1887

Abstract

causes infections associated with medical devices including central venous catheters, orthopaedic prosthetic joints and artificial heart valves. This coagulase-negative staphylococcus produces a conventional cellular lipoteichoic acid (LTA) and also releases a short-glycerophosphate-chain-length form of LTA (previously termed lipid S) into the medium during growth. The relative pro-inflammatory activities of cellular and short-chain-length exocellular LTA were investigated in comparison with peptidoglycan and wall teichoic acid from and LPS from O111. The ability of these components to stimulate the production of pro-inflammatory cytokines [interleukin (IL)-1β, IL-6 and tumour necrosis factor (TNF)-α] and nitric oxide was investigated in a murine macrophage-like cell line (J774.2), and in peritoneal and splenic macrophages. On a weight-for-weight basis the short-chain-length exocellular LTA was the most active of the products, stimulating significant amounts of each of the inflammatory cytokines and nitric oxide, although it was approximately 100-fold less active than LPS from . By comparison the full-chain-length cellular LTA and peptidoglycan were less active and the wall teichoic acid had no activity. As an exocellular product potentially released from biofilms, the short-chain-length exocellular LTA may act as the prime mediator of the host inflammatory response to device-related infection by this organism and act as the Gram-positive equivalent of LPS in Gram-negative sepsis. The understanding of the role of short-chain-length exocellular LTA in Gram-positive sepsis may lead to improved treatment strategies.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.45872-0
2005-04-01
2020-10-01
Loading full text...

Full text loading...

/deliver/fulltext/jmm/54/4/JM540401.html?itemId=/content/journal/jmm/10.1099/jmm.0.45872-0&mimeType=html&fmt=ahah

