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
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/012393-0
2008-03-01
2020-04-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/3/932.html?itemId=/content/journal/micro/10.1099/mic.0.2007/012393-0&mimeType=html&fmt=ahah

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 Dermatol109:219–224
    [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 Chem279:39798–39806
    [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 Biochem293:53–59
    [Google Scholar]
  4. Bowden G. H., Li Y. H.. 1997; Nutritional influences on biofilm development. Adv Dent Res11:81–99
    [Google Scholar]
  5. Branda S. S., Vik S., Friedman L., Kolter R.. 2005; Biofilms: the matrix revisited. Trends Microbiol13:20–26
    [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 Invest106:349–360
    [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 Dis32:1511–1515
    [Google Scholar]
  8. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M.. 1995; Microbial biofilms. Annu Rev Microbiol49:711–745
    [Google Scholar]
  9. Costerton J. W., Stewart P. S., Greenberg E. P.. 1999; Bacterial biofilms: a common cause of persistent infections. Science284:1318–1322
    [Google Scholar]
  10. Fallgren C., Andersson A., Ljungh A.. 2001; The role of glycosaminoglycan binding of staphylococci in attachment to eukaryotic host cells. Curr Microbiol43:57–63
    [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 Dis11:11–15
    [Google Scholar]
  12. Girish K. S., Kemparaju K.. 2007; The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Life Sci80:1921–1943
    [Google Scholar]
  13. Gossling J.. 1988; Occurrence and pathogenicity of the Streptococcus milleri group. Rev Infect Dis10:257–285
    [Google Scholar]
  14. Hamada S., Slade H. D.. 1980; Biology, immunology, and cariogenicity of Streptococcus mutans . Microbiol Rev44:331–384
    [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 Endod20:75–77
    [Google Scholar]
  16. Homer K., Shain H., Beighton D.. 1997; The role of hyaluronidase in growth of Streptococcus intermedius on hyaluronate. Adv Exp Med Biol418:681–683
    [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 Microbiol39:995–1001
    [Google Scholar]
  18. Hynes W. L., Walton S. L.. 2000; Hyaluronidases of Gram-positive bacteria. FEMS Microbiol Lett183:201–207
    [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 Bacteriol187:382–387
    [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 Bacteriol185:4693–4698
    [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 Bacteriol186:4740–4747
    [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 Biol32:811–815
    [Google Scholar]
  23. Nyberg A., Engstrom-Laurent A., Loof L.. 1988; Serum hyaluronate in primary biliary cirrhosis – a biochemical marker for progressive liver damage. Hepatology8:142–146
    [Google Scholar]
  24. Okayama H., Nagata E., Ito H. O., Oho T., Inoue M.. 2005; Experimental abscess formation caused by human dental plaque. Microbiol Immunol49:399–405
    [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 Immun69:4647–4653
    [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 Bacteriol186:6327–6331
    [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 Res30: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 Dis11:491–498
    [Google Scholar]
  29. Pogrel M. A., Lowe M. A., Stern R.. 1996; Hyaluronan (hyaluronic acid) in human saliva. Arch Oral Biol41:667–671
    [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 Chem217:959–966
    [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 Res37:114–118
    [Google Scholar]
  32. Ruoslahti E.. 1996; Brain extracellular matrix. Glycobiology6:489–492
    [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 Microbiol44:381–389
    [Google Scholar]
  34. Smith A. J., Addy M., Embery G.. 1995; Gingival crevicular fluid glycosaminoglycan levels in patients with chronic adult periodontitis. J Clin Periodontol22:355–361
    [Google Scholar]
  35. Starr C. R., Engleberg N. C.. 2006; Role of hyaluronidase in subcutaneous spread and growth of group A streptococcus. Infect Immun74:40–48
    [Google Scholar]
  36. Sutherland I. W.. 2001; The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol9:222–227
    [Google Scholar]
  37. Tao L., LeBlanc D. J., Ferretti J. J.. (1992; Novel streptococcal-integration shuttle vectors for gene cloning and inactivation. Gene120:105–110
    [Google Scholar]
  38. Takao A.. 2003; Cloning and expression of hyaluronate lyase genes of Streptococcus intermedius and Streptococcus constellatus subsp. constellatus . FEMS Microbiol Lett219:143–150
    [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 Immunol41:795–798
    [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 Biol35:219–224
    [Google Scholar]
  41. Tammi M. I., Day A. J., Turley E. A.. 2002; Hyaluronan and homeostasis: a balancing act. J Biol Chem277:4581–4584
    [Google Scholar]
  42. Tanner A., Maiden M. F., Lee K., Shulman L. B., Weber H. P.. 1997; Dental implant infections. Clin Infect Dis25:Suppl 2S213–S217
    [Google Scholar]
  43. Unsworth P. F.. 1989; Hyaluronidase production in Streptococcus milleri in relation to infection. J Clin Pathol42:506–510
    [Google Scholar]
  44. Westergren G., Olsson J.. 1983; Hydrophobicity and adherence of oral streptococci after repeated subculture in vitro. Infect Immun40:432–435
    [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 Microbiol30:243–244
    [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. Proteomics7:1379–1390
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/012393-0
Loading
/content/journal/micro/10.1099/mic.0.2007/012393-0
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error