB (1970) The minimum energy of bending as a possible explanation of the biconcave shape of the human red blood cell. J Theor Biol 26:61–81
Cohen CM (1983) The molecular organization of the red cell membrane skeleton. Semin Hematol 20:141–158
Deuling HJ, Helfrich W (1976) Red blood cell shapes as explained on the basis of curvature elasticity. Biophys J 16: 861–868
Doulah FA, Coakley WT, Tilley D (1984) Intrisic electric fields and membrane bending. J Biol Phys 12:44–51
Elgsaeter A, Branton D (1974) Intramembrane particle aggregation in erythrocyte ghosts I. The effects of protein removal. J Cell Biol 63:1018–1030
Elgsaeter A, Shotton DM, Branton D (1976) Intramembrane particle aggregation in erythrocyte ghosts II. The influence of spectrin aggregation. Biochim Biophys Acta 426:101–122
Evans EA (1973) New membrane concept applied to the analysis of fluid shear- and micropipette-deformed red blood cells. Biophys J 13:941–954
Evans EA (1974) Bending resistance and chemically induced moments in membrane bilayers. Biophys J 14:923–931
Evans EA, Hochmuth RM (1977) A solid — liquid composite model of the red cell membrane. J Membr Biol 30:351–362
Evans EA, Hochmuth RM (1978) Mechanochemical properties of membranes. Curr Top Membr Transport 10:1–64
Evans EA, Skalak R (1979) Mechanics and thermodynamics of biomembranes. Crit Rev Bioeng 3:181–420
Fairbanks G, Patel VP, Dino JE (1981) Biochemistry of ATP-dependent red cell membrane shape change. Scand J Clin Lab Invest 41:139–144
Fung YCB, Tong P (1968) Theory of the sphering of red blood cells. Biophys J 8:175–198
Gratzer WB (1983) The cytoskeleton of the red blood cell. Stracher A (ed) Muscle and nonmuscle motility. Academic Press, New York, pp 37–124
Johnson RM, Robinson J (1976) Morphological changes in asymmetric erythrocyte membranes induced by electrolytes. Biochem Biophys Res Commun 70:925–931
Kwok R, Evans E (1981) Thermoelasticity of large lecithin bilayer vesicles. Biophys J 35:637–652
Lange Y, Hadesman RA, Steck TL (1982a) Role of the reticulum in the stability and shape of the isolated human erythrocyte membrane. J Cell Biol 92:714–721
Lange Y, Gough A, Steck TL (1982b) Role of the bilayer in the shape of the isolated erythrocyte membrane. J Membr Biol 69:113–123
Markin VS (1981) Lateral organization of membranes and cell shape. Biophys J 36:1–19
Nicolson GL (1973) Antonic sites of human erythrocyte membranes I. Effects of trypsin, phospholipase C, and pH on the topography of bound positively changed colloidal particles. J Cell Biol 57:373–389
Papahadjopoulos D (1968) Surface properties of acidic phospholipids: Interaction of monolayers and hydrated liquid crystals with uni- and bivalent metal ions. Biochim Biophys Acta 163:240–254
Sheetz MP (1983) Membrane skeletal dynamics: Role in modulation of red cell deformability, mobility of transmembrane proteins, and shape. Sem Hematol 20:175–188
Sheetz MP, Singer SJ (1974) Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci USA 71:4457–4461
Sheetz MP, Painter RG, Singer SJ (1976) Biological membranes branes as bilayer couples. III. Compensatory shape changes induced in membranes. J Cell Biol 70:193–203
Skalak R, Tozeren A, Zarda PR, Chien S (1973) Strain energy function of red blood cell membranes. Biophys J 13: 245–264
Steck TL, Weinstein RS, Straus JH, Wallach DFH (1970) Inside-out red cell membrane vesicles: Preparation and purification. Science 168:255–257
Stokke BT (1985) The role of spectrin in determining mechanical properties, shapes, and shape transformations of human erythrocytes. Dr. ing. thesis, University of Trondheim, 4.34–4.52
Stokke BT, Mikkelsen A, Elgsaeter A (1986) The human erythrocyte membrane skeleton may be an ionic gel. I. Membrane mechanical properties. Eur Biophys J 13:203–218
Tamura A, Fujii T (1981) Roles of charged groups on the surface of membrane lipid bilayer of human erythrocytes in induction of shape change. J Biochem 90:629–634
Tanaka T, Filmore D, Sun ST, Nishio I, Swislow G, Shah A (1980) Phase transitions in ionic gels. Phys Rev Lett 45:1636–1639
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Stokke, B.T., Mikkelsen, A. & Elgsaeter, A. The human erythrocyte membrane skeleton may be an ionic gel. Eur Biophys J 13, 219–233 (1986). https://doi.org/10.1007/BF00260369
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF00260369