Relationship Between Bacterial Cell Surfaces and Adhesins

  • Itzhak Ofek
  • Ronald J. Doyle


The central dogma of bacterial adhesion requires that the adhesin(s) function from the bacterial surface. In most cases, the adhesins are assembled on the surface, but in a few cases, the adhesins are initially secreted in the soluble form and then associate with the bacterial surface (Tuomanen, 1986; Baker et al., 1991; Wentworth et al., 1991). In either case, the adhesin must dock or anchor on the bacterial surface before it can participate in adhesive processes. Because adhesion is a property of most bacteria, especially of tissue-colonizing bacteria, it follows that evolution has selected specific structures that function as adhesins or onto which adhesins can assemble. In this chapter, a concise review of bacterial surface structures, with special emphasis on macromolecules involved in adhesion, is given. More comprehensive discussions of the bacterial cell surface are provided elsewhere (Rogers et al., 1980; Nikaido and Vaara, 1985; Krell and Beveridge, 1987; Doyle and Sonnenfeld, 1989; Handley, 1990; Hancock, 1991; Irvin, 1990; Gilbert et al., 1991).


Outer Membrane Cytoplasmic Membrane Outer Membrane Protein Bacterial Adhesion Bacterial Surface 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alkan, M.L. and E.H. Beachey, 1978. Excretion of lipoteichoic acid by group A streptococci: influence of penicillin on excretion and loss of ability to adhere to human oral mucosal cells. J. Clin. Invest. 61: 671–677.PubMedGoogle Scholar
  2. Altwegg, M. and H.K. Geiss. 1989. Aeromonas as a human pathogen. CRC Crit. Rev. Microbiol. 16: 253–286.Google Scholar
  3. Aly, R. and S. Levit. 1987. Adherence of Staphylococcus aureus to squamous epithelium: role of fibronectin and teichoic acid. Rev. Infect. Dis. 9: S341 - S350.PubMedGoogle Scholar
  4. Aly, R., H.R. Shinefield, C. Litz, and H.I. Maibach. 1980. Role of teichoic acid in the binding of Staphylococcus aureus to nasal epithelial cells. J. Infect. Dis. 141: 463–465.PubMedGoogle Scholar
  5. Anderson, B., J. Dahmen, T. Frejd, H. Leffler, G. Magnusson, G. Noori, and C. Svanborg-Eden. 1983. Identification of an active disaccharide unit of a glycoconjugate receptor for pneumococci attaching to human pharyngeal epithelial cells. J. Exp. Med. 158: 559–570.Google Scholar
  6. Relationship Between Bacterial Cell Surfaces and Adhesins l 87 of guinea pig alveolar macrophages and human monocyte-derived macrophages. Infect. Immun. 59: 1673–1682.Google Scholar
  7. Attridge, S.R. and D. Rowley. 1983. The role of the flagellum in the adherence of Vibrio cholerae. J. Infect. Dis. 147: 864–872.PubMedGoogle Scholar
  8. Baddour, L.M., G.D. Christensen, W.A. Simpson, and E.H. Beachey. 1989. Microbial adherence. In: Mandell, G.L., R.G. Douglas, Jr. and J.E. Bennett (eds.), Principles and Practices of Infectious Disease. Churchill Livingstone, New York, pp. 9–25.Google Scholar
  9. Baker, N.R., V. Minor, C. Deal, M.S. Shahrabadi, D.A. Simpson, and D.E. Woods. 1991. Pseudomonas aeruginosa exoenzyme S is an adhesin. Infect. Immun. 59: 2859–2863.PubMedGoogle Scholar
  10. Birdsell, D.C., R.J. Doyle, and M. Morgenstern. 1975. Organization of teichoic acid in the cell wall of Bacillus subtilis. J. Bacteriol. 121: 726–734.PubMedGoogle Scholar
  11. Braun, V. 1975. Covalent lipoprotein from the outer membrane of Escherichia coli. Biochim. Biophys. Acta 415: 335–377.PubMedGoogle Scholar
  12. Brinton, C.C., Jr. 1959. Non-flagellar appendages of bacteria. Nature 183: 782–786.PubMedGoogle Scholar
