Animal Cell Membranes as Substrata for Bacterial Adhesion

  • Itzhak Ofek
  • Ronald J. Doyle


The purpose of this chapter is to review briefly the composition and organization of animal cell surface structures that may be potential receptors for adhesins of bacteria. The understanding of the specificity of animal cell—bacteria interactions requires a basic knowledge of the molecular structure of the animal cell surface, especially of those molecules that serve as receptors for ligands in general and for bacterial adhesins in particular. All animal cell membranes share common compositional and organizational features (Figure 3-1): (1) The major membrane lipids are arranged in a planar bilayer configuration that is predominantly in a “fluid” state under physiological conditions. The membrane lipids are commonly composed of glycerolphospholipids, sphingolipids, and sterols. (2) The bilayer membrane contains integral membrane constituents composed of both glycolipids and glycoproteins that are inserted or “intercalated” into the bilayer structure. (3) Other glycoproteins and proteins are bound to the surface of the plasma membrane by weak ionic interactions, hydrogen bonding, or the hydrophobic effect. These surface-associated glycoproteins and proteins bound to integral membrane structures are referred to as peripheral or extrinsic components. (4) In many animal cells there is a substantial layer of carbohydrate-containing materials of variable thicknesses outside the plasma membrane but in close or intimate association with the membrane. This layer is known as the cell coat or extracellular matrix. The distinction between membrane constituents as being integral, peripheral, or belonging to the cell coat is based on the method required to dissociate the constituent in question from the cell membrane. The integral constituents may be released only after disruption or perturbation of the phospholipid bilayer, usually by detergents (Lichtenberg et al., 1983). Nonintegral surface constituents are commonly released by washing the cells with buffers of different pH or ionic strength, or by using chelating agents, such as ethylenediaminetetraacetic acid (EDTA). There is no general method, however, to release selectively either peripheral or extracellular matrix constituents. As a result, the distinction between the two classes of membrane constituents is sometimes difficult to resolve and very often they are referred to as nonintegral membrane constituents. One of the key features of the membrane is its asymmetry. For nonglycosylated lipids the asymmetry is only partial, in that every phospholipid is present on both sides of the bilayer but in different amounts. In human erythrocytes, for example, lipids with positively charged head groups (e.g., phosphatidylethanolamine and phosphatidylserine) are predominant in the internal leaflet facing the cytoplasm (Marinetti and Crain, 1978). The asymmetry with respect to proteins, glycoproteins, and glycolipids is absolute: every molecule of a given membrane constituent has the same orientation across the lipid bilayer, with the carbohydrate moieties of the glycosylated compounds always exposed on the outer surface. For further information on the organization of the animal cell membrane, the reader is referred to reviews (Lodish et al., 1981; Lotan and Nicolson, 1981; Singer, 1981; Aplin and Hughes, 1982) and a book (Sim, 1982).


