The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model

Microbial Pathogenesis

Volumn 36, Issue 5, 2004, Pages 237-245

  Kristian, Sascha A ^a,b,c   Golda, Thomas ^b,c,d   Ferracin, Fabrizia ^c   Cramton, Sarah E ^a   Neumeister, Birgid ^b   Peschel, Andreas ^b   Götz, Friedrich ^a   Landmann, Regine ^c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Biofilm; ica operon; ica , S. aureus ATCC35556 ica deletion mutant; PIA, polysaccharide intercellular adhesin; Polysaccharide intercellular adhesin; SA113, S. aureus ATCC35556; Staphylococcus aureus; Tissue cage infection model; Virulence

Indexed keywords

ADHESIN; BACTERIAL POLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; POLYSACCHARIDE INTERCELLULAR ADHESIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOKINE RELEASE; DEVICE INFECTION; GUINEA PIG; IMMUNE RESPONSE; IMMUNOMODULATION; IMPLANT; LEUKOCYTE; MOUSE; MOUSE STRAIN; NONHUMAN; OPERON; PHAGOCYTE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; TISSUE INDUCTION;

ANIMALS; BACTERIAL ADHESION; BIOFILMS; CELL COUNT; CHEMOKINES; COLONY COUNT, MICROBIAL; DIFFUSION CHAMBERS, CULTURE; MICE; MICE, INBRED C57BL; PHAGOCYTES; POLYSACCHARIDES, BACTERIAL; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 1642303755     PISSN: 08824010     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micpath.2003.12.004     Document Type: Article

References (54)