  13. Brook, I. and M.L. Myhal. 1991. Adherence of Bacteroides fragilis group species. Infect. Immun. 59: 742–744.PubMedGoogle Scholar
  14. Busscher, H.J., P.S. Handley, P.G. Rouxhet, L.M. Hesketh, and H.C. van der Mei. 1991. The relationship between structural and physicochemical surface properties of tufted Streptococcus sanguis strains. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH publishers, New York, pp. 317–338.Google Scholar
  15. Christensen, G.D., W.A. Simpson, A.L. Bisno, and E.H. Beachey. 1982. Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect. Immun. 37: 318–326.PubMedGoogle Scholar
  16. Conway, P.L. and S. Kjelleberg. 1989. Protein-mediated adhesion of Lactobacillus fermentum strain 737 to mouse stomach squamous epithelium. J. Gen. Microbiol. 135: 1175–1186.PubMedGoogle Scholar
  17. Costerton, J.W., R.T. Irvin, and K.J. Cheng. 1981. The bacterial glycocalyx in nature and disease. Annu. Rev. Microbiol. 35: 299–324.PubMedGoogle Scholar
  18. DeGraaf, F.K. 1990. Genetics of adhesive fimbriae of intestinal Escherichia coli. Curr. Top. Microbiol. Immunol. 151: 29–53.Google Scholar
  19. DeGraaf, F.K. and F.R. Mooi. 1986. The fimbrial adhesins of Escherichia coli. Adv. Microbial Physiol. 28: 65–143.Google Scholar
  20. Dekker, N.P., C.J. Lammel, R.E. Mandrell, and G.F. Brooks. 1990. Opa (protein II) influences gonococcal organization in colonies, surface appearance, size and attachment to human fallopian tube tissues. Microb. Pathogen. 9: 19–31.Google Scholar
  21. DiRienzo, J.M., K. Nakamura, and M. Inouye. 1978. The outer membrane proteins of Gram-negative bacteria: biosynthesis, assembly, and functions. Annu. Rev. Biochem. 47: 481–532.PubMedGoogle Scholar
  22. Doig, P., P.A. Sastry, R.S. Hodges, K.K. Lee, W. Paranchych, and R.T. Irvin. 1990. Inhibition of pilus-mediated adhesion of Pseudomonas aeruginosa to human buccal epithelial cells by monoclonal antibodies directed against pili. Infect. Immun. 58: 124–130.PubMedGoogle Scholar
  23. Doyle, R.J. and M. Rosenberg (eds.). 1990. Microbial Cell Surface Hydrophobicity. American Society for Microbiology, Washington.Google Scholar
  24. Doyle, R.J. and E.M. Sonnenfeld. 1989. Properties of the cell surfaces of pathogenic bacteria. Int. Rev. Cytol. 18: 33–92.Google Scholar
  25. Doyle, R.J., M.L. McDannel, J.R. Heiman, and U.N. Streips, 1975. Distribution of teichoic acid in the cell wall of Bacillus subtilis. J. Bacteriol. 122: 152–158.PubMedGoogle Scholar
  26. Doyle, R.J., J. Chaloupka, and V. Vinter. 1988. Turnover of cell walls in microorganisms. Microbiol. Rev. 52: 554–567.PubMedGoogle Scholar
  27. Drake, D., K.G. Taylor, A.S. Bleiweis, and R. J. Doyle. 1988a. Specificity of the glucan binding lectin of Streptococcus cricetus. Infect. Immun. 56: 1864–1872.PubMedGoogle Scholar
  28. Drake, D., D.G. Taylor, and R.J. Doyle. 1988b. Expression of glucan-binding lectin of Streptococcus cricetus requires manganous ion. Infect. Immun. 56: 2205–2207.PubMedGoogle Scholar
  29. Duguid, J.P. and D.C. Old. 1980. Adhesive properties of Enterobacteriaceae. In: Beachey, E.H. (ed.), Bacterial Adherence (Receptors and Recognition, Vol. 6 ). Chapman and Hall, London, pp. 187–217.Google Scholar
  30. Duguid, J.P., I.W. Smith, G. Dempster, and P.N. Edmunds. 1955. Non-flagellar filamentous appendages (“fimbriae”) and hemagglutinating activity in Bacterium coli. J. Pathol. Bacteriol. 70: 335–358.PubMedGoogle Scholar
  31. Duguid, J.P., E.S. Anderson, and I. Campbell. 1966. Fimbriae and adhesive properties in salmonellae. J. Pathol. Bacteriol. 92: 107–138.PubMedGoogle Scholar