Sialic Acid Animal Cell Attachment Site Bacterial Adhesion Membrane Glycoprotein 
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  1. Aplin, J.D. and R.C. Hughes. 1982. Complex carbohydrates of the intracellular matrix: structures, interactions and biological roles. Biochim. Biophys. Acta 694: 375–418.PubMedGoogle Scholar
  2. Ashwell, G. and J. Harford. 1982. Carbohydrate-specific receptors of the liver. Annu. Rev. Biochem. 51: 531–554.PubMedCrossRefGoogle Scholar
  3. Beachey, E.H., W.A. Simpson, I. Ofek, D.K. Hasty, J.B. Dale, and E. Whitnack. 1983. Attachment of Streptococcus pyogenes to mammalian cells. Rev. Infect. Dis. 5: 5670–5677.CrossRefGoogle Scholar
  4. Callies, R., G. Schwarzmann, K. Radsak, R. Siegert, and H. Wiegandt. 1977. Characterization of the cellular binding of exogenous gangliosides. Eur. J. Biochem. 80: 425–423.PubMedCrossRefGoogle Scholar
  5. Cherry, R.J. 1979. Rotational and lateral diffusion of membrane proteins. Biochim. Biophys. Acta 559: 289–327.PubMedGoogle Scholar
  6. Clamp, J. 1974. Analysis of glycoproteins. Biochem. Soc. Symp. 40: 3–16.PubMedGoogle Scholar
  7. Critchley, D.R. 1979. Glycolipids as membrane receptors important in growth regulation. In: Hynes, R.O. (ed.), Surfaces of Normal and Malignant Cells. John Wiley & Sons, New York, pp. 63–101.Google Scholar
  8. Critchley, D.R., C.H. Streuli, S. Kellie, S. Ansell, and B. Patel. 1982. Characterization of the cholera toxin receptor on Balb/C3T3 cells as a ganglioside similar to, or identical with, ganglioside GM,: no evidence for galactoproteins with receptor activity. Biochem. J. 204: 209–219.PubMedGoogle Scholar
  9. Cuatrecasas. P. 1974. Membrane receptors. Annu. Rev. Biochem. 43: 169–214.PubMedCrossRefGoogle Scholar
  10. Duk, M., E. Lisowska, M. Kordowicz, and K. Wasniowska. 1982. Studies on the specificity of the binding site of Vicia graminea anti-N lectin. Eur. J. Biochem. 123: 105–112.PubMedCrossRefGoogle Scholar
  11. Edidin, M. 1974. Rotational and translational diffusion in membranes. Annu. Rev. Biophys. Bioeng. 8: 165–193.Google Scholar
  12. Eytan, G.D. 1982. Use of liposomes for reconstruction of biological function. Biochim. Biophys. Acta 694: 185–202.PubMedGoogle Scholar
  13. Feldner, J., W. Bredt, and I. Kahane. 1979. Adherence of erythrocytes to Mycoplasma pneumoni ae. Infect. Immun. 30: 554–561.Google Scholar
  14. Findlay, J.B.C. 1974. The receptor proteins for concanavalin A and Lens culinaris phytohemagglutinin in the membrane of the human erythrocyte. J. Biol. Chem. 249: 4398–4403.PubMedGoogle Scholar
  15. Finean, J.B., R. Coleman, and R.H. Mitchell. 1984. Membranes and Their Cellular Function, 3rd ed. Blackwell, Oxford.Google Scholar
  16. Finne, J. 1980. Identification of the blood-group ABO-active glycoprotein components of human erythrocyte membrane. Eur. J. Biochem. 104: 181–189.PubMedCrossRefGoogle Scholar
  17. Fishman, P.H. 1982. Role of membrane gangliosides in the binding and action of bacterial toxins. J. Membr. Biol. 69: 85–97.PubMedCrossRefGoogle Scholar
  18. Flowers, H.M. and N. Sharon. 1979. Glycosidases-properties and application to the study of complex carbohydrates and cell surfaces. Adv. Enzymol. 48: 29–95.PubMedGoogle Scholar
  19. Fukuda, M. and M.N. Fukuda. 1978. Changes in cell surface glycoproteins and carbohydrate structures during the development and differentiation of human erythroid cells. J. Supramol. Struct. 8: 313–324.Google Scholar
  20. Gahmberg, C.G. 1977. Cell surface proteins: changes during cell growth and malignant transformation. In: Poste, G. and G.L. Nicholson (eds.), Cell Surface Reviews. North-Holland, Amsterdam, pp. 371–421.Google Scholar