References

  1. Archibald A. R., Baddiley J. 1968; The glycerol teichoic acid from walls of Staphylococcus epidermidis I2. Biochem J 110:583–588
    [Google Scholar]
  2. Bhakdi S., Klonisch P., Nuber P., Fischer W. 1991; Stimulation of monokine production by lipoteichoic acids. Infect Immun 59:4614–4620
    [Google Scholar]
  3. Boyce J. M. 1996; Epidemiology and prevention of nosocomial infections. In The Staphylococci in Human Disease pp 309–330 Edited by Crossley K., Archer G. New York: Churchill Livingstone;
    [Google Scholar]
  4. Bucher M., Ittner K. P., Zimmermann M., Wolf K., Hobbhahn J., Kurtz A. 1997; Nitric oxide synthase isoform III gene expression in rat liver is up-regulated by lipopolysaccharide and lipoteichoic acid. FEBS Lett 412:511–514 [CrossRef]
    [Google Scholar]
  5. Cleveland M. G., Gorham J. D., Murphy T. L., Tuomanen E., Murphy K. M. 1996; Lipoteichoic acid preparations of Gram-positive bacteria induce interleukin-12 through a CD14-dependent pathway. Infect Immun 64:1906–1912
    [Google Scholar]
  6. Coley J., Duckworth M., Baddiley J. 1972; The occurrence of lipoteichoic acids in the membranes of Gram-positive bacteria. J Gen Microbiol 73:587–591 [CrossRef]
    [Google Scholar]
  7. Connaughton M., Lang S., Tebbs S. E., Littler W. A., Lambert P. A., Elliott T. S. J. 2001; Rapid serodiagnosis of Gram-positive bacterial endocarditis. J Infect 42:140–144 [CrossRef]
    [Google Scholar]
  8. Deininger S., Stadelmaier A., von Aulock S., Morath R. R., Hartung T. 2003; Definition of structural prerequisites for lipoteichoic acid-inducible cytokine induction by synthetic derivatives. J Immunol 170:4134–4138 [CrossRef]
    [Google Scholar]
  9. De Kimpe S. J., Hunter M. L., Bryant C. E., Thiemermann C., Vane J. R. 1995a; Delayed circulatory failure due to the induction of nitric oxide synthase by lipoteichoic acid from Staphylococcus aureus . Br J Pharmacol 114:1317–1323 [CrossRef]
    [Google Scholar]
  10. De Kimpe S. J., Kengatharan K. M., Thiemermann C., Vane J. R. 1995b; The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc Natl Acad Sci U S A 92:10359–10363 [CrossRef]
    [Google Scholar]
  11. Elliott T. S. J., Tebbs S. E., Moss H. A., Worthington T., Spare M. K., Faroqui M. H., Lambert P. A. 2000; A novel serological test for the diagnosis of central venous catheter-associated sepsis. J Infect 40:262–266 [CrossRef]
    [Google Scholar]
  12. Farrell A. M., Foster T. J., Holland K. T. 1993; Molecular analysis and expression of the lipase of Staphylococcus epidermidis . J Gen Microbiol 139:267–277 [CrossRef]
    [Google Scholar]
  13. Fischer W. 1993; Molecular analysis of lipid macroamphiphiles by hydrophobic interaction chromatography, exemplified with lipoteichoic acids. Anal Biochem 208:49–56 [CrossRef]
    [Google Scholar]
  14. Fischer W. 1994; Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus . Med Microbiol Immunol (Berl) 183:61–76 [CrossRef]
    [Google Scholar]
  15. Ginsburg I. 2002; Role of lipoteichoic acid in infection and inflammation. Lancet Infect Dis 2:171–179 [CrossRef]
    [Google Scholar]
  16. Hattor Y., Kasai K., Akimoto K., Thiemermann C. 1997; Induction of NO synthesis by lipoteichoic acid from Staphylococcus aureus in J774 macrophages: involvement of a CD14-dependent pathway. Biochem Biophys Res Commun 233:375–379 [CrossRef]
    [Google Scholar]
  17. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. 1999; Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749–3752
    [Google Scholar]
  18. Hussain M., Hastings J. G. M., White P. J. 1991a; A chemically defined medium for slime production by coagulase-negative staphylococci. J Med Microbiol 34:143–147 [CrossRef]
    [Google Scholar]
  19. Hussain M., Hastings J. G. M., White P. J. 1991b; Isolation and composition of the extracellular slime made by coagulase-negative staphylococci in a chemically defined medium. J Infect Dis 163:534–541 [CrossRef]
    [Google Scholar]
  20. Hussain M., Hastings J. G. M., White P. J. 1992; Comparison of cell-wall teichoic acid with high-molecular-weight extracellular slime material from Staphylococcus epidermidis . J Med Microbiol 37:368–375 [CrossRef]
    [Google Scholar]
  21. Kengatharan K. M., de Kimpe S. J., Robson C., Foster S. J., Thiemermann C. 1998; Mechanism of Gram-positive shock: identification of peptidoglycan and lipoteichoic acid moieties essential in the induction of nitric oxide synthase, shock, and multiple organ failure. J Exp Med 188:305–315 [CrossRef]
    [Google Scholar]
