1887

Abstract

Adhesion of bacterial cells to fibronectin (FN) is thought to be a pivotal step in the pathogenesis of invasive infectious diseases. Viridans group streptococci such as are considered commensal members of the oral microflora, but are important pathogens in infective endocarditis. expresses a battery of cell-surface adhesins that act alone or in concert to bind host receptors. Here, we employed molecular genetic approaches to determine the relative contributions of five known surface proteins to adherence to human FN. Binding levels to FN by isogenic mutants lacking Hsa glycoprotein were reduced by 70 %, while mutants lacking CshA and CshB fibrillar proteins showed approximately 30 % reduced binding. By contrast, disruption of antigen I/II adhesin genes s and in a wild-type background did not result in reduced FN binding. Enzymic removal of sialic acids from FN led to reduced DL1 adhesion (>50 %), but did not affect binding by the mutant, indicating that Hsa interacts with sialic acid moieties on FN. Conversely, desialylation of FN did not affect adherence levels of cells expressing SspA or SspB polypeptides. Complementation of the mutant partially restored adhesion to FN. A model is proposed for FN binding by in which Hsa and CshA/CshB are primary adhesins, and SspA or SspB play secondary roles. Understanding the basis of oral streptococcal interactions with FN will provide a foundation for development of new strategies to control infective endocarditis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032078-0
2009-11-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3572.html?itemId=/content/journal/micro/10.1099/mic.0.032078-0&mimeType=html&fmt=ahah

References

  1. Bensing, B. A. & Sullam, P. M. ( 2002; ). An accessory sec locus of Streptococcus gordonii is required for export of the surface protein GspB and for normal levels of binding to human platelets. Mol Microbiol 44, 1081–1094.[CrossRef]
    [Google Scholar]
  2. Bensing, B. A. & Sullam, P. M. ( 2009; ). Characterization of Streptococcus gordonii SecA2 as a paralogue of SecA. J Bacteriol 191, 3482–3491.[CrossRef]
    [Google Scholar]
  3. Bensing, B. A., Lopez, J. A. & Sullam, P. M. ( 2004; ). The Streptococcus gordonii surface proteins GspB and Hsa mediate binding to sialylated carbohydrate epitopes on the platelet membrane glycoprotein Ibα. Infect Immun 72, 6528–6537.[CrossRef]
    [Google Scholar]
  4. Bryan, E. M., Bae, T., Kleerebezem, M. & Dunny, G. M. ( 2000; ). Improved vectors for nisin-controlled expression in Gram-positive bacteria. Plasmid 44, 183–190.[CrossRef]
    [Google Scholar]
  5. Carsons, S., Lavietes, B. B., Slomiany, A., Diamond, H. S. & Berkowitz, E. ( 1987; ). Carbohydrate heterogeneity of fibronectins. Synovial fluid fibronectin resembles the form secreted by cultured synoviocytes but differs from the plasma form. J Clin Invest 80, 1342–1349.[CrossRef]
    [Google Scholar]
  6. Christie, J., McNab, R. & Jenkinson, H. F. ( 2002; ). Expression of fibronectin-binding protein FbpA modulates adhesion in Streptococcus gordonii. Microbiology 148, 1615–1625.
    [Google Scholar]
  7. Collins, T. J. ( 2007; ). ImageJ for microscopy. Biotechniques 43, 25–30.[CrossRef]
    [Google Scholar]
  8. Giomarelli, B., Visai, L., Hijazi, K., Rindi, S., Ponzio, M., Iannelli, F., Speziale, P. & Pozzi, G. ( 2006; ). Binding of Streptococcus gordonii to extracellular matrix proteins. FEMS Microbiol Lett 265, 172–177.[CrossRef]
    [Google Scholar]
  9. Haisman, R. J. & Jenkinson, H. F. ( 1991; ). Mutants of Streptococcus gordonii Challis over-producing glucosyltransferase. J Gen Microbiol 137, 483–489.[CrossRef]
    [Google Scholar]
  10. Heddle, C., Nobbs, A. H., Jakubovics, N. S., Gal, M., Mansell, J. P., Dymock, D. & Jenkinson, H. F. ( 2003; ). Host collagen signal induces antigen I/II adhesin and invasin gene expression in oral Streptococcus gordonii. Mol Microbiol 50, 597–607.[CrossRef]
    [Google Scholar]
  11. Hirt, H., Erlandsen, S. L. & Dunny, G. M. ( 2000; ). Heterologous inducible expression of Enterococcus faecalis pCF10 aggregation substance Asc10 in Lactococcus lactis and Streptococcus gordonii contributes to cell hydrophobicity and adhesion to fibrin. J Bacteriol 182, 2299–2306.[CrossRef]
    [Google Scholar]
  12. Holmes, A. R., Gilbert, C., Wells, J. M. & Jenkinson, H. F. ( 1998; ). Binding properties of Streptococcus gordonii SspA and SspB (antigen I/II family) polypeptides expressed on the cell surface of Lactococcus lactis MG1363. Infect Immun 66, 4633–4639.