1. Schierholz J.M., Beuth J. Implant infections: a haven for opportunistic bacteria. J Hosp Infect. 49:2001;87-93.
2. Donlan R.M. Biofilms and device-associated infections. Emerg Infect Dis. 7:2001;277-281.
3. Gentry L.O. Osteomyelitis and other infections of bones and joints. Crossley K.B., Archer G.L. The staphylococci in human disease. 1997;455-473 Churchill Livingstone.
4. O'Gara J.P., Humphreys H. Staphylococcus epidermidis biofilms: importance and implications. J Med Microbiol. 50:2001;582-587.
5. Ing M.B., Baddour L.M. Bacteremia and infective endocarditis: pathogenesis, diagnosis, and complications. Crossley K.B., Archer G.L. The staphylococci in human disease. 1995;331-334 Churchill Livingstone.
6. Götz F. Staphylococcus and biofilms. Mol Microbiol. 43:2002;1367-1378.
7. Peters G., Locci R., Pulverer G. Adherence and growth of coagulase-negative staphylococci on surfaces of intravenous catheters. J Infect Dis. 146:1982;479-482.
8. Peters G., Pulverer G. Pathogenesis and management of Staphylococcus epidermidis plastic foreign body infections. J Antimicrob Chemother. 14:(Suppl D):1984;67-71.
9. Steckelberg J.M., Osmon D.R. Prosthetic joint infections. Waldvogel F.A., Bisno A.L. Infections associated with indwelling medical devices. 2000;173-209 ASM.
10. Cramton S.E., Gerke C., Götz F. In vitro methods to study staphylococcal biofilm formation. Methods Enzymol. 336:2001;239-255.
11. Peters G., Locci R., Pulverer G. Microbial colonization of prosthetic devices. II. Scanning electron microscopy of naturally infected intravenous catheters. Zentralbl Bakteriol Mikrobiol Hyg [B]. 173:1981;293-299.
12. Christensen G.D., Bisno A.L., Parisi J.T., et al. Nosocomial septicemia due to multiply antibiotic-resistant Staphylococcus epidermidis. Ann Intern Med. 96:1982;1-10.
13. Götz F., Peters G. Colonization of medical devices coagulase-negative staphylococci. Waldvogel F.A., Bisno A.L. Infections associated with indwelling medical devices. 2000;55-88 ASM.
14. Hoyle B.D., Costerton J.W. Bacterial resistance to antibiotics: the role of biofilms. Prog Drug Res. 37:1991;91-105.
15. Cramton S.E., Gerke C., Schnell N.F., Nichols W.W., Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 67:1999;5427-5433.
16. Mack D., Fischer W., Krokotsch A., et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol. 178:1996;175-183.
17. Heilmann C., Schweitzer O., Gerke C., et al. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol. 20:1996;1083-1091.
18. Heilmann C., Gerke C., Perdreau-Remington F., Götz F. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect Immun. 64:1996;277-282.
19. Fey P.D., Ulphani J.S., Götz F., et al. Characterization of the relationship between polysaccharide intercellular adhesin and hemagglutination in Staphylococcus epidermidis. J Infect Dis. 179:1999;1561-1564.
20. Gross M., Cramton S.E., Götz F., Peschel A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect Immun. 69:2001;3423-3426.
21. Peschel A., Otto M., Jack R.W., et al. Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem. 274:1999;8405-8410.
22. Gerke C., Kraft A., Suessmuth R., Schweitzer O., Götz F. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem. 273:1998;18586-18593.
23. Cramton S.E., Ulrich M., Götz F., Doering G. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect Immun. 69:2001;4079-4085.
24. Rachid S., Ohlsen K., Witte W., Hacker J., Ziebuhr W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother. 44:2000;3357-3363.
25. Fowler V.G. Jr, Fey P.D., Reller L.B., et al. The intercellular adhesin locus ica is present in clinical isolates of Staphylococcus aureus from bacteremic patients with infected and uninfected prosthetic joints. Med Microbiol Immunol (Berl). 189:2001;127-131.
26. Yasuda H., Koga T., Fukuoka T. In vitro and in vivo models of bacterial biofilms. Methods Enzymol. 310:1999;577-595.
27. Rupp M.E., Fey P.D. In vivo models to evaluate adhesion and biofilm formation by Staphylococcus epidermidis. Methods Enzymol. 336:2001;206-215.
28. Rupp M.E., Ulphani J.S., Fey P.D., Bartscht K., Mack D. Characterization of the importance of polysaccharide intercellular adhesin/hemagglutinin of Staphylococcus epidermidis in the pathogenesis of biomaterial-based infection in a mouse foreign body infection model. Infect Immun. 67:1999;2627-2632.
29. Rupp M.E., Ulphani J.S., Fey P.D., Mack D. Characterization of Staphylococcus epidermidis polysaccharide intercellular adhesin/hemagglutinin in the pathogenesis of intravascular catheter-associated infection in a rat model. Infect Immun. 67:1999;2656-2659.
