1887

Abstract

is found in biofilms on teeth and as a commensal member of the gastrointestinal and urinary floras, but may also be associated with deep-seated purulent infections and infective endocarditis. produces hyaluronidase, an enzyme that breaks down hyaluronan (HA), a major component of the extracellular matrix of connective tissue. We investigated the involvement of hyaluronidase in biofilm formation and dispersal as well as adhesion to human cells. The hyaluronidase activity and expression of the gene were higher in growth media supplemented with HA. Inactivation of the hyaluronidase resulted in a mutant that formed up to 31 % more biofilm in media supplemented with HA. Hyaluronidase added to the medium caused dispersal of biofilm. Adhesion to epithelial cells was similar in the wild-type and the hyaluronidase mutant. We concluded that hyaluronidase may be important for detachment from biofilms but not for adhesion to epithelial cells. The ability of to detach from the surface and to spread may be crucial in the pathogenicity of this micro-organism.

Keyword(s): HA, hyaluronan
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2008-03-01
2024-03-29
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References

  1. Agren U. M., Tammi M., Ryynanen M., Tammi R. 1997; Developmentally programmed expression of hyaluronan in human skin and its appendages. J Invest Dermatol 109:219–224
    [Google Scholar]
  2. Aoki K., Matsumoto S., Hirayama Y., Wada T., Ozeki Y., Niki M., Domenech P., Umemori K., Yamamoto S. other authors 2004; Extracellular mycobacterial DNA-binding protein 1 participates in mycobacterium–lung epithelial cell interaction through hyaluronic acid. J Biol Chem 279:39798–39806
    [Google Scholar]
  3. Asteriou T., Deschrevel B., Delpech B., Bertrand P., Bultelle F., Merai C., Vincent J. C. 2001; An improved assay for the N -acetyl-d-glucosamine reducing ends of polysaccharides in the presence of proteins. Anal Biochem 293:53–59
    [Google Scholar]
  4. Bowden G. H., Li Y. H. 1997; Nutritional influences on biofilm development. Adv Dent Res 11:81–99
    [Google Scholar]
  5. Branda S. S., Vik S., Friedman L., Kolter R. 2005; Biofilms: the matrix revisited. Trends Microbiol 13:20–26
    [Google Scholar]
  6. Camenisch T. D., Spicer A. P., Brehm-Gibson T., Biesterfeldt J., Augustine M. L., Calabro A. Jr, Kubalak S., Klewer S. E., McDonald J. A. 2000; Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme. J Clin Invest 106:349–360
    [Google Scholar]
  7. Claridge J. E. III, Attorri S., Musher D. M., Hebert J., Dunbar S. 2001; Streptococcus intermedius , Streptococcus constellatus , and Streptococcus anginosus (“ Streptococcus milleri group”) are of different clinical importance and are not equally associated with abscess. Clin Infect Dis 32:1511–1515
    [Google Scholar]
  8. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M. 1995; Microbial biofilms. Annu Rev Microbiol 49:711–745
    [Google Scholar]
  9. Costerton J. W., Stewart P. S., Greenberg E. P. 1999; Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322
    [Google Scholar]
  10. Fallgren C., Andersson A., Ljungh A. 2001; The role of glycosaminoglycan binding of staphylococci in attachment to eukaryotic host cells. Curr Microbiol 43:57–63
    [Google Scholar]
  11. Feldman C., Cockeran R., Jedrzejas M. J., Mitchell T. J., Anderson R. 2007; Hyaluronidase augments pneumolysin-mediated injury to human ciliated epithelium. Int J Infect Dis 11:11–15
    [Google Scholar]
  12. Girish K. S., Kemparaju K. 2007; The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci 80:1921–1943
    [Google Scholar]
  13. Gossling J. 1988; Occurrence and pathogenicity of the Streptococcus milleri group. Rev Infect Dis 10:257–285
    [Google Scholar]
  14. Hamada S., Slade H. D. 1980; Biology, immunology, and cariogenicity of Streptococcus mutans . Microbiol Rev 44:331–384
    [Google Scholar]
  15. Hashioka K., Suzuki K., Yoshida T., Nakane A., Horiba N., Nakamura H. 1994; Relationship between clinical symptoms and enzyme-producing bacteria isolated from infected root canals. J Endod 20:75–77
    [Google Scholar]
  16. Homer K., Shain H., Beighton D. 1997; The role of hyaluronidase in growth of Streptococcus intermedius on hyaluronate. Adv Exp Med Biol 418:681–683
    [Google Scholar]
  17. Homer K. A., Roberts G., Byers H. L., Tarelli E., Whiley R. A., Philpott-Howard J., Beighton D. 2001; Mannosidase production by viridans group streptococci. J Clin Microbiol 39:995–1001
    [Google Scholar]
  18. Hynes W. L., Walton S. L. 2000; Hyaluronidases of Gram-positive bacteria. FEMS Microbiol Lett 183:201–207
    [Google Scholar]
  19. Itoh Y., Wang X., Hinnebusch B. J., Preston J. F. III, Romeo T. 2005; Depolymerization of β -1,6- N -acetyl-d-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol 187:382–387
    [Google Scholar]
  20. Kaplan J. B., Ragunath C., Ramasubbu N., Fine D. H. 2003; Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous β -hexosaminidase activity. J Bacteriol 185:4693–4698
