1887

Abstract

The major bacterial pathogens associated with periodontitis include . We previously discovered that sialic acid stimulates biofilm growth of , and that sialidase activity is key to utilization of sialoconjugate sugars and is involved in host–pathogen interactions . The aim of this work was to assess the influence of the NanH sialidase on initial biofilm adhesion and growth in experiments where the only source of sialic acid was sialoglycoproteins or human oral secretions. After showing that can utilize sialoglycoproteins for biofilm growth, we showed that growth and initial adhesion with sialylated mucin and fetuin were inhibited two- to threefold by the sialidase inhibitor oseltamivir. A similar reduction (three- to fourfold) was observed with a mutant compared with the wild-type. Importantly, these data were replicated using clinically relevant serum and saliva samples as substrates. In addition, the ability of the mutant to form biofilms on glycoprotein-coated surfaces could be restored by the addition of purified NanH, which we show is able to cleave sialic acid from the model glycoprotein fetuin and, much less efficiently, 9--acetylated bovine submaxillary mucin. These data show for the first time that glycoprotein-associated sialic acid is likely to be a key nutrient source for when growing in a biofilm, and suggest that sialidase inhibitors might be useful adjuncts in periodontal therapy.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.052498-0
2011-11-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/11/3195.html?itemId=/content/journal/micro/10.1099/mic.0.052498-0&mimeType=html&fmt=ahah

