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Identification of a novel lectin inStreptococcus pyogenes and its possible role in bacterial adherence to pharyngeal cells

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Abstract

During investigation of the interaction of human lactoferrin (HLf) with variou bacteria, it was found that inStreptococcus pyogenes, HLf binding occurred to agar-rather than broth-grown cells irrespective of the nutrients used. Furthermore, binding of HLf to broth-grown, heat-killed bacteria was induced by overnight incubation on agar media or short-time exposure of the cells to water-soluble agar extract. The binding pattern was revealed in most of 92S. pyogenes strains representing various M-or T-types with no apparent type variation. The component thus bridging the attachment of HLf to the streptococcal cell surface was recovered in extracts of agar-grown cells and isolated by affinity chromatography on HLf-sepharose. By gel filtration in the presence of radiolabeled HLf, this component exhibited similar elution position as crude water-soluble agar extract. Chemical analysis identified the active HLf-binding agar component to be a galactose-rich polysaccharide (GRP). Further binding tests showed that the interaction between streptococci and GRP was stable in the presence of high molar NaCl, KSCN, or urea and was unaffected by various serum or matrix proteins or by streptococcal lipoteichoic acid; however, a moderate inhibition by heparin or bovine mucin was observed. Studies on isogenic mutants ofS. pyogenes did not support the involvement of M-protein or the hyaluronate capsule in the binding of GRP. SDS-PAGE and Western blot analyses revealed a GRP-binding protein of approximately 70 kDa in the cell-wall extracts of two strains ofS. pyogenes, types M19 and M55. Finally, the adherence of (broth-grown)3H-thymidine-labeledS. pyogenes, type M19, to the pharyngeal epithelial cell line DT-562 or to normal tonsillar epithelial cells was inhibited by GRP in a dose-related manner. We thus propose that the streptococcal GRP-binding component may represent a novel surface lectin acting as a mucosal adhesin forS. pyogenes, in accordance with previous data indicating that galactosecontaining sugar moieties may serve as ligands for the adherence of streptococci to pharyngeal cells. Our results also indicate that GRP-like components such as mucin or heparin might act to block epithelial adherence ofS. pyogenes at the mucosal level.

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Literature Cited

  1. Andersson NS, Dolan TCS, Rees, DA (1965) Evidence for a common structural pattern in the polysaccharide sulphates of the Rhodophyceae. Nature 205:1060–1062

    PubMed  Google Scholar 

  2. Arnold RR, Cole MF, McGhee JR (1977) A bactericidal effect for human lactoferrin. Science 197:263–265

    PubMed  Google Scholar 

  3. Beachey EH (1981) Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surfaces. J Infect Dis 143:325–345

    PubMed  Google Scholar 

  4. Beachey EH, Simpson WA (1982) The adherence of group A streptococci to oropharyngeal cells; the lipoteichoic acid adhesin and fibronectin receptor. Infection 10:107–111

    PubMed  Google Scholar 

  5. Bergey EJ, Stinson ME (1988) Heparin-inhibitable basement membrane-binding protein ofStreptococcus pyogenes. Infect Immun 56:1715–1721

    PubMed  Google Scholar 

  6. Bridson EY (1990) Media in microbiology. Rev. Med Microbiol 1:1–9

    Google Scholar 

  7. Bullen JJ, Rogers HJ, Leigh L (1972) Iron-binding proteins in milk and resistance toEscherichia coli infections in infants. Br Med J 1:69–75

    PubMed  Google Scholar 

  8. Caparon MG, Stephens DS, Olsén A, Scott JR (1991) Role of M protein in adherence of group A streptococci., Infect Immun 59:1811–1817

    PubMed  Google Scholar 

  9. Cheung AL, Fischetti VA (1988) Variation in the expression of cell wall proteins ofStaphylococcus aureus grown on solid and liquid media. Infect Immun 56:1061–1065

    PubMed  Google Scholar 

  10. Cohen JO, Gross, H, Harrell WK (1975) Simple procedure for production by group C streptococci of phage-associated lysin active against group A streptococci. Appl Microbiol 29:175–178

    PubMed  Google Scholar 

  11. Drake D, Taylor KG, Bleiweis AS, Doyle RJ (1988) Specificity of the glucan-binding lectin ofStreptococcus cricetus. Infect Immun 56:1864–1872

