The effect of subminimal inhibitory concentrations of antibiotics on virulence factors expressed by Staphylococcus aureus biofilms

Journal of Applied Microbiology

Volumn 108, Issue 4, 2010, Pages 1281-1291

  Haddadin, R N S ^a,d   Saleh, S ^b   Al Adham, I S I ^c   Buultjens, T E J ^a   Collier, P J ^a  

^a UNIVERSITY OF ABERTAY DUNDEE   (United Kingdom)

^b APPLIED SCIENCE PRIVATE UNIVERSITY   (Jordan)

^c UNIVERSITY OF PETRA   (Jordan)

^d UNIVERSITY OF JORDAN   (Jordan)

Author keywords

Biofilm; Coagulase; Splenocytes; Subminimal inhibitory concentrations; Toxic Shock Syndrome Toxin; Virulence

Indexed keywords

ANTIBIOTICS; BACTERIA; CELL CULTURE; MICROWAVE INTEGRATED CIRCUITS; TOXIC MATERIALS;

CEFALEXIN; COAGULASE; INHIBITORY CONCENTRATION; SPLENOCYTES; STAPHYLOCOCCUS AUREUS; SUBMINIMAL INHIBITORY CONCENTRATION; TOXIC SHOCK SYNDROME TOXIN; TOXIC SHOCKS; VIRULENCE; VIRULENCE FACTORS;

BIOFILMS;

CEFALEXIN; CIPROFLOXACIN; COAGULASE; ROXITHROMYCIN; TOXIC SHOCK SYNDROME TOXIN 1;

ANTIBIOTICS; BACTERIUM; BIOASSAY; BIOFILM; ENZYME ACTIVITY; FILTER; GENE EXPRESSION; INHIBITOR; PATHOGEN; RODENT; TOXIN; VIRULENCE;

ANIMAL CELL; ARTICLE; BIOFILM; CELL PROLIFERATION; CELL SUSPENSION; CONTROLLED STUDY; DRUG CONCENTRATION; ENZYME SYNTHESIS; MOUSE; NONHUMAN; PURIFICATION; SPLEEN CELL; STAPHYLOCOCCUS AUREUS; TOXIN ANALYSIS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 77949419502     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04529.x     Document Type: Article

References (57)

