Interactions of Bacterial Adhesins with the Extracellular Matrix

  • Åsa Ljungh
  • Torkel Wadström
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 408)


The role of microbial adhesion to epithelia in mucosa-associated infections has been recognized for a long time. The discovery by Kuusela in 197823 that Staphylococcus aureus strains specifically bind the extracellular matrix (ECM) and plasma glycoprotein fibronectin, Fn, launched a broad field of research on (i) how microbes, i.e. bacteria, parasites, fungi and viruses, interact with ECM components, and (ii) the role of interaction with these subepithelial structures in the pathogenesis of various infectious diseases30. We will here describe some of these interactions, and emphasize some possible targets for anti-adhesion therapy.


Bacterial Adhesion Microbial Adhesion Biomaterial Surface Basement Membrane Protein Fibronectin Binding 
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  1. 1.
    Adams, J. C. and J. Lawler. 1993. The thrombospondin family. Curr. Biol. 3:188–190.PubMedCrossRefGoogle Scholar
  2. 2.
    Aleljung, P., W. Shen, B. Rozalska, U. Hellman, Å. Ljungh, and T. Wadström. 1994. Purification of collagen binding proteins of Lactobacillus reuteri. Curr. Microbiol. 28:231–236.PubMedCrossRefGoogle Scholar
  3. 3.
    Arvidson, S., L. Janzon and S. Löfdahl. 1990. The role of the δ-lysin gene (hid) in the ögr-dependent regulation of exoprotein synthesis in Staphylococcus aureus, p. 421–433. In R. P. Novick. (ed.), Molecular Biology of the Staphylococci. VCH Publ, New York.Google Scholar
  4. 4.
    Ascencio, F., H.-A. Hansson, O. Larm, and T. Wadström. 1995. Helicobacter pylori interacts with heparin and heparin-dependent growth factors. FEMS Immunol. Med. Microbiol. 12:265–272.PubMedCrossRefGoogle Scholar
  5. 5.
    Ascencio, F., O. D. Liang, L.-Ä. Fransson, and T. Wadström. 1993. Affinity of the gastric pathogen Helicobacter pylori for the N-sulphated glycosaminoglycan heparan sulphate. J.Med.Microbiol. 38:240- 244.CrossRefGoogle Scholar
  6. 6.
    Bazzoni, G., A. B. Nunez, G. Mascellani, P. Bianchini, E. Dejana, and A. Del Maschio. 1993. Effect of heparin, dermatan sulfate, and related oligo-derivatives on human polymorphonuclear leukocyte functions. J. Lab. Clin. Med. 121:268–275.PubMedGoogle Scholar
  7. 7.
    Berge, A. and U. Sjöbring. 1993. PAM, a novel plasminogen-binding protein from Streptococcus pyogenes. J. Biol. Chem. 268:25417–25424.PubMedGoogle Scholar
  8. 8.
    Carlsson Wistedt, A., U. Ringdahl, W. Müller-Esterl, and U. Sjöbring. 1995. Identification of a plasminogen-binding motif in PPAM, a bacterial surface protein. Molec. Microbiol. 18:569–578.CrossRefGoogle Scholar
  9. 9.
    Evans, D. G., D. J. Evans,Jr, J. J. Mouls, and D. Y. Graham. 1988. N-acetylneuraminyllactose-binding fibrillar hemagglutinin of Campylobacter pylori: a putative colonization factor antigen. Infect. Immun. 56:2896–2906.PubMedGoogle Scholar
  10. 10.
    Fabrizius-Homan, D. J. and S. L. Cooper. 1991. Competitive adsorption of vitronectin with albumin, fibrinogen and fibronectin on polymeric biomaterials. J. Biomed. Mat. Res. 25:953–971.CrossRefGoogle Scholar
  11. 11.
    Flock, J.-I., S. A. Hienz, A. Heimdahl, and T. Schennings. 1996. Reconsideration of the role for fibronectin binding in endocarditis caused by Staphylococcus aureus. Infect. Immun, in press.Google Scholar
  12. 12.
    Gaffney, P. R., J. J. O’Leary, C. T. Doyle, A. Gaffney, J. Hogan, F. Smew, and P. Annis. 1991. Response to heparin in patients with ulcerative colitis. Lancet 337:238–239.PubMedCrossRefGoogle Scholar
  13. 13.
    Gatermann, S. and H.-G. W. Meyer. 1994. Staphylococcus saprophyticus hemagglutinin binds fibronectin. Infect. Immun. 62:4556–4563.PubMedGoogle Scholar
  14. 14.