    PubMed  Google Scholar 

  12. Ellen RP, Gibbons RJ (1972) “M” protein-associated adherence ofStreptococcus pyogenes to epithelial surfaces: prerequisite for virulence. Infect Immun 5:826–830

    PubMed  Google Scholar 

  13. Fischetti VA (1989) Streptococcal M protein: molecular design and biological behaviour. Clin Microbiol Rev 2:285–314

    PubMed  Google Scholar 

  14. Gibbons RJ, Fitzgerald RJ (1969) Dextran-induced agglutination ofStreptococcus mutans and its potential role in the formation of microbial dental plaques. J Bacteriol 98:341–346

    PubMed  Google Scholar 

  15. Grabovskaya KB, Totolian AA, Ryc M, Havlicek J, Burova LA, Bicova R (1980) Adherence of group A streptococci to epithelial cells in tissue culture. Zentralbl Baktericol Mikrobiol Hyg [A] 247:303–314

    Google Scholar 

  16. Hanski E, Caparon M (1992) Protein F, a fibronectin-binding protein, is an adhesin of the group A streptococcusStreptococcus pyogenes Proc Natl Acad Sci USA 89:6172–6176.

    PubMed  Google Scholar 

  17. Hasty DL, Ofek I, Courtney HS, Doyle RJ (1992) Multiple adhesins of Streptococci. Infect Immun 60:2147–2152

    PubMed  Google Scholar 

  18. Izumi K (1973) Structural analysis of agar-type polysaccharides by NMR spectroscopy. Biochim Biophys Acta 320:311–317

    PubMed  Google Scholar 

  19. Kishore AR, Erdei J, Naidu SS, Falsen E, Forsgren A, Naidu AS (1991) Specific binding of lactoferrin toAeromonas hydrophila. FEMS Microbiol Lett 83:115–120

    Google Scholar 

  20. Kishore AR, Erdei J, Kalfas S, Forsgren A, Naidu AS (1992) Detection of bacterial interaction with lactoferrin by an enzymelinked ligand binding assay (ELBA). J Med Microbiol 37:341–345

    PubMed  Google Scholar 

  21. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  22. Malmquist J, Johansson BG (1971) Interaction of lactoferrin with agar gels and with trypan blue. Biochim Biophys Acta 236:38–46

    PubMed  Google Scholar 

  23. Masson PL, Heremans JF, Dive C (1966) An iron-binding protein common to many extenal secretions. Clin Chim Acta 14:735–739

    Google Scholar 

  24. Mirelman D, Ofek I (1986) Introduction to microbial lectins and agglutinins. In: Mirelman D (ed) Microbial lectins and agglutinins. New York: Johns Wiley & Sons, pp 1–20

    Google Scholar 

  25. Naidu AS, Jimenez J Aleljung P, Nilsson-Ehle P, Larsson L, Hedström SÅ (1989) Crystal violet binding, cell surface properties and extracellular enzyme profiles ofStaphylococcus aureus producing toxic shock, syndrome toxin-1. Zentralbl Bakteriol 271:11–21

    PubMed  Google Scholar 

  26. Naidu AS, Miedzobrodzki J, Andersson M, Nilsson L-E, Forsgren A, Watts JL (1990) Bovine lactoferrin binding to six species of coagulase-negative staphylococci isolated from bovine intramammary infections. J Clin Microbiol 28:2312–2319

    PubMed  Google Scholar 

  27. Naidu SS, Erdei J, Czirók É, Kalfas S, Gadó I, Thorén A, Forsgren A, Naidu AS (1991) Specific binding of lactoferrin toEscherichia coli isolated from human intestinal infections. APMIS 99:1142–1150

    PubMed  Google Scholar 

  28. Naidu AS, Andersson M, Forsgren A (1992) Identification of a human lactoferrin-binding protein inStaphylococcus, aureus. J Med Microbiol 36:177–183

    PubMed  Google Scholar 

  29. Nakamura RM, Voller A, Bidwell DE (1986) Enzyme immunoassays: heterogeneous and homogeneous systems. In: Weir DM (ed) Handbook of experimental immunology. Oxford: Blackwell Scientific Publications, pp 27.1–27.20