References

  1. Angata T., Varki A..( 2002;). Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem Rev102:439–470 [CrossRef][PubMed]
    [Google Scholar]
  2. Aruni W., Vanterpool E., Osbourne D., Roy F., Muthiah A., Dou Y., Fletcher H. M..( 2011;). Sialidase and sialoglycoproteases can modulate virulence in Porphyromonas gingivalis. Infect Immun79:2779–2791 [CrossRef][PubMed]
    [Google Scholar]
  3. Banerjee A., Van Sorge N. M., Sheen T. R., Uchiyama S., Mitchell T. J., Doran K. S..( 2010;). Activation of brain endothelium by pneumococcal neuraminidase NanA promotes bacterial internalization. Cell Microbiol12:1576–1588 [CrossRef][PubMed]
    [Google Scholar]
  4. Bradshaw D. J., Homer K. A., Marsh P. D., Beighton D..( 1994;). Metabolic cooperation in oral microbial communities during growth on mucin. Microbiology140:3407–3412 [CrossRef][PubMed]
    [Google Scholar]
  5. Bradshaw D. J., Marsh P. D., Watson G. K., Allison C..( 1998;). Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect Immun66:4729–4732[PubMed]
    [Google Scholar]
  6. Byers H. L., Tarelli E., Homer K. A., Beighton D..( 1999;). Sequential deglycosylation and utilization of the N-linked, complex-type glycans of human alpha1-acid glycoprotein mediates growth of Streptococcus oralis. Glycobiology9:469–479 [CrossRef][PubMed]
    [Google Scholar]
  7. Byres E., Paton A. W., Paton J. C., Löfling J. C., Smith D. F., Wilce M. C., Talbot U. M., Chong D. C., Yu H. et al.( 2008;). Incorporation of a non-human glycan mediates human susceptibility to a bacterial toxin. Nature456:648–652 [CrossRef][PubMed]
    [Google Scholar]
  8. Cointe D., Leroy Y., Chirat F..( 1998;). Determination of the sialylation level and of the ratio α-(2→3)/α-(2→6) sialyl linkages of N-glycans by methylation and GC/MS analysis. Carbohydr Res311:51–59 [CrossRef][PubMed]
    [Google Scholar]
  9. Corfield T..( 1992;). Bacterial sialidases–roles in pathogenicity and nutrition. Glycobiology2:509–521 [CrossRef][PubMed]
    [Google Scholar]
  10. Dabelsteen E..( 1996;). Cell surface carbohydrates as prognostic markers in human carcinomas. J Pathol179:358–369 [CrossRef][PubMed]
    [Google Scholar]
  11. Demuth D. R., Golub E. E., Malamud D..( 1990;). Streptococcal-host interactions. Structural and functional analysis of a Streptococcus sanguis receptor for a human salivary glycoprotein. J Biol Chem265:7120–7126[PubMed]
    [Google Scholar]
  12. Derrien M., van Passel M. W., van de Bovenkamp J. H., Schipper R. G., de Vos W. M., Dekker J..( 2010;). Mucin-bacterial interactions in the human oral cavity and digestive tract. Gut Microbes1:254–268 [CrossRef][PubMed]
    [Google Scholar]
  13. El-Kheshen M..( 2009;). DentistDecember 2008:48–50
    [Google Scholar]
  14. Ellen R. P., Fillery E. D., Chan K. H., Grove D. A..( 1980;). Sialidase-enhanced lectin-like mechanism for Actinomyces viscosus and Actinomyces naeslundii hemagglutination. Infect Immun27:335–343[PubMed]
    [Google Scholar]
  15. Falkler W. A. Jr, Burger B. W..( 1981;). Microbial surface interactions: reduction of the haemagglutination activity of the oral bacterium Fusobacterium nucleatum by absorption with Streptococcus and Bacteroides. Arch Oral Biol26:1015–1025 [CrossRef][PubMed]
    [Google Scholar]
  16. Gabriel M. O., Grünheid T., Zentner A..( 2005;). Glycosylation pattern and cell attachment-inhibiting property of human salivary mucins. J Periodontol76:1175–1181 [CrossRef][PubMed]
    [Google Scholar]
  17. Honma K., Mishima E., Sharma A..( 2011;). Role of Tannerella forsythia NanH sialidase in epithelial cell attachment. Infect Immun79:393–401 [CrossRef][PubMed]
    [Google Scholar]
  18. King S. J., Hippe K. R., Weiser J. N..( 2006;). Deglycosylation of human glycoconjugates by the sequential activities of exoglycosidases expressed by Streptococcus pneumoniae. Mol Microbiol59:961–974 [CrossRef][PubMed]
    [Google Scholar]
  19. Kolenbrander P. E., Palmer R. J..( 2004;). Human oral bacterial biofilms. Microbial Biofilms85–117 Ghannoum M. A., O’Toole G. A.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  20. Krivan H. C., Roberts D. D., Ginsburg V..( 1988;). Many pulmonary pathogenic bacteria bind specifically to the carbohydrate sequence GalNAc beta 1-4Gal found in some glycolipids. Proc Natl Acad Sci U S A85:6157–6161 [CrossRef][PubMed]
    [Google Scholar]
  21. Kuroiwa A., Hisatsune A., Isohama Y., Katsuki H..( 2009;). Bacterial neuraminidase increases IL-8 production in lung epithelial cells via NF-κB-dependent pathway. Biochem Biophys Res Commun379:754–759 [CrossRef][PubMed]
    [Google Scholar]
  22. Leake J. R., Read D. J..( 1990;). Chitin as a nitrogen source for micorrhizal fungi. Mycol Res94:993–995 [CrossRef]