30. Rupp M.E., Fey P.D., Heilmann C., Götz F. Characterization of the importance of Staphylococcus epidermidis autolysin and polysaccharide intercellular adhesin in the pathogenesis of intravascular catheter-associated infection in a rat model. J Infect Dis. 183:2001;1038-1042.
31. Schwank S., Rajacic Z., Zimmerli W., Blaser J. Impact of bacterial biofilm formation on in vitro and in vivo activities of antibiotics. Antimicrob Agents Chemother. 42:1998;895-898.
32. Perdreau-Remington F., Sande M.A., Peters G., Chambers H.F. The abilities of a Staphylococcus epidermidis wild-type strain and its slime-negative mutant to induce endocarditis in rabbits are comparable. Infect Immun. 66:1998;2778-2781.
33. Francois P., Tu Quoc P.H., Bisognano C., et al. Lack of biofilm contribution to bacterial colonisation in an experimental model of foreign body infection by Staphylococcus aureus and Staphylococcus epidermidis. FEMS Immunol Med Microbiol. 35:2003;135-140.
34. Zimmerli W., Waldvogel F.A., Vaudaux P., Nydegger U.E. Pathogenesis of foreign body infection: description and characteristics of an animal model. J Infect Dis. 146:1982;487-497.
35. Zimmerli W. Tissue cage infection model. Zak O., Sande M.A. Handbook of animal models of infection. 1999;409-417 Academic Press.
36. Kristian S.A., Lauth X., Nizet V., et al. Alanylation of teichoic acids protects Staphylococcus aureus against Toll-like receptor 2-dependent host defense in a mouse tissue cage infection model. J. Infect Dis. 188:2003;414-423.
37. Iordanescu S., Surdeanu M. Two restriction and modification systems in Staphylococcus aureus NCTC8325. J Gen Microbiol. 96:1976;277-281.
38. Cauwels A., Frei K., Sansano S., et al. The origin and function of soluble CD14 in experimental bacterial meningitis. J Immunol. 162:1999;4762-4772.
39. Dawson J., Rordorf-Adam C., Geiger T., et al. Interleukin-1 (IL-1) production in a mouse tissue chamber model of inflammation. I. Development and initial characterisation of the model. Agents Actions. 38:1993;247-254.
40. Dayer E., Yoshida H., Izui S., Lambert P.H. Quantitation of retroviral gp70 antigen, autoantibodies, and immune complexes in extravascular space in arthritic MRL-lpr/lpr mice. Use of a subcutaneously implanted tissue cage model. Arthritis Rheum. 30:1987;1274-1282.
41. Gresham H.D., Lowrance J.H., Caver T.E., et al. Survival of Staphylococcus aureus inside neutrophils contributes to infection. J Immunol. 164:2000;3713-3722.
42. Nicoletti I., Migliorati G., Pagliacci M.C., Grignani F., Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods. 139:1991;271-279.
43. Vaudaux P., Pittet D., Haeberli A., et al. Host factors selectively increase staphylococcal adherence on inserted catheters: a role for fibronectin and fibrinogen or fibrin. J Infect Dis. 160:1989;865-875.
44. Tsujimoto H., Ono S., Mochizuki H., et al. Role of macrophage inflammatory protein 2 in acute lung injury in murine peritonitis. J Surg Res. 103:2002;61-67.
45. Verhoef J. Host defense against infection. Crossley K.B., Archer G.L. The staphylococci in human disease. 1997;213-232 Churchill Livingstone.
46. Kharazmi A. Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa. Immunol Lett. 30:1991;201-205.
47. Leid J.G., Shirtliff M.E., Costerton J.W., Stoodley A.P. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun. 70:2002;6339-6345.
48. Stewart P.S., Costerton J.W. Antibiotic resistance of bacteria in biofilms. Lancet. 358:2001;135-138.
49. Shive M.S., Salloum M.L., Anderson J.M. Shear stress-induced apoptosis of adherent neutrophils: a mechanism for persistence of cardiovascular device infections. Proc Natl Acad Sci USA. 97:2000;6710-6715.
50. Zimmerli W., Lew P.D., Waldvogel F.A. Pathogenesis of foreign body infection. Evidence for a local granulocyte defect. J Clin Invest. 73:1984;1191-1200.
51. Bliss S.K., Marshall A.J., Zhang Y., Denkers E.Y. Human polymorphonuclear leukocytes produce IL-12, TNF-alpha, and the chemokines macrophage-inflammatory protein-1 alpha and -1 beta in response to Toxoplasma gondii antigens. J Immunol. 162:1999;7369-7375.
52. Kasahara Y., Iwai K., Yachie A., et al. Involvement of reactive oxygen intermediates in spontaneous and CD95 (Fas/APO-1)-mediated apoptosis of neutrophils. Blood. 89:1997;1748-1753.
53. Haslett C. Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes. Clin Sci (Lond). 83:1992;639-648.
54. Yamamoto A., Taniuchi S., Tsuji S., Hasui M., Kobayashi Y. Role of reactive oxygen species in neutrophil apoptosis following ingestion of heat-killed Staphylococcus aureus. Clin Exp Immunol. 129:2002;479-484.