    Google Scholar 

  30. Reiter B, Oram JD (1967) Bacterial inhibitors in milk and other biological fluids. Nature 216:328–330

    PubMed  Google Scholar 

  31. Rejman JJ, Hegarty HM, Hurley WL (1989) Purification and characterization of bovine lactoferrin from secretions of the involuting mammary gland: identification of multiple molecular weight forms. Comp Biochem Physiol [B] 93:929–934

    Google Scholar 

  32. Roussel P, Lamblin G, Lhermitte M, Houdret N, Lefitte JJ, Perini JM, Klein A, Scharfman A (1988) The complexity of mucins. Biochimie 70:1471–1482

    PubMed  Google Scholar 

  33. Sawardeker JS, Sloneker HH, Jeanes A (1965) Quantitative determination of monosaccharides as their alditol acetates by gas-liquid chromatography. Anal Biochem 37:1602–1604

    Google Scholar 

  34. Schryvers AB (1989) Identification of the transferrin-and lactoferrin-binding proteins inHaemophilus influenzae. J Med Microbiol 29:121–130

    PubMed  Google Scholar 

  35. Schryvers AB, Morris LJ (1988) Identification and characterization of the human lactoferrin-binding protein fromNeisseria meningitidis. Infect Immun 56:1144–1149

    PubMed  Google Scholar 

  36. Selinger DS, Julie N, Reed WP, Williams Jr RC (1978) Adherence of group A streptococci to pharyngeal cells: a role in the pathogenesis of rheumatic fever. Science 201:455–457

    PubMed  Google Scholar 

  37. Spanier JG, Cleary PP (1980) Bacteriophage control of antiphagocytic determinants in group A streptococci. J Exp Med 152:1393–1406

    PubMed  Google Scholar 

  38. Stáhl S, Stjernquist-Desatnik A, Schalén C, Gebreselassie D (1992) Role of hyaluronic acid capsule and M-protein for the virulence ofStreptococcus pyogenes, type M50., In: Orefici G (ed) New perspectives on Streptococci and streptococcal infections. Zentralbl Bakteriol Suppl 22:440–441

  39. Stollerman GH (1975) Rheumatic fever and streptococcal infection. New York: Grune and Stratton, pp 47–62

    Google Scholar 

  40. Talay SR, Ehrenfeld E, Chhatwal GS, Timmis KN (1991) Expression of the fibronectin-binding components ofStreptococus pyogenes inEscherichia coli demonstrates that they are proteins. Mol Microbiol 5:1727–1734

    PubMed  Google Scholar 

  41. Tigyi Z, Kishore AR, Maeland JA, Forsgren A, Naidu AS (1992) Lactoferrin-binding proteins inShigella flexneri. Infect Immun 60:2619–2626

    PubMed  Google Scholar 

  42. Towbin H, Stachelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitro cellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354

    PubMed  Google Scholar 

  43. Tylewska SK, Fischetti VA, Gibbons RJ (1988) Binding selectivity ofStreptococcus pyogenes and M protein to epithelial cells differs from that of lipoteichoic acid. Curr Microbiol 16:209–216

    Google Scholar 

  44. Wadström T, S Tylewska T (1982) Glycoconjugates as possible receptors forStreptococcus pyogenes. Curr Microbiol 7:343–346

    Google Scholar 

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Authors and Affiliations

  1. Department of Medical Microbiology, Malmö General Hospital, University of Lund, Malmö, Sweden

    D. Gerlach, Z. Tigyi, A. Forsgren & A. S. Naidu

  2. Institute of Experimental Microbiology, Jena, Germany

    D. Gerlach

  3. Department of Medical Microbiology, Sölvegatan 23, S22362, Lund, Sweden

    C. Schalén

  4. BioCarb Technology AB, Lund, Sweden

    B. Nilsson

Authors
  1. D. Gerlach
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  2. C. Schalén
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  3. Z. Tigyi
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  4. B. Nilsson
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  5. A. Forsgren
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  6. A. S. Naidu
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Gerlach, D., Schalén, C., Tigyi, Z. et al. Identification of a novel lectin inStreptococcus pyogenes and its possible role in bacterial adherence to pharyngeal cells. Current Microbiology 28, 331–338 (1994). https://doi.org/10.1007/BF01570197

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