1. 1281-1291 Al-Hmoud, N. (2002) Studies on the development of anti-microbial tolerance in monospecies and binary biofilms. PhD Thesis, University of Abertay Dundee, Dundee, UK.
2. Allsop, A., Brooks, G., Edwards, P., Kawra, A. and Southgate, R. (1996) Inhibitors of bacterial signal peptidase: a series of 6-(substituted oxyethyl) penems. J Antibiot 49, 921-928.
3. Arvidson, S. (2004) Virulence gene regulation and their role in pathogenesis of disease. In Staphylococcus aureus, Molecular and Clinical Aspects ed. Ala'Aldeen, D. and Hiramatsu, K. pp. 154-176. Chichester, UK: Horwood publishing.
4. Bayston, R. (2000) Biofilm and prosthetic devices. In Community Structure and Co-operation in Biofilms ed. Allison, D., Gilbert, P., Lappin-Scott, H. and Wilson, M. pp. 295-308. Society for General Microbiology Symposium 59th. Cambridge: Cambridge University press.
5. Bernardo, K., Pakulat, N., Fleer, S., Schnaith, A., Utermöhlen, O., Krut, O., Muller, S. and Kronke, M. (2004) Sub-MIC of linezolid reduce Staphylococcus aureus virulence factor expression. Antimicrob Agents Chemother 48, 546-555.
6. Black, M. and Bruton, G. (1998) Inhibitors of bacterial signal peptidases. Curr Pharm Des 4, 133-154.
7. Blanco, L., Choi, E., Connolly, K., Thompson, M. and Bonventre, P. (1990) Mutants of staphylococcal shock syndrome toxin 1: mitogenicity and recognition by a neutralizing monoclonal antibody. Infect Immun 58, 3020-3028.
8. Blomster-Hautamaa, D., Kreiswirth, B., Kornblum, J., Novick, R. and Schlievert, P. (1986) The nucleotide and partial amino acid sequence of toxic shock syndrome toxin-1. J Biol Chem 261, 15783-15786.
9. Bonventre, P., Heeg, H. and Lian, C. (1993) Toxicity of recombinant toxic shock syndrome toxin 1 and mutant toxins produced by Staphylococcus aureus in a rabbit infection model of toxic shock syndrome. Infect Immun 61, 793-799.
10. Bradford, M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
11. Caiazza, N. and O'Toole, G. (2003) Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J Bacteriol 185, 3214-3217.
12. Cohn, S., Cohn, K., Rafferty, M., Smith, A., Degutis, L., Kowalsky, S. and Shah, A. (1995) Enteric absorption of ciprofloxacin during the immediate postoperative period. J Antimicrob Chemother 36, 717-721.
13. Costerton, J., Stewart, P. and Greenberg, E. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322.
14. Czajgucki, Z., Zimecki, M. and Andruszkiewicz, R. (2007) The immunoregulatory effects of edeine analogues in mice. Cell Mol Biol Lett 12, 149-161.
15. Deighton, M., Capstick, J., Domalewski, E. and Nguyen, T. (2001) Methods for studying biofilms produced by Staphylococcus epidermidis. In Methods in Enzymology. Microbial growth in biofilms. Part A: Developmental and molecular biological aspects, vol. 336 ed. Doyle, R. pp. 177-195. New York: Academic press.
16. Deppermann, K. and Lode, H. (1993) Fluoroquinolones: interaction profile during enteral absorption. Drugs 45 (Suppl), 365-372.
17. Dickgiesser, N. and Wallach, U. (1987) Toxic shock syndrome toxin-1 (TSST-1): influence of its production by subinhibitory antibiotic concentrations. Infection 15, 351-353.
18. Dinges, M., Orwin, P. and Schlievert, P. (2000) Exotoxins of Staphylococcus aureus. Clin Microbiol Rev 13, 16-34.
19. Doss, S., Tillotson, G. and Amyes, S. (1993) Effect of subinhibitory concentrations of antibiotics on the virulence of Staphylococcus aureus. J Appl Bacteriol 75, 123-128.
20. Fux, C., Costerton, J., Stewart, P. and Stoodley, P. (2005) Survival strategies of infectious biofilms. Trends Microbiol 13, 34-40.
21. Gemmell, C. (1995) Antibiotics and the expression of staphylococcal virulence. J Antimicrob Chemother 36, 283-291.
22. Gemmell, C. and Ford, C. (2002) Virulence factor expression by Gram-positive cocci exposed to subinhibitory concentrations of linezolid. J Antimicrob Chemother 50, 665-672.
23. Grinius, L., Morris, C., Curnow, A., Hu, X. and Demuth, T. (2001) Identification and characterization of new signal peptidase inhibitors among 5S-penems. Abstr Intersci Conf Antimicrob Agents Chemother Intersci Conf Antimicrob Agents Chemother (41st: Chicago, Ill). Abstract no. F-388.
24. Hanlon, G., Denyer, S., Hodges, N., Brant, J., Lansley, A. and Al-Rustamani, W. (2004) Biofilm formation and changes in bacterial cell surface hydrophobicity during growth in a CAPD model system. J Pharm Pharmacol 56, 847-854.
25. Harris, D., Powers, M. and Romesberg, F. (2009) Synthesis and biological evaluation of penem inhibitors of bacterial signal peptidase. Bioorg Med Chem Lett 19, 3787-3790.
26. Herbert, S., Barry, P. and Novick, R. (2001) Subinhibitory clindamycin differentially inhibits transcription of exoprotein genes in Staphylococcus aureus. Infect Immun 69, 2996-3003.
27. Hodgson, A., Nelson, S., Brown, M. and Gilbert, P. (1995) A simple in vitro model for growth control of bacterial bio-films. J Appl Bacteriol 79, 87-93.
28. Hogan, D. and Kolter, R. (2002) Why are bacteria refractory to antimicrobials? Curr Opin Microbiol 5, 472-477.
29. Hu, E., Kim, N., Grinius, L., Morris, C., Wallace, C., Mieling, G. and Demuth, T. (2003) Synthesis of (5S)-tricyclic penems as novel and potent inhibitors of bacterial signal peptidases. Synthesis 11, 1732-1738.
30. Jonsson, P., Lindberg, M., Haraldsson, I. and Wadstrom, T. (1985) Virulence of Staphylococcus aureus in a mouse mastitis model: studies of alpha hemolysin, coagulase, and protein A as possible virulence determinants with protoplast fusion and gene cloning. Infect Immun 49, 765-769.