    [Google Scholar]
  13. Jakubovics, N. S., Smith, A. W. & Jenkinson, H. F. ( 2000; ). Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38, 140–153.[CrossRef]
    [Google Scholar]
  14. Jakubovics, N. S., Kerrigan, S. W., Nobbs, A. H., Strömberg, N., van Dolleweerd, C. J., Cox, D. M., Kelly, C. G. & Jenkinson, H. F. ( 2005a; ). Functions of cell surface-anchored antigen I/II family and Hsa polypeptides in interactions of Streptococcus gordonii with host receptors. Infect Immun 73, 6629–6638.[CrossRef]
    [Google Scholar]
  15. Jakubovics, N. S., Strömberg, N., van Dolleweerd, C. J., Kelly, C. G. & Jenkinson, H. F. ( 2005b; ). Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Mol Microbiol 55, 1591–1605.[CrossRef]
    [Google Scholar]
  16. Jenkinson, H. F. ( 1987; ). Novobiocin-resistant mutants of Streptococcus sanguis with reduced cell hydrophobicity and defective in coaggregation. J Gen Microbiol 133, 1909–1918.
    [Google Scholar]
  17. Joh, D., Wann, E. R., Kreikemeyer, B., Speziale, P. & Höök, M. ( 1999; ). Role of fibronectin-binding MSCRAMMs in bacterial adherence and entry into mammalian cells. Matrix Biol 18, 211–223.[CrossRef]
    [Google Scholar]
  18. Lowrance, J. H., Hasty, D. L. & Simpson, W. A. ( 1988; ). Adherence of Streptococcus sanguis to conformationally specific determinants in fibronectin. Infect Immun 56, 2279–2285.
    [Google Scholar]
  19. McNab, R., Jenkinson, H. F., Loach, D. M. & Tannock, G. W. ( 1994; ). Cell-surface-associated polypeptides CshA and CshB of high molecular mass are colonization determinants in the oral bacterium Streptococcus gordonii. Mol Microbiol 14, 743–754.[CrossRef]
    [Google Scholar]
  20. McNab, R., Holmes, A. R., Clarke, J. M., Tannock, G. W. & Jenkinson, H. F. ( 1996; ). Cell surface polypeptide CshA mediates binding of Streptococcus gordonii to other oral bacteria and to immobilized fibronectin. Infect Immun 64, 4204–4210.
    [Google Scholar]
  21. McNab, R., Forbes, H., Handley, P. S., Loach, D. M., Tannock, G. W. & Jenkinson, H. F. ( 1999; ). Cell wall-anchored CshA polypeptide (259 kilodaltons) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties. J Bacteriol 181, 3087–3095.
    [Google Scholar]
  22. Nobbs, A. H., Shearer, B. H., Drobni, M., Jepson, M. A. & Jenkinson, H. F. ( 2007; ). Adherence and internalization of Streptococcus gordonii by epithelial cells involves β1 integrin recognition by SspA and SspB (antigen I/II family) polypeptides. Cell Microbiol 9, 65–83.[CrossRef]
    [Google Scholar]
  23. Petersen, F. C., Assev, S., van der Mei, H. C., Busscher, H. J. & Scheie, A. A. ( 2002; ). Functional variation of the antigen I/II surface protein in Streptococcus mutans and Streptococcus intermedius. Infect Immun 70, 249–256.[CrossRef]
    [Google Scholar]
  24. Plummer, C. & Douglas, C. W. ( 2006; ). Relationship between the ability of oral streptococci to interact with platelet glycoprotein Ibα and with the salivary low-molecular-weight mucin, MG2. FEMS Immunol Med Microbiol 48, 390–399.[CrossRef]
    [Google Scholar]
  25. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  26. Schwarz-Linek, U., Werner, J. M., Pickford, A. R., Gurusiddappa, S., Kim, J. H., Pilka, E. S., Briggs, J. A., Gough, T. S., Höök, M. & other authors ( 2003; ). Pathogenic bacteria attach to human fibronectin through a tandem β-zipper. Nature 423, 177–181.[CrossRef]
    [Google Scholar]
  27. Schwarz-Linek, U., Höök, M. & Potts, J. R. ( 2006; ). Fibronectin-binding proteins of Gram-positive cocci. Microbes Infect 8, 2291–2298.[CrossRef]
    [Google Scholar]
  28. Sy, R. W., Chawantanpipat, C., Richmond, D. R. & Kritharides, L. ( 2009; ). Development and validation of a time-dependent risk model for predicting mortality in infective endocarditis. Eur Heart JMar 28 [Epub ahead of print].