  32. Dziarski, R. 1991. Peptidoglycan and lipopolysaccharide bind to the same binding site on lymphocytes. J. Biol. Chem. 266: 4719–4725.PubMedGoogle Scholar
  33. Eshdat, Y., N. Sharon, I. Ofek and D. Mirelman. 1978. Isolation of a mannose-specific lectin from Escherichia coli and its role in the adherence of the bacteria to epithelial cells. Biochem. Biophys. Res. Commun. 85: 1551–1559.PubMedGoogle Scholar
  34. Eshdat, Y., V. Speth, and K. Jann. 1981a. Participation of pili and cell wall adhesin in the yeast agglutination activity of Escherichia coli. Infect. Immun. 34: 980–986.PubMedGoogle Scholar
  35. Eshdat, Y., M. Izhar, N. Sharon, and D. Mirelman. 198lb. Structural association of the outer surface mannose-specific lectin of Escherichia coli with bacterial flagella. Isr. J. Med. Sci. 16: 479.Google Scholar
  36. Fauchere, J.L., M. Kervella, A. Rosenau, K. Mohanna, and M. Vernon. 1989. Adhesion to HeLa cells of Campylobacter jejuni and C. coli outer membrane components. Res. Microbiol. 140: 379–392.PubMedGoogle Scholar
  37. Fischer, W. 1988. Physiology of lipoteichoic acids in bacteria. Adv. Microbial Physiol. 29: 233–302.Google Scholar
  38. Fischetti, V. 1991. Streptococcal M protein. Sci. Am., June pp. 58–65.Google Scholar
  39. Fulks, K.A., C.F. Marrs, S.P. Stevens, and M.R. Green. 1990. Sequence analysis of the inversion region containing the pilin genes of Moraxella bovis. J. Bacteriol. 172: 310–316.PubMedGoogle Scholar
  40. Gaastra, W. and F.K. DeGraaf. 1982. Host-specific fimbrial adhesins and noninvasive enterotoxigenic Escherichia coli strains. Microbiol. Rev. 46: 129–161.PubMedGoogle Scholar
  41. Gilbert, P., D.J. Evans, I.G. Duguid, E. Evans, and M.R. W. Brown. 1991. Cell surface properties of Escherichia coli and Staphylococcus epidermidis. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.). Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH Publishers, New York, pp. 339–356.Google Scholar
  42. Gilboa-Garber, N. 1982. Pseudomonas aeruginosa lectins. Meth. Enzymol. 83: 378–385.PubMedGoogle Scholar
  43. Goldhar, J., R. Perry, J.R. Golecki, H. Hoschutzky, B. Jann and K. Jann. 1987. Nonfimbrial, mannose-resistant adhesins from uropathogenic Escherichia coli 083:K1:H4 and 014:K?: H 11. Infect. Immun. 55: 1837–1842.PubMedGoogle Scholar
  44. Gotschlich, E.C. 1983. Thoughts on the evolution of strategies used by bacteria for evasion of host defenses. Rev. Infect. Dis. 5 (Suppl. 4): S778 - S783.PubMedGoogle Scholar
  45. Gunnarsson, A., P.A. Mardh, A. Lundblad, and S. Svensson. 1984. Oligosaccharide structures mediating agglutination of sheep erythrocytes by Staphylococcus saprophyticus. Infect. Immun. 45: 41–46.PubMedGoogle Scholar
  46. Hacker, J. 1990. Genetic determinants coding for fimbrial adhesins of extra-intestinal Escherichia coli. Curr. Top. Microbiol. Immunol. 151: 1–27.PubMedGoogle Scholar
  47. Hancock, I.C. 1991. Microbial cell surface architecture. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH publishers, New York, pp. 21–59.Google Scholar
  48. Handley, P.S. 1990. Structure, composition and functions of surface structures of oral bacteria. Biofouling 2: 239–264.Google Scholar
  49. Handley, P.S. 1991a. Negative staining. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH Publishers, New York, pp. 63–86.Google Scholar
  50. Handley, P.S. 1991b. Detection of cell surface carbohydrate components. In: N. Mozes, P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH Publishers, New York, pp. 87–107.Google Scholar