    Gristina, A. G. 1987. Biomaterial-centered infection: Microbial adhesion versus tissue integration. Science 237:1588–1595.PubMedCrossRefGoogle Scholar
  15. 15.
    Herrmann, M., S. J. Suchard, L. A. Boxer, F. A. Waldvogel, and P. D. Lew. 1991. Thrombospondin binds to Staphylococcus aureus and promotes staphylococcal adherence to surfaces. Infect. Immun. 59:279–288.PubMedGoogle Scholar
  16. 16.
    Hirmo, S., S. Keim, R. Schauer, B. Nilsson, and T. Wadström. 1996. Adhesion of Helicobacter pylori strains to a-2,3-linked sialic acids. Glycoconjugate J, in press.Google Scholar
  17. 17.
    Hirmo, S., M. Utt, M. Ringner, and T. Wadström. 1995. Inhibition of heparan sulphate and other glycosaminoglycans binding to Helicbacter pylori by various polysulphated carbohydrates. FEMS Immunol. Med. Microbiol. 10:301–306.PubMedCrossRefGoogle Scholar
  18. 18.
    Höök, M., L. M. Switalski, T. Wadström and M. Lindberg. 1989. Interactions of pathogenic microorganisms with fibronectin. p. 295–308. In D. F. Mosher. (ed.), Fibronectin. Academic Press, San Diego.Google Scholar
  19. 19.
    Jönsson, K., C. Signäs, H.-P. Müller, and M. Lindberg. 1991. Two different genes encode fibronectin- binding proteins in Staphylococcus aureus. The complete nucleotide sequence and characterization of a second gene. Eur. J. Biochem. 292:1041–1048.CrossRefGoogle Scholar
  20. 20.
    Korhonen, T. K., R. Virkola, K. Lähteenmäki, Y. Björkman, M. Kukkonen, T. Raunio, A.-M. Tarkkanen, and B. Westerlund. 1992. Penetration of fimbriate enteric bacteria through basement membranes: A hypothesis. FEMS Microbiol. Immunol. 100:3072–3125.Google Scholar
  21. 21.
    Kreis, T. and R. Vale. 1993. Guidebook to the Extracellular Matrix and adhesion proteins. Oxford University Press, Oxford, New York and Tokyo.Google Scholar
  22. 22.
    Kukkonen, M., T. Raunio, R. Virkola, K. Lähteenmäki, P. H. Mäkelä, B. Westerlund, and T. K. Korhonen. 1993.Basement membrane carbohydrate as a target for bacterial adhesion: binding of type I fimbriae of Salmonella enterica and Escherichia coli to laminin. Molec. Microbiol. 7:229–237.CrossRefGoogle Scholar
  23. 23.
    Kuusela, P. 1978. Fibronectin binds to Staphylococcus aureus. Nature 276:718–720.PubMedCrossRefGoogle Scholar
  24. 24.
    Kuusela, P., S.-F. Kaukoranta-Tolvanen, M. Ullberg, G. Kronvall and O. Saksela. 1994. Surface associated activation of plasminogen on staphylococci and streptococci, and novel mechanisms for bacteriemia to use the activator system of the host. p. 97–102. In T. Wadström, I. A. Holder, and G. Kronvall. (ed.), Molecular pathogenesis of surgical infections. Gustav Fischer Verlag, Stuttgart.Google Scholar
  25. 25.
    Kuypers, J. M. and R. A. Proctor. 1989. Reduced adherence to traumatized rat heart valves by a low fibronectin-binding mutant of Staphylococcus aureus. Infect. Immun. 57:2306–2312.PubMedGoogle Scholar
  26. 26.
    Lelwala-Guruge, J., F. Ascencio, A. S. Kreger, Å. Ljungh, and T. Wadström. 1993. Isolation of a sialic acid-specific surface hemagglutinin of Helicobacter pylori strain NCTC 11637. Zbl Bakt 280:93–106.Google Scholar
  27. 27.
    Liang, O. D., F. Ascencio, L.-Ä. Fransson, and T. Wadström. 1992. Binding of heparan sulfate to Staphylococcus aureus. Infect. Immun. 60:899–906.PubMedGoogle Scholar
  28. 28.
    Liang, O. D., F. Ascencio, R. Vazquez-Juarez, and T. Wadström. 1993. Binding of collagen, fibronectin, lactoferrin, laminin, vitronectin and heparan sulfate to Staphylococcus aureus strain V8 at various growth phases and under nutrient stress conditions. Zbl Bakt 279:180–190.Google Scholar
  29. 29.
