Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3978-3991

  Vergara Irigaray, Marta ^a   Valle, Jaione ^a   Merino, Nekane ^a   Latasa, Cristina ^a   García, Begoña ^a   De Los Mozos, Igor Ruiz ^a   Solano, Cristina ^a   Toledo Arana, Alejandro ^a   Penadés, José R ^b   Lasa, Iñigo ^a  

^a PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^b INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EXOPOLYSACCHARIDE; FIBRONECTIN BINDING PROTEIN; GLUCOSE; MEMBRANE PROTEIN; N ACETYLGLUCOSAMINE; POLY N ACETYLGLUCOSAMINE; POLYSACCHARIDE INTERCELLULAR ADHESIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM ISOLATE; BIOFILM; CATHETER INFECTION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MUTATIONAL ANALYSIS; NONHUMAN; OSMOTIC STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCANNING ELECTRON MICROSCOPY;

ACETYLGLUCOSAMINE; ADHESINS, BACTERIAL; BACTERIAL PROTEINS; BIOFILMS; CATHETER-RELATED INFECTIONS; HUMANS; POLYSACCHARIDES, BACTERIAL; SOS RESPONSE (GENETICS); STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANS-ACTIVATORS;

EID: 69049112927     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00616-09     Document Type: Article

References (57)