  51. Handley, P.S. J. Hargreaves, and D.W. Harty. 1988. Ruthenium red staining reveals surface fibrils and a layer external to the cell wall in Streptococcus salivarius HB and adhesion deficient mutants. J. Gen. Microbiol. 134: 3165–3172.PubMedGoogle Scholar
  52. Heesemann, J. and L. Gruter. 1987. Genetic evidence that the outer membrane protein YOP1 of Yersinia enterocolitica mediates adherence and phagocytosis resistance to human epithelial cells. FEMS Microbiol. Let. 40: 37–41.Google Scholar
  53. Hogt, A.H., J. Dankert, and J. Feijen. 1983. Encapsulation, slime production and surface hydrophobicity of coagulase-negative staphylococci. FEMS Microbiol. Lett. 18: 211–215.Google Scholar
  54. Hultgren, S.J., J.L. Duncan, A.J. Schaeffer, and S.K. Amundsen. 1990. Mannosesensitive haemagglutination in the absence of piliation in Escherichia coli. Mol. Microbiol. 4: 1311–1318.PubMedGoogle Scholar
  55. Irvin, R.T. 1990. Hydrophobicity of proteins and bacterial fimbriae. In: Doyle, R.J. and M. Rosenberg (eds.), Microbial Cell Surface Hydrophobicity. American Society for Microbiology, Washington, pp. 137–177.Google Scholar
  56. Isaacson, R.E. 1980. Factors affecting expression of the Escherichia coli pilus K99. Infect. Immun. 28: 190–194.PubMedGoogle Scholar
  57. 90.
    I Bacterial Adhesion to Cells & TissuesGoogle Scholar
  58. Isaacson, R.E. 1983. Regulation of expression of Escherichia coli pilus K99. Infect. Immun. 40: 633–639.PubMedGoogle Scholar
  59. Ishiguro, E.E., W.W. Kay, T. Ainsworth, J.B. Chamberlain, R.A. Austen, J.T. Buckley, and T.J. Trust. 1981. Loss of virulence during culture of Aeromonas salmonicida at high temperature. J. Bacteriol. 148: 333–340.Google Scholar
  60. James, A.M. 1991. Charge properties of microbial cell surfaces. p. 221–262. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structure and Physicochemical Methods. VCH Publishers, New York, pp. 339–356.Google Scholar
  61. Janda, J.M. and P.S. Duffy. 1988. Mesophilic aeromonads in human disease: current taxonomy, laboratory identification and infection disease spectrum. Rev. Infect. Dis. 10: 980–997.PubMedGoogle Scholar
  62. Janda, J.M., L.S. Oshiro, S.K. Abbott, and P.S. Duffey. 1987. Virulence markers of the mesophilic aeromonads: association of the autoagglutination phenomenon with mouse pathogenicity and the presence of the peripheral cell-associated layer. Infect. Immun. 55: 3070–3077.PubMedGoogle Scholar
  63. Jann, K. and H. Hoschützky. 1990. Nature and organization of adhesins. Curr. Top. Microbiol. Immunol. 151: 55–70.PubMedGoogle Scholar
  64. Jann, K., G. Schmidt, E. Blumenstock, and K. Vosbeck. 1981. Escherichia coli adhesion to Saccharomyces cerevisiae and mammalian cells: role of piliation and surface hydrophobicity. Infect. Immun. 32: 484–489.PubMedGoogle Scholar
  65. Knox, K.W. and A.J. Wicken. 1973. Immunological properties of teichoic acids. Bacteriol. Rev. 37: 215–257.PubMedGoogle Scholar
  66. Koch, A.L., M.L. Higgins, and R.J. Doyle. 1982. The role of surface stress in the morphology of microorganisms. J. Gen. Microbiol. 128: 927–945.PubMedGoogle Scholar
  67. Korhonen, T.K., R. Virkola, B. Westerlund, H. Holthofer, and J. Parkkinen. 1990. Tissue tropism of Escherichia coli adhesins in human extraintestinal infection. Curr. Top. Microbiol. Immunol. 151: 115–127.PubMedGoogle Scholar
  68. Koval, S.F. 1988. Paracrystalline protein surface arrays on bacteria. Can. J. Microbiol. 34: 407–414.Google Scholar
  69. Krell, P.J. and T.J. Beveridge. 1987. The structure of bacteria and molecular biology of viruses. Int. Rev. Cytol. 175: 15–88.Google Scholar