    [Google Scholar]
  23. Martin M. J., Rayner J. C., Gagneux P., Barnwell J. W., Varki A..( 2005;). Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. Proc Natl Acad Sci U S A102:12819–12824 [CrossRef][PubMed]
    [Google Scholar]
  24. Mizan S., Henk A., Stallings A., Maier M., Lee M. D..( 2000;). Cloning and characterization of sialidases with 2-6′ and 2-3′ sialyl lactose specificity from Pasteurella multocida. J Bacteriol182:6874–6883 [CrossRef][PubMed]
    [Google Scholar]
  25. Offner G. D., Troxler R. F..( 2000;). Heterogeneity of high-molecular-weight human salivary mucins. Adv Dent Res14:69–75 [CrossRef][PubMed]
    [Google Scholar]
  26. Pham T. K., Roy S., Noirel J., Douglas I., Wright P. C., Stafford G. P..( 2010;). A quantitative proteomic analysis of biofilm adaptation by the periodontal pathogen Tannerella forsythia. Proteomics10:3130–3141 [CrossRef][PubMed]
    [Google Scholar]
  27. Pigman W., Gottschalk A..( 1966;). Submaxillary gland glycoproteins. Glycoproteins. Their Composition, Structure, and Function434–445 Amsterdam, The Netherlands: Elsevier;
    [Google Scholar]
  28. Reinholdt J., Tomana M., Mortensen S. B., Kilian M..( 1990;). Molecular aspects of immunoglobulin A1 degradation by oral streptococci. Infect Immun58:1186–1194[PubMed]
    [Google Scholar]
  29. Roy S., Douglas C. W., Stafford G. P..( 2010;). A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia. J Bacteriol192:2285–2293 [CrossRef][PubMed]
    [Google Scholar]
  30. Salyers A. A., Pajeau M., McCarthy R. E..( 1988;). Importance of mucopolysaccharides as substrates for Bacteroides thetaiotaomicron growing in intestinal tracts of exgermfree mice. Appl Environ Microbiol54:1970–1976[PubMed]
    [Google Scholar]
  31. Scannapieco F. A..( 1994;). Saliva-bacterium interactions in oral microbial ecology. Crit Rev Oral Biol Med5:203–248[PubMed]
    [Google Scholar]
  32. Severi E., Hood D. W., Thomas G. H..( 2007;). Sialic acid utilization by bacterial pathogens. Microbiology153:2817–2822 [CrossRef][PubMed]
    [Google Scholar]
  33. Skoza L., Mohos S..( 1976;). Stable thiobarbituric acid chromophore with dimethyl sulphoxide. Application to sialic acid assay in analytical de-O-acetylation. Biochem J159:457–462[PubMed]
    [Google Scholar]
  34. Socransky S. S., Haffajee A. D., Cugini M. A., Smith C., Kent R. L. Jr.( 1998;). Microbial complexes in subgingival plaque. J Clin Periodontol25:134–144 [CrossRef][PubMed]
    [Google Scholar]
  35. Soong G., Muir A., Gomez M. I., Waks J., Reddy B., Planet P., Singh P. K., Kaneko Y., Wolfgang M. C. et al.( 2006;). Bacterial neuraminidase facilitates mucosal infection by participating in biofilm production. J Clin Invest116:2297–2305 [CrossRef][PubMed]
    [Google Scholar]
  36. Spiro R. G., Bhoyroo V. D..( 1974;). Structure of the O-glycosidically linked carbohydrate units of fetuin. J Biol Chem249:5704–5717[PubMed]
    [Google Scholar]
  37. Steenbergen S. M., Jirik J. L., Vimr E. R..( 2009;). YjhS (NanS) is required for Escherichia coli to grow on 9-O-acetylated N-acetylneuraminic acid. J Bacteriol191:7134–7139 [CrossRef][PubMed]
    [Google Scholar]
  38. Takahashi Y., Konishi K., Cisar J. O., Yoshikawa M..( 2002;). Identification and characterization of hsa, the gene encoding the sialic acid-binding adhesin of Streptococcus gordonii DL1. Infect Immun70:1209–1218 [CrossRef][PubMed]
    [Google Scholar]
  39. Takahashi Y., Yajima A., Cisar J. O., Konishi K..( 2004;). Functional analysis of the Streptococcus gordonii DL1 sialic acid-binding adhesin and its essential role in bacterial binding to platelets. Infect Immun72:3876–3882 [CrossRef][PubMed]
    [Google Scholar]
  40. Tanner A. C., Izard J..( 2006;). Tannerella forsythia, a periodontal pathogen entering the genomic era. Periodontol 200042:88–113 [CrossRef][PubMed]
    [Google Scholar]
  41. Thompson H., Homer K. A., Rao S., Booth V., Hosie A. H..( 2009;). An orthologue of Bacteroides fragilis NanH is the principal sialidase in Tannerella forsythia. J Bacteriol191:3623–3628 [CrossRef][PubMed]
    [Google Scholar]
  42. Tong H. H., Blue L. E., James M. A., DeMaria T. F..( 2000;). Evaluation of the virulence of a Streptococcus pneumoniae neuraminidase-deficient mutant in nasopharyngeal colonization and development of otitis media in the chinchilla model. Infect Immun68:921–924 [CrossRef][PubMed]
    [Google Scholar]
  43. Varki A..( 1997;). Sialic acids as ligands in recognition phenomena. FASEB J11:248–255[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.052498-0
Loading
/content/journal/micro/10.1099/mic.0.052498-0
Loading

Data & Media loading...

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