31. Komori, Y., Bernardo, K., Kronke, M. and Krut, O. (2007) Effects of capsaicin on intestinal cephalexin absorption in rats. Biol Pharm Bull 30, 547.
32. Koszczol, C., Bernardo, K., Kronke, M. and Krut, O. (2006) Subinhibitory quinupristin?dalfopristin attenuates virulence of Staphylococcus aureus. J Antimicrob Chemother 58, 564-574.
33. Kum, W., Laupland, K., See, R. and Chow, A. (1993) Improved purification and biologic activities of staphylococcal toxic shock syndrome toxin 1. J Clin Microbiol 31, 2654-2660.
34. Lammertyn, E., Van Mellaert, L., Meyen, E., Lebeau, I., De Buck, E., Anne, J. and Geukens, N. (2004) Molecular and functional characterization of type I signal peptidase from Legionella pneumophila. Microbiology 150 (Pt 5), 1475-1483.
35. Lee, J. and Bohach, G. (2004) Pathogenesis of disease. In Staphylococcus aureus, Molecular and Clinical Aspects ed. Ala'Aldeen, D. and Hiramatsu, K. pp. 177-236. Chichester, UK: Horwood publishing.
36. Lowy, F. (1998) Staphylococcus aureus infections. N Engl J Med 339, 520-532.
37. Lyu, S. and Park, W. (2006) Mistletoe lectin (Viscum album coloratum) modulates proliferation and cytokine expressions in murine splenocytes. J Biochem Mol Biol 39, 662-670.
38. Masadeh, M. (2005) Studies on the effects of sub-minimal inhibitory concentrations of antibiotics on the virulence factors of biofilm bacteria. PhD Thesis, University of Abertay Dundee, Dundee, UK.
39. McDevitt, D., Vaudaux, P. and Foster, T. (1992) Genetic evidence that bound coagulase of Staphylococcus aureus is not clumping factor. Infect Immun 60, 1514-1523.
40. Micusan, V., Mercier, G., Bhatti, A., Reiser, R., Bergdoll, M. and Oth, D. (1986) Production of human and murine interleukin-2 by toxic shock syndrome toxin-1. Immunology 58, 203-208.
41. Moneib, N., Shibl, A., el-Said, M. and el-Masry, E. (1993) Macrolides induced suppression of virulence factors produced by Staphylococcus aureus. J Chemother 5, 289-292.
42. Ohlsen, K., Ziebuhr, W., Koller, K., Hell, W., Wichelhaus, T. and Hacker, J. (1998) Effects of subinhibitory concentrations of antibiotics on alpha-toxin (hla) gene expression of methicillin-sensitive and methicillin-resistant Staphylococcus aureus isolates. Antimicrob Agents Chemother 42, 2817-2823.
43. Paetzel, M., Dalbey, R. and Strynadka, N. (1998) Crystal structure of a bacterial signal peptidase in complex with a betalactam inhibitor. Nature 396, 186-190.
44. Perez-Giraldo, C., Rodriguez-Benito, A., Moran, F., Hurtado, C., Blanco, M., Rachid, S., Ohlsen, K., Witte, W. and Gomez-Garcia, A. (1994) In-vitro slime production by Staphylococcus epidermis in the presence of subinhibitory concentrations of ciprofloxacin, ofloxacin and sparfloxacin. J Antimicrob Chemother 33, 845-848.
45. Rachid, S., Ohlsen, K., Witte, W., Hacker, J. and Zeibuhr, W. (2000) Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermis. Antimicrob Agents Chemother 44, 3357-3363.
46. Reiser, R., Robbins, R., Khoe, G. and Bergdoll, M. (1983) Purification and some physicochemical properties of toxic-shock toxin. Biochemistry 22, 3907-3912.
47. Rupp, M. and Hamer, K. (1998) Effect of subinhibitory concentrations of vancomycin, cefazolin, ofloxacin, L-ofloxacin and D-ofloxacin on adherence to intravascular catheters and biofilm formation by Staphylococcus epidermidis. J Antimicrob Chemother 41, 155-161.
48. Sawai, T., Tomono, K., Yanagihara, K., Yamamoto, Y., Kaku, M., Hirakata, Y., Koga, H., Tashiro, T. et al. (1997) Role of coagulase in a murine model of hematogenous pulmonary infection induced by intravenous injection of Staphylococcus aureus enmeshed in agar beads. Infect Immun 65, 466-471.
49. Schlievert, P. (2005) Comment on: staphylococcal toxic shock syndrome: still a problem. Med J Aust 182, 651-652.
50. Schlievert, P., Tripp, T. and Peterson, M. (2004) Re-emergence of staphylococcal toxic shock syndrome in Minneapolis-St. Paul, Minnesota, during the 2000-2003 Surveillance Period. J Clin Microbiol 42, 2875-2876.
51. Shen, L., Shi, Y., Zhang, D., Wei, J., Surette, M. and Duan, K. (2008) Modulation of secreted virulence factor genes by subinhibitory concentrations of antibiotics in Pseudomonas aeruginosa. J Microbiol, 46, 441-447.
52. Sibbald, M., Ziebandt, A., Engelmann, S., Hecker, M., de Jong, A., Harmsen, H., Raangs, G., Stokroos, I. et al. (2006) Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70, 755-788.
53. Stepanovic, S., Vukovic, D., Dakic, I., Savic, B. and Svabic-Vlahovic, M. (2000) A modified microtitre-plate test for quantification of staphylococcal biofilm formation. J Microbiol Meth 40, 175-179.
54. Stevens, D., Ma, Y., Salmi, D., McIndoo, E., Wallace, R. and Bryant, A. (2007) Impact of antibiotics on expression of virulence-associated exotoxin genes in methicillin-sensitive and methicillin-resistant Staphylococcus aureus. J Infect Dis 195, 202-211.
55. Vuong, C. and Otto, M. (2002) Staphylococcus epidermidis infections. Microbes Infect 4, 481-489.
56. Winder, C., Al-Adham, I., Abdel Malek, S., Buultjens, T., Horrocks, A. and Collier, P. (2000) Outer membrane protein shifts in biocide resistant Pseudomonas aeruginosa PAO1. J Appl Microbiol 89, 289-295.
57. Yanagihara, K., Tashiro, M., Fukuda, Y., Ohno, H., Higashiyama, Y., Miyazaki, Y., Hirakata, Y., Tomono, K. et al. (2006) Effects of short interfering RNA against methicillin-resistant Staphylococcus aureus coagulase in vitro and in vivo. J Antimicrob Chemother 57, 122-126.