  70. Krogfelt, K.A. 1991. Bacterial adhesion: genetics, biogenesis and role in pathogenesis of fimbrial adhesins of Escherichia coli. Rev. Infect. Dis. 13: 721–735.PubMedGoogle Scholar
  71. Kroncke, K.D., I. Orskov, F. Orskov, B. Jann, and K. Jann. 1990. Electron microscopic study of coexpression of adhesive protein capsules and polysaccharide capsules in Escherichia coli. Infect. Immun. 58: 2710–2714.PubMedGoogle Scholar
  72. Lachica, R.V. 1990. Significance of hydrophobicity in the adhesion of pathogenic Gram-negative bacteria: In: Doyle, R.J. and M. Rosenberg (eds.), Microbial Cell Surface Hydrophobicity: American Society for Microbiology, Washington, pp. 297–313.Google Scholar
  73. Layh-Schmitt, G., S. Schmitt, and T.M. Buchanan. 1989. Interaction of non-pilated Neisseria gonorrhoeae strain 7122 and protein lA with an epithelial cell monolayer. Int. J. Med. Microbiol. 271: 158–170.Google Scholar
  74. Lesher, R.J., G.R. Bender, and R.E. Marquis. 1977. Bacteriolytic action of fluoride ions. Antimicrob. Agents Chemother. 12: 339–345.PubMedGoogle Scholar
  75. Liang, L., D. Drake and R.J. Doyle. 1989. Stability of the glucan-binding lectin of oral streptococci. J. Dent. Res. 68 (Spec. Issue): 1677.Google Scholar
  76. Macnab, R.M. 1989. Motility and chemotaxis. In: Neidhardt, F.C., J.L. Ingraham, K.B. Low, B. Magasanik, M. Schaechter, and H.E. Umbarger (eds.), Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, pp. 732–759.Google Scholar
  77. McCoy, E.C., D. Doyle, K. Burda, L.B. Corbeil, and A.J. Winter. 1975. Superficial antigens of Campylobacter (Vibrio) fetus: characterization of the antiphagocytic component. Infect. Immun. 11: 517–525.PubMedGoogle Scholar
  78. McIntire, F.C., A.E. Vatter, J. Baros, and J. Arnold. 1978. Mechanism of coaggregation between Actinomyces viscosus T14V and Streptococcus sanguis 34. Infect. Immun. 21: 978–988.PubMedGoogle Scholar
  79. McSweegan, E. and R.I. Walker. 1986. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect. Immun. 53: 141–148.PubMedGoogle Scholar
  80. Meyer, T.F. 1990. Variation of pilin and opacity-associated protein in pathogenic Neisseria species. In: Iglewski, B. and V.L. Clark (eds.), Molecular Basis of Bacterial Pathogenesis. Academic Press, San Diego, pp. 137–153.Google Scholar
  81. Mobley, H.L. T., L.K. Jolliffe, and R.J. Doyle. 1983. Cell wall-polypeptide complexes in Bacillus subtilis. Carbohydr. Res. 116: 113–125.Google Scholar
  82. Moon, H. 1990. Colonization factor antigens of enterotoxigenic Escherichia coli in animals. Curr. Topics Microbiol. Immunol. 151: 147–165.Google Scholar
  83. Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.). 1991. Microbial Cell Surface Analysis: Structure and Physicochemical Methods. VCH Publishers, New York.Google Scholar
  84. Nesbitt, W.E., R.H. Staat, B. Rosan, K.G. Taylor, and R.J. Doyle. 1980. Association of proteins with the cell wall of Streptococcus mutans. Infect. Immun. 28: 118–126.PubMedGoogle Scholar
  85. Nikaido, H. and M. Vaara. 1985. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49: 1–32.PubMedGoogle Scholar
  86. Ofek, I., W.A. Simpson, and E.H. Beachey. 1982. Formation of molecular complexes between a structurally defined M protein and acylated or deacylated lipoteichoic acid of Streptococcus pyogenes. J. Bacteriol. 149: 426–433.PubMedGoogle Scholar
  87. Ofek, I., E. Whitnack, and E.H. Beachey. 1983. Hydrophobic interactions of group A streptococci with hexadecane droplets. J. Bacteriol. 154: 139–145.PubMedGoogle Scholar
