Induction of fibronectin adhesins in quinolone-resistant Staphylococcus aureus by subinhibitory levels of ciprofloxacin or by sigma B transcription factor activity is mediated by two separate pathways

Antimicrobial Agents and Chemotherapy

Volumn 49, Issue 3, 2005, Pages 916-924

  Li, Dongmei ^a   Renzoni, Adriana ^a   Estoppey, Tristan ^a   Bisognano, Carmelo ^a   Francois, Patrice ^a   Kelley, William L ^a   Lew, Daniel P ^a   Schrenzel, Jacques ^a   Vaudaux, Pierre ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL RNA; CIPROFLOXACIN; DNA TOPOISOMERASE IV; FIBRONECTIN BINDING PROTEIN; LEXA PROTEIN; PROTEINASE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RECA PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SIGMA B; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; ASP23 GENE; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; CONTROLLED STUDY; DNA REPAIR; FLOW CYTOMETRY; FNBA GENE; FNBB GENE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPERON; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REGULON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RSBU GENE; SARA GENE; SIGB GENE; STAPHYLOCOCCUS AUREUS; STRESS;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; CIPROFLOXACIN; DRUG RESISTANCE, BACTERIAL; FIBRONECTINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGMA FACTOR; STAPHYLOCOCCUS AUREUS; TRANS-ACTIVATORS;

EID: 14744270782     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.49.3.916-924.2005     Document Type: Article

References (66)

1. Arvidson, S., and K. Tegmark. 2001. Regulation of virulence determinants in Staphylococcus aureus. Int. J. Med. Microbiol. 291:159-170.
2. Bischoff, M., P. Dunman, J. Kormanec, D. Macapagal, E. Murphy, W. Mounts, B. Berger-Bachi, and S. Projan. 2004. Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J. Bacteriol. 186:4085-4099.
3. Bischoff, M., J. M. Entenza, and P. Giachino. 2001. Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus. J. Bacteriol. 183:5171-5179.
4. 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 RecA-LexA-dependent pathway mediates ciprofloxacin-induced fibronectin binding in Staphylococcus aureus. J. Biol. Chem. 279:9064-9071.
5. Bisognano, C., P. Vaudaux, D. P. Lew, E. Y. W. Ng, and D. C. Hooper. 1997. Increased expression of fibronectin-binding proteins by fluoroquinolone-resistant Staphylococcus aureus exposed to subinhibitory levels of ciprofloxacin. Antimicrob. Agents Chemother. 41:906-913,
6. Bisognano, C., P. Vaudaux, P. Rohner, D. P. Lew, and D. C. Hooper. 2000. Induction of fibronectin-binding proteins and increased adhesion of quinolone-resistant Staphylococcus aureus by subinhibitory levels of ciprofloxacin. Antimicrob. Agents Chemother. 44:1428-1437.
7. Blevins, J. S., K. E. Beenken, M. O. Elasri, B. K. Hurlburt, and M. S. Smeltzer. 2002. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect. Immun. 70:470-480.
8. Blevins, J. S., A. F. Gillaspy, T. M. Rechtin, B. K. Hurlburt, and M. S. Smeltzer. 1999. The staphylococcal accessory regulator (sar) represses transcription of the Staphylococcus aureus collagen adhesin gene (cna) in an agr-independent manner. Mol. Microbiol. 33:317-326.
9. Brown, T., and K. Mackey. 1997. Analysis of RNA by Northern and slot blot hybridization, p. 4.9.1-4.9.16. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. John Wiley & Sons, Inc., New York, N.Y.
10. Cheung, A. L., A. S. Bayer, G. Zhang, H. Gresham, and Y. Q. Xiong. 2004 Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol. Med. Microbiol. 40:1-9.
11. Cheung, A. L., M. G. Bayer, and J. H. Heinrichs. 1997. sar genetic determinants necessary for transcription of RNAII and RNAIII in the agr locus of Staphylococcus aureus. J. Bacteriol. 179:3963-3971.