1. Arnaud, M., A. Chastanet, and M. Débarbouillé. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891.
2. Arrizubieta, M. J., A. Toledo-Arana, B. Amorena, J. R. Penades, and I. Lasa. 2004. Calcium inhibits Bap-dependent multicellular behavior in Staphylococcus aureus. J. Bacteriol. 186:7490-7498.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1990. Current protocols in molecular biology. John Wiley & Sons, New York, NY.
4. Bateman, B. T., N. P. Donegan, T. M. Jarry, M. Palma, and A. L. Cheung. 2001. Evaluation of a tetracycline-inducible promoter in Staphylococcus aureus in vitro and in vivo and its application in demonstrating the role of sigB in microcolony formation. Infect. Immun. 69:7851-7857.
5. Beenken, K. E., J. S. Blevins, and M. S. Smeltzer. 2003. Mutation of sarA in Staphylococcus aureus limits biofilm formation. Infect. Immun. 71:4206-4211.
6. Beenken, K. E., P. M. Dunman, F. McAleese, D. Macapagal, E. Murphy, S. J. Projan, J. S. Blevins, and M. S. Smeltzer. 2004. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186:4665-4684.
7. Bisognano, C., W. L. Kelley, T. Estoppey, P. Francois, J. Schrenzel, D. Li, D. P. Lew, D. C. Hooper, A. L. Cheung, and P. Vaudaux. 2004. A recALexA-dependent pathway mediates ciprofloxacin-induced fibronectin binding in Staphylococcus aureus. J. Biol. Chem. 279:9064-9071.
8. Boles, B. R., and A. R. Horswill. 2008. Agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog. 4:e1000052.
9. Corrigan, R. M., D. Rigby, P. Handley, and T. J. Foster. 2007. The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153:2435-2446.
10. Cramton, S. E., C. Gerke, N. F. Schnell, W. W. Nichols, and F. Gotz. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
11. Cucarella, C., C. Solano, J. Valle, B. Amorena, I. Lasa, and J. R. Penades. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896.
12. Donlan, R. M., and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167-193.
13. Fischer, B., P. Vaudaux, M. Magnin, Y. el Mestikawy, R. A. Proctor, D. P. Lew, and H. Vasey. 1996. Novel animal model for studying the molecular mechanisms of bacterial adhesion to bone-implanted metallic devices: role of fibronectin in Staphylococcus aureus adhesion. J. Orthop. Res. 14:914-920.
14. Fitzpatrick, F., H. Humphreys, and J. P. O'Gara. 2005. Evidence for icaADBC-independent biofilm development mechanism in methicillin-resistant Staphylococcus aureus clinical isolates. J. Clin. Microbiol. 43:1973-1976.
15. Fluckiger, U., M. Ulrich, A. Steinhuber, G. Doring, D. Mack, R. Landmann, C. Goerke, and C. Wolz. 2005. Biofilm formation, icaADBC transcription, and polysaccharide intercellular adhesin synthesis by staphylococci in a device-related infection model. Infect. Immun. 73:1811-1819.
16. Francois, P., P. H. Tu Quoc, C. Bisognano, W. L. Kelley, D. P. Lew, J. Schrenzel, S. E. Cramton, F. Gotz, and P. Vaudaux. 2003. 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. 35:135-140.
17. Greene, C., D. McDevitt, P. Francois, P. E. Vaudaux, D. P. Lew, and T. J. Foster. 1995. Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol. Microbiol. 17:1143-1152.
18. Heilmann, C., C. Gerke, F. Perdreau-Remington, and F. Gotz. 1996. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun. 64:277-282.
19. Heilmann, C., O. Schweitzer, C. Gerke, N. Vanittanakom, D. Mack, and F. Gotz. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20:1083-1091.
20. Hennig, S., S. Nyunt Wai, and W. Ziebuhr. 2007. Spontaneous switch to PIA-independent biofilm formation in an ica-positive Staphylococcus epidermidis isolate. Int. J. Med. Microbiol. 297:117-122.
21. Herman, R. A., V. R. Kee, K. G. Moores, and M. B. Ross. 2008. Etiology and treatment of community-associated methicillin-resistant Staphylococcus aureus. Am. J. Health Syst. Pharm. 65:219-225.
22. Kaplan, J. B., K. Velliyagounder, C. Ragunath, H. Rohde, D. Mack, J. K. Knobloch, and N. Ramasubbu. 2004. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J. Bacteriol. 186:8213-8220.
23. Keane, F. M., A. W. Clarke, T. J. Foster, and A. S. Weiss. 2007. The N-terminal A domain of Staphylococcus aureus fibronectin-binding protein A binds to tropoelastin. Biochemistry 46:7226-7232.
24. Kennedy, A. D., M. Otto, K. R. Braughton, A. R. Whitney, L. Chen, B. Mathema, J. R. Mediavilla, K. A. Byrne, L. D. Parkins, F. C. Tenover, B. N. Kreiswirth, J. M. Musser, and F. R. Deleo. 2008. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc. Natl. Acad. Sci. USA 105:1327-1332.
25. Kristian, S. A., T. Golda, F. Ferracin, S. E. Cramton, B. Neumeister, A. Peschel, F. Gotz, and R. Landmann. 2004. The ability of biofilm formation does not influence virulence of Staphylococcus aureus and host response in a mouse tissue cage infection model. Microb. Pathog. 36:237-245.
26. Kropec, A., T. Maira-Litran, K. K. Jefferson, M. Grout, S. E. Cramton, F. Gotz, D. A. Goldmann, and G. B. Pier. 2005. Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect. Immun. 73:6868-6876.
27. Kuroda, M., R. Ito, Y. Tanaka, M. Yao, K. Matoba, S. Saito, I. Tanaka, and T. Ohta. 2008. Staphylococcus aureus surface protein SasG contributes to intercellular autoaggregation of Staphylococcus aureus. Biochem. Biophys. Res. Commun. 377:1102-1106.
28. Lim, Y., M. Jana, T. T. Luong, and C. Y. Lee. 2004. Control of glucose- and NaCl-induced biofilm formation by rbf in Staphylococcus aureus. J. Bacteriol. 186:722-729.
29. Little, J. W. 1993. LexA cleavage and other self-processing reactions. J. Bacteriol. 175:4943-4950.
30. Maira-Litran, T., A. Kropec, D. A. Goldmann, and G. B. Pier. 2005. Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated staphylococcal poly-N-acetyl-β-(1-6)-glucosamine. Infect. Immun. 73:6752-6762.