  88. Old, D.C. and J.P. Duguid. 1970. Selective outgrowth of fimbriate bacteria in static liquid medium. J. Bacteriol. 103: 447–456.PubMedGoogle Scholar
  89. Olsen, A., A. Jonsson, and S. Normark. 1989. Fibronectin binding mediated by a novel class of surface organelles on Escherichia coli. Nature 338: 652–655.PubMedGoogle Scholar
  90. Onderdonk, A.B., N.E. Moon, D.L. Kasper, and J.G. Bartlett. 1978. Adherence of Bacteroides fragilis in vivo. Infect. Immun. 19: 1083–1087.PubMedGoogle Scholar
  91. Orskov, I. and F. Orskov. 1990. Serologic classification of fimbriae. Curr. Top. Microbiol. Immunol. 151: 71–90.PubMedGoogle Scholar
  92. Orskov, I., A. Birch-Anderson, J.P. Duguid, J. Stenderuys, and F. Orskov. 1985. An adhesive protein capsule of Escherichia coli. Infect. Immun. 47: 191–200.PubMedGoogle Scholar
  93. Ottow, J.C. G. 1975. Ecology, physiology and genetics of fimbriae and pili. Annu. Rev. Microbiol. 29: 79–108.PubMedGoogle Scholar
  94. Oudega, B. and F.K. DeGraaf. 1988. Genetic organization and biogenesis of adhesive fimbriae of Escherichia coli. Antonie van Leeuwenhoek 54: 285–299.PubMedGoogle Scholar
  95. Oyston, P.C. and P.S. Handley. 1991. Surface components of Bacteroides fragilis involved in adhesion and hemagglutination. J. Med. Microbiol. 34: 51–55.PubMedGoogle Scholar
  96. Paerregaard, A., F. Espersen, and M. Skurnik. 1991. Role of Yersinia outer membrane protein YadA in adhesion to rabbit intestinal tissue and rabbit intestinal brush border membrane vesicles. APMIS 99: 226–232.PubMedGoogle Scholar
  97. Paranchych, W. 1990. Molecular studies on N-methylphenylalanine pili. In: Iglewski, B. and V.L. Clark (eds.), Molecular Basis of Bacterial Pathogenesis. Academic Press, San Diego, pp. 61–78.Google Scholar
  98. Paranchych, W. and L.S. Frost. 1988. The physiology and biochemistry of pili. Adv. Microbial Physiol. 29: 53–114.Google Scholar
  99. Pearce, W.A. and T.M. Buchanan. 1980. Structure and cell membrane-binding properties of bacterial fimbriae. In: Beachey, E.H. (ed.), Bacterial Adherence (Receptors and Recognition, Vol. 6 ). Chapman and Hall, London, pp. 288–344.Google Scholar
  100. Perry, A. and I. Ofek. 1984. Inhibition of blood clearance and hepatic tissue binding of Escherichia coli by liver lectin-specific sugars and glycoproteins. Infect. Immun. 43: 257–262.PubMedGoogle Scholar
  101. Plummer, D.T., A.M. James, and W.R. Maxted. 1962. Some physical investigations of the behavior of bacterial surfaces. V. The variation of the surface structure of streptococci during growth. Biochim. Biophys. Acta 60: 595–603.PubMedGoogle Scholar
  102. Ramphal, R., C. Gray, and G. Pier. 1987. Pseudomonas aeruginosa adhesins for tracheobronchial mucin. Infect. Immun. 55: 600–603.PubMedGoogle Scholar
  103. Ramphal, R., L. Koo, K.S. Ishimoto, P.A. Totten, J.C. Lara, and S. Lory. 1991. Adhesion of Pseudomonas aeruginosa pilin-deficient mutants to mucin. Infect. Immun. 59: 1307–1311.PubMedGoogle Scholar
  104. Razin, S. 1986. Mycoplasmal adhesins and lectins. In: D. Mirelman (ed.). Microbial Lectins and Agglutinins: Properties and Biological Activity. John Wiley & Sons, New York, pp. 217–235.Google Scholar
  105. Rogers, H.J., H.R. Perkins, and J.B. Ward. 1980. Microbial Cell Walls and Membranes. Chapman and Hall, London.Google Scholar
  106. Rosenberg, M. and R.J. Doyle. 1990. Microbial cell surface hydrophobicity: history, measurement and significance. In: Doyle, R.J. and M. Rosenberg (eds.), Microbial Cell Surface Hydrophobicity. American Society for Microbiology, Washington, pp. 1–37.Google Scholar