    Ljungh, Å., T. Kronevi and T. Wadström. 1990. Fibronectin-substituted gels for treatment of experimental wound infections in a pig model, p. 163–168. In T. Wadström, I. Eliasson, I. A. Holder, and Å. Ljungh. (ed.), Pathogenesis of wound and biomaterial-associated infections. Springer Verlag, London.Google Scholar
  30. 30.
    Ljungh, Å. and T. Wadström. 1995. Binding of extracellular matrix proteins by microbes, p. 501–514. In R. J. Doyle and I. Ofek. (ed.), Methods of Enzymology. Microbial adhesion. Academic Press, New York.CrossRefGoogle Scholar
  31. 31.
    Lottenberg, R., D. Minning-Wenz, and M. D. R Boyle. 1994. Capturing host plasmin(ogen): a common mechanism for invasive pathogens? Trends Microbiol 2:20–24.PubMedCrossRefGoogle Scholar
  32. 32.
    Lowrance, J. H., L. M. Baddour, and W. A. Simpson. 1990. The role of fibronectin binding in the rat model of experimental endocarditis caused by Streptococcus sanguis. J. Clin. Invest. 86:7–13.PubMedCrossRefGoogle Scholar
  33. 33.
    Mamo, W., P. Jonsson, J.-I. Flock, M. Lindberg, H.-P. Muller, T. Wadström, and L. Nelson. 1994. Vaccination against Staphylococcus aureus mastitis: immunological response of mice vaccinated with fibronectin-binding protein (FnBP-A) to challenge with S.aureus. Vaccine 12:988–992.PubMedCrossRefGoogle Scholar
  34. 34.
    Marshall, K. C. 1992. Biofilms: An overview of bacterial adhesion, activity, and control at surfaces. ASM News 58:202–207.Google Scholar
  35. 35.
    McDevitt, D., P. Francois, P. Vaudaux, and T. J. Foster. 1994. Molecular characterization of the clumping factor (fibrinogen receptor) of Staphylococcus aureus. Molec. Microbiol. 11:237–248.CrossRefGoogle Scholar
  36. 36.
    Modun, B., P. Williams, W. J. Pike, A. Cockayne, J. P. Arbuthnott, R. Finch, and S. P. Denyer. 1992. Cell envelope proteins of Staphylococcus epidermidis grown in vivo in a peritoneal chamber implant. Infect. Immun. 60:2551–2553.PubMedGoogle Scholar
  37. 37.
    Pascu, C., S. Hirmo, A. Ljungh, and T. Wadström. 1995. Inhibition of extracellular matrix and serum protein binding to Staphylococcus aureus by heparin and various polysulphated agents. Med. Microbiol. Lett. 4:397–405.Google Scholar
  38. 38.
    Pascu, C., Å. Ljungh, and T. Wadström. 1996. Staphylococci bind heparin-binding host growth factors. Curr. Microbiol. 32:000–000.CrossRefGoogle Scholar
  39. 39.
    Patti, J. M., B. L. Allen, M. J. McGavin, and M. Höök. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annual Review of Microbiology 48:585–617.PubMedCrossRefGoogle Scholar
  40. 40.
    Patti, J. M., T. Bremell, D. Krajewska-Pietrasik, A. Abdelnour, A. Tarkowski, C. Ryden, and M. Höök. 1994.The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect. Immun. 62:152–161.PubMedGoogle Scholar
  41. 41.
    Patti, J. M., H. Jonsson, B. Guss, L. M. Switalski, K. Wiberg, M. Lindberg, and M. Hook. 1992. Molecular characterization and expression of a gene encoding a Staphylococcus aureus collagen adhesive protein. J. Biol. Chem. 267:4766–4772.PubMedGoogle Scholar
  42. 42.
    Paulsson, M., I. Gouda, O. Larm, and Å. Ljungh. 1994. Adherence of coagulase-negative staphylococci to heparin and other glycosaminoglycans immobilized on polymer surfaces. J. Biomed. Mat. Res. 28:311–317.CrossRefGoogle Scholar
  43. 43.
    Paulsson, M., M. Kober, C. Freij-Larsson, M. Stollenwerk, B. Wesslen, and Å. Ljungh. 1993. Adhesion of staphylococci to chemically modified and native polymers and the influence of preadsorbed fi- bronectin, vitronectin and fibrinogen. Biomaterials 14:845–853.PubMedCrossRefGoogle Scholar
  44. 44.