  22. Lambe D. W., Ferguson K. P., Keplinger J. L., Gemmell C. G., Kalbfleisch J. H. 1990; Pathogenicity of Staphylococcus lugdunensis , Staphylococcus schleiferi , and three other coagulase-negative staphylococci in a mouse model and possible virulence factors. Can J Microbiol 36:455–463 [CrossRef]
    [Google Scholar]
  23. Lambert P. A., van Maurik A., Parvatham S., Akhtar Z., Fraise A. P., Krikler S. J. 1996; Potential of exocellular carbohydrate antigens of Staphylococcus epidermidis in the serodiagnosis of orthopaedic prosthetic infection. J Med Microbiol 44:355–361 [CrossRef]
    [Google Scholar]
  24. Lambert P. A., Worthington T., Tebbs S. E., Elliott T. S. J. 2000; Lipid S, a novel Staphylococcus epidermidis exocellular antigen with potential for the serodiagnosis of infections. FEMS Immunol Med Microbiol 29:195–202 [CrossRef]
    [Google Scholar]
  25. Molnàr C., Hevessy Z., Rozgonyi F., Gemmell C. G. 1994; Pathogenicity and virulence of coagulase-negative staphylococci in relation to adherence, hydrophobicity, and toxin production in vitro. J Clin Pathol 47:743–748 [CrossRef]
    [Google Scholar]
  26. Morath S., Geyer A., Hartung T. 2001; Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus . J Exp Med 193:393–398 [CrossRef]
    [Google Scholar]
  27. Morath S., Stadelmaier A., Geyer A., Schmidt R. R., Hartung T. 2002; Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J Exp Med 195:1635–1640 [CrossRef]
    [Google Scholar]
  28. Neuhaus F. C., Baddiley J. 2003; A continuum of anionic charge: structures and functions of d-alanyl-teichoic acids in Gram-positive bacteria. Microbiol Mol Biol Rev 67:686–723 [CrossRef]
    [Google Scholar]
  29. Ohta K., Komatsuzawa H., Sugai M., Suginaka H. 1998; Zymographic characterization of Staphylococcus aureus cell wall. Microbiol Immunol 42:231–235 [CrossRef]
    [Google Scholar]
  30. Paulsson M., Ljungh A., Wadström T. 1992; Rapid identification of fibronectin, vitronectin, laminin, and collagen cell surface binding proteins on coagulase-negative staphylococci by particle agglutination assays. J Clin Microbiol 30:2006–2012
    [Google Scholar]
  31. Peters G., Schumacher-Perdreau F. 1994; Extracellular slime substance as a virulence determinant in Staphylococcus epidermidis . In Molecular Pathogenesis of Surgical Infections pp 109–116 Edited by Wadström T., Holder I., Kronvall G. Deerfield Beach: Gustav Fischer Verlag;
    [Google Scholar]
  32. Poxton I. R., Hancock I. C. 1988; Separation and purification of surface components. In Bacterial Cell Surface Techniques pp 67–135 Chichester: Wiley;
    [Google Scholar]
  33. Rafiq M., Worthington T., Tebbs S. E., Treacy R. B. C., Dias R., Lambert P. A., Elliott T. S. J. 2000; Serological detection of Gram-positive bacterial infection around protheses. J Bone Joint Surg Br 82:B1156–1161
    [Google Scholar]
  34. Sadovskaya I., Vinogradov E., Li J., Jabbouri S. 2004; Structural elucidation of the extracellular and cell-wall teichoic acids of Staphylococcus epidermidis RP62A, a reference biofilm-positive strain. Carbohydr Res 339:1467–1473 [CrossRef]
    [Google Scholar]
  35. Schroder N. W., Morath S., Alexander C., Hamann L., Hartung T., Zahringer U., Gobel U. B., Weber J. R., Schumann R. R. 2003; Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD14, whereas TLR-4 and MD-2 are not involved. J Biol Chem 278:15587–15594 [CrossRef]
    [Google Scholar]
  36. Schwandner R., Dziarski R., Wesche W., Rothe M., Kirschning C. J. 1999; Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J Biol Chem 274:17406–17409 [CrossRef]
    [Google Scholar]
  37. Thiemermann C. 2002; Interactions between lipoteichoic acid and peptidoglycan from Staphylococcus aureus : a structural and functional analysis. Microbes Infect 4:927–935 [CrossRef]
    [Google Scholar]
  38. Van Langevelde P., Ravensbergen E., Grashoff P., Beekhuizen H., Groeneveld P. H., van Dissel J. T. 1999; Antibiotic-induced cell wall fragments of Staphylococcus aureus increase endothelial chemokine secretion and adhesiveness for granulocytes. Antimicrob Agents Chemother 43:2984–2989
    [Google Scholar]
  39. Wang J. E., Dahle M. K., McDonald M., Foster S. J., Aasen A. O., Thiemermann C. 2003; Peptidoglycan and lipoteichoic acid in Gram-positive bacterial sepsis: receptors, signal transduction, biological effects, and synergism. Shock 20:402–414 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.45872-0
Loading
/content/journal/jmm/10.1099/jmm.0.45872-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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