12. Cheung, A. L., Y. T. Chien, and A. S. Bayer. 1999. Hyperproduction of alpha-hemolysin in a sigB mutant is associated with elevated SarA expression in Staphylococcus aureus. Infect. Immun. 67:1331-1337.
13. Cheung, A. L., S. J. Projan, and H. Gresham. 2002. The genomic aspect of virulence, sepsis, and resistance to killing mechanisms in Staphylococcus aureus. Curr. Infect. Dis. Rep. 4:400-410.
14. Crossley, K. B., and G. L. Archer. 1997. The staphylococci in human disease. Churchill Livingstone, New York, N.Y.
15. SB of Staphylococcus aureus: characterization and role in transcription of the global regulatory locus sar. J. Bacteriol. 179:6355-6359.
16. Dubrac, S., and T. Msadek. 2004. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J. Bacteriol. 186:1175-1181.
17. Dunman, P. M., E. Murphy, S. Haney, D. Palacios, G. Tucker-Kellogg, S. Wu, E. L. Brown, R. J. Zagursky, D. Shlaes, and S. J. Projan. 2001. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183:7341-7353.
18. 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.
19. Fournier, B., A. Klier, and G. Rapoport. 2001. The two-component system ArlS-ArlR is a regulator of virulence gene expression in Staphylococcus aureus. Mol. Microbiol. 41:247-261.
20. Fowler, T., E. R. Wann, D. Joh, S. A. Johansson, T. J. Foster, and M. Höök. 2000. Cellular invasion by Staphylococcus aureus involves a fibronectin bridge between the bacterial fibronectin-binding MSCRAMMs and host cell β1 integrins. Eur. J. Cell Biol. 79:672-679.
21. Francois, P., J. Schrenzel, C. Stoerman-Chopard, H. Favre, M. Herrmann, T. J. Foster, D. P. Lew, and P. Vaudaux. 2000. Identification of plasma proteins adsorbed on hemodialysis tubing that promote Staphylococcus aureus adhesion. J. Lab. Clin. Med. 135:32-42.
22. Fujimoto, D. F., E. W. Brunskill, and K. W. Bayles. 2000. Analysis of genetic elements controlling Staphylococcus aureus lrgAB expression: potential role of DNA topology in SarA regulation. J. Bacteriol. 182:4822-4828.
23. B-dependent transcription of sigB and asp23 in two different Staphylococcus aureus strains. Mol. Gen. Genet. 261:558-566.
24. B regulon in Staphylococcus aureus. J. Bacteriol. 182:6983-6991.
25. B activity depends on RsbU in Staphylococcus aureus. J. Bacteriol. 183:1843-1852.
26. Greene, C., D. McDevitt, P. François, P. 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.
27. Herbert, S., P. Barry, and R. P. Novick. 2001. Subinhibitory clindamycin differentially inhibits transcription of exoprotein genes in Staphylococcus aureus. Infect. Immun. 69:2996-3003.
28. B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184:5457-5467.
29. Huesca, M., R. Peralta, D. N. Sauder, A. E. Simor, and M. J. McGavin, 2002. Adhesion and virulence properties of epidemic Canadian methicillin-resistant Staphylococcus aureus strain 1: identification of novel adhesion functions associated with plasmin-sensitive surface protein. J. Infect. Dis. 185:1285-1296.
30. Karlsson, A., and S. Arvidson. 2002. Variation in extracellular protease production among clinical isolates of Staphylococcus aureus due to different levels of expression of the protease repressor SarA. Infect. Immun. 70:4239-4246.
31. Karlsson, A., P. Saravia-Otten, K. Tegmark, E. Morfeldt, and S. Arvidson. 2001. Decreased amounts of cell wall-associated protein A and fibronectin-binding proteins in Staphylococcus aureus sarA mutants due to up-regulation of extracellular proteases. Infect. Immun. 69:4742-4748.
32. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520-532.
33. Manna, A., and A. L. Cheung. 2001. Characterization of sarR, a modulator of sar expression in Staphylococcus aureus. Infect. Immun. 69:885-896.
34. Manna, A. C., M. G. Bayer, and A. L. Cheung. 1998. Transcriptional analysis of different promoters in the sar locus in Staphylococcus aureus. J. Bacteriol. 180:3828-3836.
35. Manna, A. C., and A. L. Cheung. 2003. sarU, a sarA homolog, is repressed by SarT and regulates virulence genes in Staphylococcus aureus. Infect. Immun. 71:343-353.
36. McGavin, M. J., C. Zahradka, K. Rice, and J. E. Scott. 1997. Modification of the Staphylococcus aureus fibronectin binding phenotype by V8 protease. Infect. Immun. 65:2621-2628.
37. McNamara, P. J., K. C. Milligan-Monroe, S. Khalili, and R. A. Proctor. 2000. Identification, cloning, and initial characterization of rot, a locus encoding a regulator of virulence factor expression in Staphylococcus aureus. J. Bacteriol. 182:3197-3203.
38. Miyazaki, E., J. M. Chen, C. Ko, and W. R. Bishai. 1999. The Staphylococcus aureus rsbW (orf159) gene encodes an anti-sigma factor of SigB. J. Bacteriol. 181:2846-2851.
39. Morfeldt, E., K. Tegmark, and S. Arvidson. 1996. Transcriptional control of the agr-dependent virulence gene regulator, RNAIII, in Staphylococcus aureus. Mol. Microbiol. 21:1227-1237.
40. Nair, S. P., M. Bischoff, M. M. Senn, and B. Berger-Bächi. 2003. The sigma B regulon influences internalization of Staphylococcus aureus by osteoblasts. Infect. Immun. 71:4167-4170.
41. NCCLS. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 6th ed. Approved standard M7-A6. NCCLS, Wayne, Pa. Infect. Immun. 71:4167-4170.
42. Nicholas, R. O., T. Li, D. McDevitt, A. Marra, S. Sucoloski, P. L. Demarsh, and D. R. Gentry. 1999. Isolation and characterization of a sigB deletion mutant of Staphylococcus aureus. Infect. Immun. 67:3667-3669.
43. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429-1449.
44. Novick, R. P., and D. Jiang. 2003. The staphylococcal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology 149:2709-2717.
45. Patti, J. M., B. L. Allen, M. J. McGavin, and M. Höök. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48:585-617.
46. Pragman, A. A., J. M. Yarwood, T. J. Tripp, and P. M. Schlievert. 2004. Characterization of virulence factor regulation by SrrAB, a two-component system in Staphylococcus aureus. J. Bacteriol. 186:2430-2438.
47. Projan, S. J., and R. P. Novick. 1997. The molecular basis of pathogenicity, p. 55-81. In K. B. Crossley and G. L. Archer (ed.), The staphylococci in human disease. Churchill Livingstone, New York, N.Y.
48. Renzoni, A., P. Francois, D. Li, W. L. Kelley, D. P. Lew, P. Vaudaux, and J. Schrenzel. 2004. Modulation of fibronectin adhesins and other virulence factors in a teicoplanin-resistant derivative of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 48:2958-2965.
49. Rice, K., M. Huesca, D. Vaz, and M. J. McGavin. 2001. Variance in fibronectin binding and fnb locus polymorphisms in Staphylococcus aureus: identification of antigenic variation in a fibronectin binding protein adhesin of the epidemic CMRSA-1 strain of methicillin-resistant S. aureus. Infect. Immun. 69:3791-3799.
50. Rosner, B. 1990. Analysis of variance, p. 474-526. In M. R. Payne, S. Hankinson, and S. London (ed.), Fundamentals of biostatistics. PWS-KENT Publishing Company, Belmont, Calif.