  107. by x-ray photoelectron spectroscopy. In: Mozes, N., P.S. Handley, H.J. Busscher, and P.G. Rouxhet (eds.), Microbial Cell Surface Analysis: Structural and Physicochemical Methods. VCH Publishers, New York, pp. 173–220.Google Scholar
  108. Runnels, P.L. and H.W. Moon. 1984. Capsule reduces adherence of enterotopathogenic Escherichia coli to isolated intestinal epithelial cells of pigs. Infect. Immun. 45: 737–740.PubMedGoogle Scholar
  109. Schifferli, D.M. and E.H. Beachey. 1988a. Bacterial adhesion: modulation by antibiotics which perturb protein synthesis. Antimicrob. Agents Chemother. 32: 1603–1608.PubMedGoogle Scholar
  110. Schifferli, D.M. and E.H. Beachey. 1988b. Bacterial adhesion: modulation by antibiotics with primary targets other than protein synthesis. Antimicrob. Agents Chemother. 32: 1609–1613.PubMedGoogle Scholar
  111. Sherman, P., F. Cockerill III, R. Soni, and J. Brunton. 1991. Outer membranes are competitive inhibitors of Escherichia coli 0157:H7 adherence to epithelial cells. Infect. Immun. 59: 890–999.PubMedGoogle Scholar
  112. Sonnenfeld, E.M., T.J. Beveridge, A.L. Koch, and R.J. Doyle. 1985. Asymmetric distribution of charge on the cell wall of Bacillus subtilis. J. Bacteriol. 163: 1167–1171PubMedGoogle Scholar
  113. St. Geme, J.W. III and S. Falkow. 1991. Loss of capsule expression by Hemophilus influenzae type b results in enhanced adherence to and invasion of human cells. Infect. Immun. 59: 1325–1333.Google Scholar
  114. Sutherland, I.W. 1977. Bacterial exopolysaccharides, their nature and production. In: Sutherland, I.W. (ed.), Surface Carbohydrates of the Prokaryotic Cell. Academic Press, London, pp. 27–96.Google Scholar
  115. Swanson, J. 1988. Genetic mechanisms responsible for changes in pilus expression by gonococci. UCLA Symp. Mol. Cell Biol. New Ser. 20: 347–363.Google Scholar
  116. Swanson, J., E. Sparks, D. Young, and G. King. 1975. Studies on gonococcus infection. X. Pili and leukocyte association factor as mediators of interactions between gonococci and eukaryotic cells in vitro. Infect. Immun. 11: 1352–1361.PubMedGoogle Scholar
  117. Tuomanen, E. 1986. Piracy of adhesins: attachment of superinfecting pathogens to respira- tory cilia by secreted adhesins of Bordetella pertussis. Infect. Immun. 54: 905–908.PubMedGoogle Scholar
  118. Tylewska, S. and W. Hryniewicz. 1987. Streptococcus pyogenes cell wall protein responsible for binding to pharyngeal epithelial cells. Zbt. Bakt. Microb. Hyg. A265: 146–150.Google Scholar
  119. Van der Mei, H.C., A.J. Leonard, A.H. Weerkamp, P.G. Rouxhet, and H.J. Busscher. 1988. Surface properties of Streptococcus salivarius HB and nonfibrillar mutants. Measurement of zeta potential and elemental composition with x-ray photoelectron spectroscopy. J. Bacteriol. 170: 2462–2466.PubMedGoogle Scholar
  120. Wentworth, J., F.E. Austin, N. Garber, N. Gilboa-Garber, C. Paterson, and R.J. Doyle. 1991. Cytoplasmic lectins contribute to the adhesion of Pseudomonas aeruginosa. Biofouling 4: 99–104.Google Scholar
  121. Westergren, G. and J. Olsson. 1983. Hydrophobicity and adherence of oral streptococci after repeated subculture in vitro. Infect. Immun. 40: 432–435.PubMedGoogle Scholar
  122. Wright, S.D., S.M. Levine, M.C. T. Jong, Z. Chad, and L.G. Kabbash. 1989. CR3 (CD11b/CD18) expresses one binding site for Arg-Gly-Asp-containing peptides and a second site for bacterial lipopolysaccharide. J. Exp. med. 169: 175–183.PubMedGoogle Scholar

Copyright information

© Chapman & Hall, Inc. 1994

Authors and Affiliations

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

Personalised recommendations