    [Google Scholar]
  21. King S. J., Allen A. G., Maskell D. J., Dowson C. G., Whatmore A. M. 2004; Distribution, genetic diversity, and variable expression of the gene encoding hyaluronate lyase within the Streptococcus suis population. J Bacteriol 186:4740–4747
    [Google Scholar]
  22. Last K. S., Embery G. 1987; Hyaluronic acid and hyaluronidase activity in gingival exudate from sites of acute ulcerative gingivitis in man. Arch Oral Biol 32:811–815
    [Google Scholar]
  23. Nyberg A., Engstrom-Laurent A., Loof L. 1988; Serum hyaluronate in primary biliary cirrhosis – a biochemical marker for progressive liver damage. Hepatology 8:142–146
    [Google Scholar]
  24. Okayama H., Nagata E., Ito H. O., Oho T., Inoue M. 2005; Experimental abscess formation caused by human dental plaque. Microbiol Immunol 49:399–405
    [Google Scholar]
  25. Petersen F. C., Pasco S., Ogier J., Klein J. P., Assev S., Scheie A. A. 2001; Expression and functional properties of the Streptococcus intermedius surface protein antigen I/II. Infect Immun 69:4647–4653
    [Google Scholar]
  26. Petersen F. C., Pecharki D., Scheie A. A. 2004; Biofilm mode of growth of Streptococcus intermedius favored by a competence-stimulating signaling peptide. J Bacteriol 186:6327–6331
    [Google Scholar]
  27. Pfaffl M. W., Horgan G. W., Dempfle L. 2002; Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36
    [Google Scholar]
  28. Piscitelli S. C., Shwed J., Schreckenberger P., Danziger L. H. 1992; Streptococcus milleri group: renewed interest in an elusive pathogen. Eur J Clin Microbiol Infect Dis 11:491–498
    [Google Scholar]
  29. Pogrel M. A., Lowe M. A., Stern R. 1996; Hyaluronan (hyaluronic acid) in human saliva. Arch Oral Biol 41:667–671
    [Google Scholar]
  30. Reissig J. L., Storminger J. L., Leloir L. F. 1955; A modified colorimetric method for the estimation of N -acetylamino sugars. J Biol Chem 217:959–966
    [Google Scholar]
  31. Rovelstad G. H., Geller J. H., Cohen A. H. 1958; The hyaluronidase activity of saliva. II. The relationship of hyaluronidase activity to dental caries experience, gingivitis, and oral hygiene in young male adults. J Dent Res 37:114–118
    [Google Scholar]
  32. Ruoslahti E. 1996; Brain extracellular matrix. Glycobiology 6:489–492
    [Google Scholar]
  33. Shain H., Homer K. A., Beighton D. 1996; Purification and properties of a novel glycosaminoglycan depolymerase from Streptococcus intermedius strain UNS 35. J Med Microbiol 44:381–389
    [Google Scholar]
  34. Smith A. J., Addy M., Embery G. 1995; Gingival crevicular fluid glycosaminoglycan levels in patients with chronic adult periodontitis. J Clin Periodontol 22:355–361
    [Google Scholar]
  35. Starr C. R., Engleberg N. C. 2006; Role of hyaluronidase in subcutaneous spread and growth of group A streptococcus. Infect Immun 74:40–48
    [Google Scholar]
  36. Sutherland I. W. 2001; The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol 9:222–227
    [Google Scholar]
  37. Tao L., LeBlanc D. J., Ferretti J. J. (1992; Novel streptococcal-integration shuttle vectors for gene cloning and inactivation. Gene 120:105–110
    [Google Scholar]
  38. Takao A. 2003; Cloning and expression of hyaluronate lyase genes of Streptococcus intermedius and Streptococcus constellatus subsp. constellatus . FEMS Microbiol Lett 219:143–150
    [Google Scholar]
  39. Takao A., Nagashima H., Usui H., Sasaki F., Maeda N., Ishibashi K., Fujita H. 1997; Hyaluronidase activity in human pus from which Streptococcus intermedius was isolated. Microbiol Immunol 41:795–798
    [Google Scholar]
  40. Tammi R., Tammi M., Hakkinen L., Larjava H. 1990; Histochemical localization of hyaluronate in human oral epithelium using a specific hyaluronate-binding probe. Arch Oral Biol 35:219–224
    [Google Scholar]
  41. Tammi M. I., Day A. J., Turley E. A. 2002; Hyaluronan and homeostasis: a balancing act. J Biol Chem 277:4581–4584
    [Google Scholar]
  42. Tanner A., Maiden M. F., Lee K., Shulman L. B., Weber H. P. 1997; Dental implant infections. Clin Infect Dis 25:Suppl 2S213–S217
    [Google Scholar]
  43. Unsworth P. F. 1989; Hyaluronidase production in Streptococcus milleri in relation to infection. J Clin Pathol 42:506–510
    [Google Scholar]
  44. Westergren G., Olsson J. 1983; Hydrophobicity and adherence of oral streptococci after repeated subculture in vitro. Infect Immun 40:432–435
    [Google Scholar]
  45. Whiley R. A., Beighton D., Winstanley T. G., Fraser H. Y., Hardie J. M. 1992; Streptococcus intermedius , Streptococcus constellatus , and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol 30:243–244
    [Google Scholar]
  46. Zhang M., McDonald F. M., Sturrock S. S., Charnock S. J., Humphery-Smith I., Black G. W. 2007; Group A streptococcus cell-associated pathogenic proteins as revealed by growth in hyaluronic acid-enriched media. Proteomics 7:1379–1390
    [Google Scholar]
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