  21. Gahmberg, C.G. 1981. Membrane glycoproteins and glycolipids: structure, localization and function of carbohydrates. In: Finean, J.B. and R.H. Mitchell (eds.), Membrane Structure. Elsevier/North-Holland, Amsterdam, pp. 127–160.CrossRefGoogle Scholar
  22. Gahmberg, C.G. and L.C. Anderson. 1982. Surface glycoproteins of malignant cells. Biochim. Biophys. Acta 651: 65–83.PubMedGoogle Scholar
  23. Garoff, H. 1979. Structure and assembly of the Semliki Forest virus membrane. Biochem. Soc. Trans. 7: 301–306.PubMedGoogle Scholar
  24. Geiger, B. 1983. Membrane cytoskeleton interactions. Biochim. Biophys. Acta 737: 305–341.PubMedGoogle Scholar
  25. Hakomori, S. 1981. Glycosphingolipids in cellular interaction, differentiation and oncogenesis. Annu. Rev. Biochem. 50: 733–764.PubMedCrossRefGoogle Scholar
  26. Hynes, R.O. and K.M. Yamada. 1982. Fibronectins: multifunctional molecular glycoproteins. J. Cell Biol. 95: 369–377.PubMedCrossRefGoogle Scholar
  27. Izhar, M., Y. Nuchamowitz, and D. Mirelman. 1982. Adherence of Shigella flexneri to guinea pig intestinal cells is mediated by a mucosal adhesin. Infect. Immun. 35: 1110–1118.PubMedGoogle Scholar
  28. Kallenius, G., S.B. Svensson, R. Mollby, B. Cedergren, H. Hultberg, and J. Winberg. 1981. Structure of carbohydrate part of receptor on human uroepithelial cells for pyelonephritogenic Escherichia coli. Lancet 2: 604–606.Google Scholar
  29. Koscielak, J., H. Miller-Podraza, R. Krauze, and A. Piasek. 1976. Isolation and characterization of poly(glycosyl) ceramides (megaloglycolipids) with A,H and I blood-group activities. Eur. J. Biochem. 71: 9–18.PubMedCrossRefGoogle Scholar
  30. Leffler, H. and C. Svanborg-Eden. 1981. Glycolipid receptors for uropathogenic Escherichia coli on human erythrocytes and uroepithelial cells. Infect. Immun. 34: 920–929.PubMedGoogle Scholar
  31. Lichtenberg, D., R.J. Robson, and E.A. Dennis. 1983. Solubilization of phospholipids by detergents: structural and kinetic aspects. Biochim. Biophys. Acta 737: 285–304.PubMedGoogle Scholar
  32. Lodish, H.F., W.A. Braell, A.L. Schwartz, G.J.A.M. Strous, and A. Zilberstein. 1981. Synthesis and assembly of membrane and organelle proteins. Int. Rev. Cytol. Suppl. 12: 247–307.PubMedGoogle Scholar
  33. Lotan, R. and G.L. Nicolson. 1981. Plasma membrane of eukaryotes, In: Schwartz, L.M. and M.M. Azar (eds.), Advanced Cell Biology. Van Nostrand-Reinhold, Princeton, NJ, pp. 129–154.Google Scholar
  34. Marchesi, V.T., H., Furthmayr, and M., Tornita. 1976. The red cell membrane. Annu. Rev. Biochem. 45: 667–698.PubMedCrossRefGoogle Scholar
  35. Marinetti, G.V. and R.C., Crain, 1978. Topology of amino-phospholipids in the red-cell membrane. J. Supramol. Struct. 8: 191–213.CrossRefGoogle Scholar
  36. Mirelman, D. and I. Ofek. 1986. Introduction to microbial lectins and agglutinins. In: Mirelman, D. (ed.), Microbial Lectins and Agglutinins. John Wiley & Sons, New York, pp. 1–19.Google Scholar
  37. Nicolson, G.L. 1976. Trans-membrane control of the receptors on normal and tumor cells. I. Cytoplasmic influence of cell surface components. Biochim. Biophys. Acta 457: 57–108.PubMedGoogle Scholar
  38. Nicolson, G.L. 1979. Topographic display of cell surface components and their role in trans-membrane signaling. Curr. Top. Dev. Biol. 3: 305–338.CrossRefGoogle Scholar
  39. Ofek, I., H. Lis, and N. Sharon. 1985. Animal cell surface membranes. In: Savage, D.C. and M. Fletcher (eds.), Bacterial Adhesion: Mechanisms and Physiological Significance, Plenum Press, New York, pp. 71–88.Google Scholar
  40. Prives, J.M. 1980. Nicotinic acetylcholine receptors. In: Schulster, D. and A. Levitski (eds.), Cellular Receptors for Hormones and Neurotransmitters. John Wiley & Sons, New York, pp. 331–351.Google Scholar