51. Said-Salim, B., P. M. Dunman, F. M. McAleese, D. Macapagal, E. Murphy, P. J. McNamara, S. Arvidson, T. J. Foster, S. J. Projan, and B. N. Kreiswirth. 2003. Global regulation of Staphylococcus aureus genes by Rot. J. Bacteriol. 185:610-619.
52. Sakoulas, G., G. M. Eliopoulos, R. C. J. Moellering, R. P. Novick, L. Venkataraman, C. Wennersten, P. C. Degirolami, M. J. Schwaber, and H. S. Gold. 2003. Staphylococcus aureus accessory gene regulator (agr) group II: is there a relationship to the development of intermediate-level glycopeptide resistance? J. Infect. Dis. 187:929-938.
53. Sakoulas, G., G. M. Eliopoulos, R. C. J. Moellering, C. Wennersten, L. Venkataraman, R. P. Novick, and H. S. Gold. 2002. Accessory gene regulator (agr) locus in geographically diverse Staphylococcus aureus isolates with reduced susceptibility to vancomycin. Antimicrob. Agents Chemother. 46:1492-1502.
54. Saravia-Otten, P., H. P. Müller, 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.
55. Savolainen, K., L. Paulin, B. Westerlund-Wikström, T. J. Foster, T. K. Korhonen, and P. Kuusela. 2001. Expression of pls, a gene closely associated with the mecA gene of methicillin-resistant Staphylococcus aureus, prevents bacterial adhesion in vitro. Infect. Immun. 69:3013-3020.
56. Schmidt, K. A., A. C. Manna, S. Gill, and A. L. Cheung. 2001. SarT, a represser of α-hemolysin in Staphylococcus aureus. Infect. Immun. 69:4749-4758.
57. Sinha, B., P. P. Francois, O. Nüsse, 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. 1:101-118.
58. Vaudaux, P., P. Francois, C. Bisognano, W. L. Kelley, D. P. Lew, J. Schrenzel, R. A. Proctor, P. J. McNamara, G. Peters, and C. Von Eiff. 2002. Increased expression of clumping factor and fibronectin-binding proteins by hemB mutants of Staphylococcus aureus expressing small colony variant phenotypes. Infect. Immun. 70:5428-5437.
59. Vaudaux, P., P. Francois, D. P. Lew, and F. A. Waldvogel. 2000. Host factors predisposing to and influencing therapy of foreign body infections, p. 1-26. In F. A. Waldvogel and A. L. Bisno (ed.), Infections associated with indwelling medical devices. American Society for Microbiology, Washington, D.C.
60. Vaudaux, P., V. Monzillo, P. Francois, D. P. Lew, T. J. Foster, and B. Berger-Bächi. 1998. Introduction of the mec element (methicillin resistance) into Staphylococcus aureus alters in vitro functional activities of fibrinogen and fibronectin adhesins. Antimicrob. Agents Chemother. 42:564-570.
61. Windle, H. J., and D. Kelleher. 1997. Identification and characterization of a metalloprotease activity from Helicobacter pylori. Infect. Immun. 65:3132-3137.
62. Wolz, C., P. Pöhlmann-Dietze, A. Steinhuber, Y. T. Chien, A. Manna, W. Van Wamel, and A. L. Cheung. 2000. Agr-independent regulation of fibronectin-binding protein(s) by the regulatory locus sar in Staphylococcus aureus. Mol. Microbiol. 36:230-243.
63. Wu, S. W., H. De Lencastre, and A. Tomasz. 1996. Sigma-B, a putative operon encoding alternate sigma factor of Staphylococcus aureus RNA polymerase: molecular cloning and DNA sequencing. J. Bacteriol. 178:6036-6042.
64. 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.
65. Yarwood, J. M., J. K. McCormick, and P. M. Schlievert. 2001. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 183:1113-1123.
66. Yarwood, J. M., and P. M. Schlievert. 2003. Quorum sensing in Staphylococcus infections. J. Clin. Investig. 112:1620-1625.