    Paulsson, M., Å. Ljungh, and T. Wadstrom. 1992. Rapid identification of fibronectin, vitronectin, laminin and collagen cell surface binding proteins on coagulase-negative staphylococci by particle agglutination assays. J. Clin. Microbiol. 30:2006–2012.PubMedGoogle Scholar
  45. 45.
    Pekna, M., R. Larsson, B. Formgren, U. R. Nilsson, and B. Nilsson. 1993. Complement activation by polymethylmethacrylate minimized by end-point heparin attachment. Biomaterials 14:189–192.PubMedCrossRefGoogle Scholar
  46. 46.
    Peters, G., R. Locci, and G. Pulverer. 1982. Adherence and growth of coagulase-negative staphylococci on surfaces of intravascular catheters. J. Infect. Dis. 146:479–482.PubMedCrossRefGoogle Scholar
  47. 47.
    Ringner, M., K. H. Valkonen, and T. Wadstrom. 1994. Binding of vitronectin and plasminogen to Helicobacter pylori. FEMS Microbiol. Immunol. 9:29–34.Google Scholar
  48. 48.
    Rozalska, B. and T. Wadstrom. 1993. Protective opsonic activity of antibodies against fibronectin-binding proteins (FnBPs) of Staphylococcus aureus. Scand. J. Immunol. 37:575–580.PubMedCrossRefGoogle Scholar
  49. 49.
    Sakata, N., B. Rozalska, and T. Wadstrom. 1994. Immunological recognition of fibronectin-binding proteins of Staphylococcus aureus and Staphylococcus capitis, strain LK499. Microbiol. Immunol. 38:359–366.PubMedGoogle Scholar
  50. 50.
    Schierholz, J., B. Jansen, L. Jaenicke, and G. Pulverer. 1994. In-vitro efficacy of an antibiotic releasing silicone ventricle catheter to prevent shunt infection. Biomaterials 15:996–1000.PubMedCrossRefGoogle Scholar
  51. 51.
    Schulze-Koops, H., H. Burkhardt, J. Heesemann, T. Kirsch, B. Swoboda, C. Bull, S. Goodman, and F. Emmrich. 1993. Outer membrane protein YadA of enteropathogenic Yersinias mediates specific binding to cellular but not plasma fibronectin. Infect. Immun. 61:2513–2519.PubMedGoogle Scholar
  52. 52.
    Shen, W., H. Steinriick, and Å. Ljungh. 1995. Expression of binding of plasminogen, thrombospondin, vitronectin, and fibrinogen, and adhesive properties by Escherichia coli strains isolated from patients with colonic diseases. Gut 36:401–406.PubMedCrossRefGoogle Scholar
  53. 53.
    Sjobring, U., G. Pohl, and A. Olsen. 1994. Plasminogen, adsorbed by Escherichia coli expressing curli or by Salmonella enteritidis expressing thin aggregative fimbriae, can be activated by simultaneously captured tissue-type plasminogen activator (t-PA). Molec. Microbiol. 14:443–452.CrossRefGoogle Scholar
  54. 54.
    Slomiany, B. L., V. L. N. Murty, J. Piotrowski and A. Slomiany. 1994. Effects of antiulcer agents on the physicochemical properties of gastric mucus, p. 179–192. In E. Chantler and N. A. Ratcliffe. (ed.), Mucus and related topics. Soc Experim Biol, Cambridge.Google Scholar
  55. 55.
    Slomiany, B. L., J. Piotrowski, S. Sengupta, and A. Slomiany. 1991. Inhibition of gastric mucosal laminin receptor by Helicobacter pylori lipopolysaccharide. Biochem. Biophys. Res. Commun. 175:963–970.PubMedCrossRefGoogle Scholar
  56. 56.
    Sodeinde, O., Y. Subrahmanyam, K. Stark, T. Quan, Y. Bao, and J. Goguen. 1992. A surface protease and the invasive character of plague. Science 258:1004–1007.PubMedCrossRefGoogle Scholar
  57. 57.
    Switalski, L. M., J. M. Patti, W. Butcher, A. G. Gristina, P. Speziale, and M. Höök. 1993. A collagen receptor on Staphylococcus aureus strains isolated from patients with septic arthritis mediates adhesion to cartilage. Molec. Microbiol. 7:99–107.CrossRefGoogle Scholar
  58. 58.
    Toba, T., R. Virkola, B. Westerlund, Y. Bjorkman, J. Sillanpaa, T. Vartio, N. Kalkkinen, and T. K. Korhonen. 1995. A collagen-binding S-layer protein in Lactobacillus crispatus. Appl. Environm. Microbiol. 61:2467–2471.Google Scholar
  59. 59.