  41. Raff, M.C. and S. dePetris. 1973. Movement of lymphocyte surface antigens and receptors: the fluid nature of the lymphocyte plasma membrane and its immunological significance. Fed. Proc. 32: 48–54.PubMedGoogle Scholar
  42. Roth, J. 1980. The use of lectins as probes for carbohydrates-cytochemical techniques and their application in studies on cell surface dynamics. Acta Histochem. Suppl. 22: 113–121.PubMedGoogle Scholar
  43. Ruoslahti, E. 1988. Fibronectin and its receptors. Annu. Rev. Biochem. 57:375–413. Ruoslahti, E. 1991. Integrins. J. Clin. Invest. 87: 1–5.Google Scholar
  44. Ruoslahti, E., M. Pierschbacher, E.G. Hayman, and E. Engvall. 1982. Fibronectin: a molecule with remarkable structural and functional diversity. Trends Biochem. Sci. 7: 188–190.CrossRefGoogle Scholar
  45. Schulster, D. and A. Levitski (eds.). 1980. Cellular Receptors for Hormones and Neurotransmitters. John Wiley & Sons, New York.Google Scholar
  46. Sedlacek, H.H., J. Stark, F.R. Seiler, W. Ziegler, and H. Wiegandt. 1976. Cholera toxin induces redistribution of sialoglycolipid receptor at the lymphocyte membrane. FEBS Lett. 61: 272–276.PubMedCrossRefGoogle Scholar
  47. Sharon, N. 1975. Complex Carbohydrates: Their Chemistry, Biosynthesis, and Functions. Addison-Wesley, Reading, MA.Google Scholar
  48. Sharon, N. 1981. Glycoproteins in membranes. In: Balian, R., M. Chabre, and P.F. Devaux (eds.), Membranes and Intercellular Communications. North-Holland, Amsterdam, pp. 117–182.Google Scholar
  49. Sharon, N. and H. Lis 1981. Glycoproteins: research booming on long-ignored, ubiquitous compounds. Chem. Engr. News 59: 21–24.CrossRefGoogle Scholar
  50. Sharon, N. and H. Lis. 1982. Glycoproteins. In: Neurath, H., and R.L. Hill (eds.), The Proteins, Vol. V, 3rd ed. Academic Press, New York, pp. 1–144.Google Scholar
  51. Sharon, N. and H. Lis. 1989. Lectins as cell recognition molecules. Science 246: 227–234.PubMedCrossRefGoogle Scholar
  52. Sim, E. 1982. Membrane Biochemistry. Chapman and Hall, London.CrossRefGoogle Scholar
  53. Singer, S.J. 1974. The molecular organization of membranes. Annu. Rev. Biochem. 43: 805–833.PubMedCrossRefGoogle Scholar
  54. Singer, S.J. 1981. The cell membrane. In: Balian, R., M. Chabre, and P.F. Devaux (eds.), Membranes and Intercellular Communication. North-Holland, Amsterdam, pp. 1–16.Google Scholar
  55. Singer, S.J. and G.L. Nicolson. 1972. The fluid mosaic model of cell membranes. Science 175: 710–731.CrossRefGoogle Scholar
  56. Steck, T.L. 1978. Band 3 protein of the human red cell membrane: a review. J. Supramol. Struct. 8: 311–324.PubMedCrossRefGoogle Scholar
  57. Tanner, M.J.A. 1978. Erythrocyte glycoproteins. Curr. Top. Membr. Transp. 11: 279–325.CrossRefGoogle Scholar
  58. Tollefsen, S.E. and R. Kornfeld. 1983. The B4 lectin from Vicia villosa interacts with N-acetylgalactosamine residues linked to serine or threonine residues in cell surface glycoproteins. J. Biol. Chem. 258: 5172–5176.PubMedGoogle Scholar
  59. Wicken, A.J. and K.W. Knox. 1981. Composition and properties of amphiphiles. In: Shockman, G.D. and A.J. Wicken (eds.), Chemistry and Biological Activities of Bacterial Surface Amphiphiles. Academic Press, New York, pp. 1–7.Google Scholar
  60. Wiegandt, H., S. Kanda, K. Inoue, K. Utsumi, and S. Nojima. 1981. Studies on the cell association of exogenous glycolipids. Adv. Exp. Med. Biol. 152: 343–352.Google Scholar
  61. Yamakawa, T. and Y. Nagai. 1978. Glycolipids at the cell surface and their biological functions. Trends Biochem. Sci. 3: 128–131.CrossRefGoogle Scholar

Copyright information

© Chapman & Hall, Inc. 1994

Authors and Affiliations

  • Itzhak Ofek
    • 1
  • Ronald J. Doyle
    • 2
  1. 1.Tel-AvivIsrael
  2. 2.LouisvilleUSA

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