    [Google Scholar]
  29. Tajiri, M., Yoshida, S. & Wada, Y. ( 2005; ). Differential analysis of site-specific glycans on plasma and cellular fibronectins: application of a hydrophilic affinity method for glycopeptide enrichment. Glycobiology 15, 1332–1340.[CrossRef]
    [Google Scholar]
  30. 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 Immun 70, 1209–1218.[CrossRef]
    [Google Scholar]
  31. 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 Immun 72, 3876–3882.[CrossRef]
    [Google Scholar]
  32. Takahashi, Y., Takashima, E., Shimazu, K., Yagishita, H., Aoba, T. & Konishi, K. ( 2006; ). Contribution of sialic acid-binding adhesin to pathogenesis of experimental endocarditis caused by Streptococcus gordonii DL1. Infect Immun 74, 740–743.[CrossRef]
    [Google Scholar]
  33. Takamatsu, D., Bensing, B. A., Cheng, H., Jarvis, G. A., Siboo, I. R., Lopez, J. A., Griffiss, J. M. & Sullam, P. M. ( 2005; ). Binding of the Streptococcus gordonii surface glycoproteins GspB and Hsa to specific carbohydrate structures on platelet membrane glycoprotein Ibα. Mol Microbiol 58, 380–392.[CrossRef]
    [Google Scholar]
  34. Takamatsu, D., Bensing, B. A., Prakobphol, A., Fisher, S. J. & Sullam, P. M. ( 2006; ). Binding of the streptococcal surface glycoproteins GspB and Hsa to human salivary proteins. Infect Immun 74, 1933–1940.[CrossRef]
    [Google Scholar]
  35. Tanzer, J. M., Grant, L., Thompson, A., Li, L., Rogers, J. D., Haase, E. M. & Scannapieco, F. A. ( 2003; ). Amylase-binding proteins A (AbpA) and B (AbpB) differentially affect colonization of rats' teeth by Streptococcus gordonii. Microbiology 149, 2653–2660.[CrossRef]
    [Google Scholar]
  36. Tomás Carmona, I., Diz Dios, P. & Scully, C. ( 2007; ). Efficacy of antibiotic prophylactic regimens for the prevention of bacterial endocarditis of oral origin. J Dent Res 86, 1142–1159.[CrossRef]
    [Google Scholar]
  37. Troffer-Charlier, N., Ogier, J., Moras, D. & Cavarelli, J. ( 2002; ). Crystal structure of the V-region of Streptococcus mutans antigen I/II at 2.4 Å resolution suggests a sugar preformed binding site. J Mol Biol 318, 179–188.[CrossRef]
    [Google Scholar]
  38. Wizemann, T. M., Moskovitz, J., Pearce, B. J., Cundell, D., Arvidson, C. G., So, M., Weissbach, H., Brot, N. & Masure, H. R. ( 1996; ). Peptide methionine sulfoxide reductase contributes to the maintenance of adhesins in three major pathogens. Proc Natl Acad Sci U S A 93, 7985–7990.[CrossRef]
    [Google Scholar]
  39. Xiong, Y. Q., Bensing, B. A., Bayer, A. S., Chambers, H. F. & Sullam, P. M. ( 2008; ). Role of the serine-rich surface glycoprotein GspB of Streptococcus gordonii in the pathogenesis of infective endocarditis. Microb Pathog 45, 297–301.[CrossRef]
    [Google Scholar]
  40. Xu, P., Alves, J. M., Kitten, T., Brown, A., Chen, Z., Ozaki, L. S., Manque, P., Ge, X., Serrano, M. G. & other authors ( 2007; ). Genome of the opportunistic pathogen Streptococcus sanguinis. J Bacteriol 189, 3166–3175.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032078-0
Loading
/content/journal/micro/10.1099/mic.0.032078-0
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