    Trust, T. J., P. Doig, L. Emödy, Z. Kienle, T. Wadström, and P. O’Toole. 1991. High-affinity binding of the basement membrane proteins collagen type IV and laminin to the gastric pathogen Helicobacter pylori. Infect. Immun. 59:4398–4404.PubMedGoogle Scholar
  60. 60.
    Tyrrell, D. J., S. Kilfeather, and C. P. Page. 1996. Therapeutic uses of heparin beyond its traditional role as an anticoagulant. Trends in Polysaccharide Science 16:198–204.CrossRefGoogle Scholar
  61. 61.
    Valkonen, K. H., M. Ringner, Å. Ljungh, and T. Wadströom. 1993. High-affinity binding of laminin by Helicobacter pylori: Evidence for a lectin-like interaction. FEMS Immunol. Med. Microbiol. 7:29–38.Google Scholar
  62. 62.
    Valkonen, K. H., T. Wadstrom, and A. P. Moran. 1994. Interaction of lipopolysaccharide of Helicobacter pylori with basement membrane protein laminin. Infect. Immun. 62:3640–3648.PubMedGoogle Scholar
  63. 63.
    Vaudaux, P., D. Pittet, A. Haeberli, P. G. Lerch, J.-J. Morgenthaler, R. A. Proctor, F. A. Waldvogel, and D. P. Lew. 1993. Fibronectin is more active than fibrin or fibrinogen in promoting Staphylococcus aureus adherence to inserted intravascular catheters. J. Infect. Dis. 167:633–641.PubMedCrossRefGoogle Scholar
  64. 64.
    Virkola, R., J. Parkkinen, J. Hacker, and T. K. Korhonen. 1993. Sialyloligosaccharide chains of laminin as an extracellular matrix target for S fimbriae of Escherichia coli. Infect. Immun. 61:4480–4484.PubMedGoogle Scholar
  65. 65.
    Wadström, T. 1995. An update on Helicobacter pylori. Current Science 11:69–75.Google Scholar
  66. 66.
    Wadström, T., S. Hirmo, and T. Boren. 1996. Biochemical aspects of Helicobacter pylori colonization of the human gastric mucosa. Alimentary Pharmacology and Therapy 10:in pressGoogle Scholar
  67. 67.
    Wadström, T., M. Paulsson and Å. Ljungh. 1994. Molecular pathogenesis of staphylococcal infections: Microbial adhesion to extracellular matrix and colonization of wounded tissues and biomaterial surfaces, p. 343–352. In R. Möllby, J.-I. Flock, C. E. Nord, and B. Christensson. (ed.), Staphylococcal Infections. Gustav Fischer Verlag, Stuttgart.Google Scholar
  68. 68.
    Wadström, T., J. Rydberg, B. Rozalska, and J. Lelwala-Guruge. 1994. Intravenous Helicobacter pylori induces low levels of TNF-α and IL-lα in a murine model. APMIS 102:49–52.PubMedCrossRefGoogle Scholar
  69. 69.
    Westerlund, B., I. van Die, C. Kramer, P. Kuusela, H. Holthöfer, A.-M. Tarkkanen, R. Virkola, N. Riegman, H. Bergmans, W. Hoekstra, and T. K. Korhonen. 1991. Multifunctional nature of P fimbriae of uropatho- genic Escherichia coli’, mutations in fsoE and fsoF influence fimbrial binding to renal tubuli and immobilized fibronectin. Molec. Microbiol. 5:2965–2975.CrossRefGoogle Scholar
  70. 70.
    Yu, J., R. Andersson, L.-Q. Wang, S. Bengmark, and Å. Ljungh. 1995. Fibronectin on the surface of biliary drain materials - a role in bacterial adherence. J. Surg. Res. 59:000–000.CrossRefGoogle Scholar
  71. 71.
    Yu, J., M. Nordman-Montelius, M. Paulsson, I. Gouda, O. Larm, L. Montelius, and Å. Ljungh. 1994. Adhesion of coagulase-negative Staphylococci and adsorption of plasma proteins to heparinized polymer surfaces. Biomaterials 15:805–814.PubMedCrossRefGoogle Scholar
  72. 72.
    Yu, J. L., R. Andersson, and Å. Ljungh. 1995. Protein adsorption and bacterial adhesion to biliary stent materials. J Surg Res, in press.Google Scholar

Copyright information

© Plenum Press, New York 1996

Authors and Affiliations

  • Åsa Ljungh
    • 1
  • Torkel Wadström
    • 1
  1. 1.Department of Medical MicrobiologyLund UniversityLundSweden

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