31. Mazmanian, S. K., G. Liu, E. R. Jensen, E. Lenoy, and O. Schneewind. 2000. Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. Proc. Natl. Acad. Sci. USA 97:5510-5515.
32. Mckenney, D., K. Pouliot, V. Wang, V. Murthy, M. Ulrich, G. Dšring, J. C. Lee, D. A. Goldmann, and G. B. Pier. 1999. Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284:1523-1527.
33. Merino, N., A. Toledo-Arana, M. Vergara-Irigaray, J. Valle, C. Solano, E. Calvo, J. A. Lopez, T. J. Foster, J. R. Penades, and I. Lasa. 2009. Protein A-mediated multicellular behavior in Staphylococcus aureus. J. Bacteriol. 191:832-843.
34. Novick, R. P. 1991. Genetic systems in staphylococci. Methods Enzymol. 204:587-636.
35. Novick, R. P. 1990. The Staphylococcus as a molecular genetic system, p. 1-37. In R. P. Novick (ed.), Molecular biology of the Staphylococcus. VCH Publishers, New York, NY.
36. O'Neill, E., C. Pozzi, P. Houston, H. Humphreys, D. A. Robinson, A. Loughman, T. J. Foster, and J. P. O'Gara. 2008. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J. Bacteriol. 190:3835-3850.
37. O'Neill, E., C. Pozzi, P. Houston, D. Smyth, H. Humphreys, D. A. Robinson, and J. P. O'Gara. 2007. Association between methicillin susceptibility and biofilm regulation in Staphylococcus aureus isolates from device-related infections. J. Clin. Microbiol. 45:1379-1388.
38. Pattee, P. A. 1981. Distribution of Tn551 insertion sites responsible for auxotrophy on the Staphylococcus aureus chromosome. J. Bacteriol. 145:479-488.
39. Prigent-Combaret, C., G. Prensier, T. T. Le Thi, O. Vidal, P. Lejeune, and C. Dorel. 2000. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ. Microbiol. 2:450-464.
40. Queck, S. Y., M. Jameson-Lee, A. E. Villaruz, T. H. Bach, B. A. Khan, D. E. Sturdevant, S. M. Ricklefs, M. Li, and M. Otto. 2008. RNAIII-independent target gene control by the agr quorum-sensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol. Cell 32:150-158.
41. Rachid, S., S. Cho, K. Ohlsen, J. Hacker, and W. Ziebuhr. 2000. Induction of Staphylococcus epidermidis biofilm formation by environmental factors: the possible involvement of the alternative transcription factor sigB. Adv. Exp. Med. Biol. 485:159-166.
42. Rachid, S., K. Ohlsen, W. Witte, J. Hacker, and W. Ziebuhr. 2000. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob. Agents Chemother. 44:3357-3363.
43. Roche, F. M., R. Downer, F. Keane, P. Speziale, P. W. Park, and T. J. Foster. 2004. The N-terminal A domain of fibronectin-binding proteins A and B promotes adhesion of Staphylococcus aureus to elastin. J. Biol. Chem. 279:38433-38440.
44. Saravia-Otten, P., H. P. Muller, and S. Arvidson. 1997. Transcription of Staphylococcus aureus fibronectin binding protein genes is negatively regulated by agr and an agr-independent mechanism. J. Bacteriol. 179:5259-5263.
45. Shanks, R. M., N. P. Donegan, M. L. Graber, S. E. Buckingham, M. E. Zegans, A. L. Cheung, and G. A. O'Toole. 2005. Heparin stimulates Staphylococcus aureus biofilm formation. Infect. Immun. 73:4596-4606.
46. Shanks, R. M. Q., M. A. Meehl, K. M. Brothers, R. M. Martinez, N. P. Donegan, M. L. Graber, A. L. Cheung, and G. A. O'Toole. 2008. Genetic evidence for an alternative citrate-dependent biofilm formation pathway of Staphylococcus aureus that is dependent on fibronectin binding proteins and the GraRS two-component regulatory system. Infect. Immun. 76:2469-2477.
47. Sinha, B., P. Francois, Y. A. Que, M. Hussain, C. Heilmann, P. Moreillon, D. Lew, K. H. Krause, G. Peters, and M. Herrmann. 2000. Heterologously expressed Staphylococcus aureus fibronectin-binding proteins are sufficient for invasion of host cells. Infect. Immun. 68:6871-6878.
48. Sinha, B., P. P. Francois, O. Nusse, M. Foti, O. M. Hartford, P. Vaudaux, T. J. Foster, D. P. Lew, M. Herrmann, and K. H. Krause. 1999. Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin alpha5beta1. Cell Microbiol. 1:101-117.
49. Toledo-Arana, A., N. Merino, M. Vergara-Irigaray, M. Debarbouille, J. R. Penades, and I. Lasa. 2005. Staphylococcus aureus develops an alternative, ica-independent biofilm in the absence of the arlRS two-component system. J. Bacteriol. 187:5318-5329.
50. Tormo, M. A., E. Knecht, F. Gotz, I. Lasa, and J. R. Penades. 2005. Bap-dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology 151:2465-2475.
51. Traber, K. E., E. Lee, S. Benson, R. Corrigan, M. Cantera, B. Shopsin, and R. P. Novick. 2008. agr function in clinical Staphylococcus aureus isolates. Microbiology 154:2265-2274.
52. Ubeda, C., E. Maiques, E. Knecht, I. Lasa, R. P. Novick, and J. R. Penades. 2005. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 56:836-844.
53. B is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48:1075-1087.
54. Vuong, C., H. L. Saenz, F. Gotz, and M. Otto. 2000. Impact of the agr quorum-sensing system on adherence to polystyrene in Staphylococcus aureus. J. Infect. Dis. 182:1688-1693.
55. Wann, E. R., S. Gurusiddappa, and M. Hook. 2000. The fibronectin-binding MSCRAMM FnbpA of Staphylococcus aureus is a bifunctional protein that also binds to fibrinogen. J. Biol. Chem. 275:13863-13871.
56. Wolz, C., P. Pohlmann-Dietze, A. Steinhuber, Y. T. Chien, A. Manna, W. van Wamel, and A. Cheung. 2000. Agr-independent regulation of fibronectin-binding protein(s) by the regulatory locus sar in Staphylococcus aureus. Mol. Microbiol. 36:230-243.
57. Xiong, Y. Q., A. S. Bayer, M. R. Yeaman, W. Van Wamel, A. C. Manna, and A. L. Cheung. 2004. Impacts of sarA and agr in Staphylococcus aureus strain Newman on fibronectin-binding protein A gene expression and fibronectin adherence capacity in vitro and in experimental infective endocarditis. Infect. Immun. 72:1832-1836.