SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development

Journal of Bacteriology

Volumn 187, Issue 7, 2005, Pages 2348-2356

  Tormo, María Ángeles ^a   Martí, Miguel ^a   Valle, Jaione ^b   Manna, Adhar C ^d   Cheung, Ambrose L ^d   Lasa, Iñigo ^b   Penadés, José R ^a,c  

^a UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

^b CSIC   (Spain)

^c INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; OLIGONUCLEOTIDE; POLYSACCHARIDE; SMAD ANCHOR FOR RECEPTOR ACTIVATION; VIRULENCE FACTOR;

ARTICLE; BACTERIAL STRAIN; BIOFILM; GEL MOBILITY SHIFT ASSAY; GENETIC COMPLEMENTATION; MUTATION; OPERON; PLASMID; PRIORITY JOURNAL; PROTEIN PURIFICATION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

ACETYLGLUCOSAMINE; BACTERIAL PROTEINS; BASE SEQUENCE; BIOFILMS; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MUTATION; OPERON; POLYSACCHARIDES; POLYSACCHARIDES, BACTERIAL; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; STAPHYLOCOCCUS EPIDERMIDIS; TRANS-ACTIVATORS; UP-REGULATION;

EID: 15244358390     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.7.2348-2356.2005     Document Type: Article

References (51)

1. Arnaud, M., A. Chastanet, and M. Debarbouille. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891.
2. Augustin, J., R. Rosenstein, B. Wieland, U. Schneider, N. Schnell, G. Engelke, K. D. Entian, and F. Götz. 1992. Genetic analysis of epidermin biosynthetic genes and epidermin-negative mutants of Staphylococcus epidermidis. Eur. J. Biochem. 204:1149-1154.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Strahl. 1990. Current protocols in molecular biology. John Wiley & Sons, New York, N.Y.
4. 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.
5. Chan, P. F., and S. J. Foster. 1998. Role of SarA in virulence determinant production and environmental signal transduction in Staphylococcus aureus. J. Bacteriol. 180:6232-6241.
6. Chien, Y. T., A. C. Manna, S. J. Projan, and A. L. Cbeung. 1999. SarA, a global regulator of virulence determinants in Staphylococcus aureus, binds to a conserved motif essential for sar-dependent gene regulation. J. Biol. Chem. 274:37169-37176.
7. Conlon, K. M., H. Humphreys, and J. P. O'Gara. 2002. icaR encodes a transcriptional repressor involved in environmental regulation of ica operon expression and biofilm formation in Staphylococcus epidermidis. J. Bacteriol. 184:4400-4408.
8. Conlon, K. M., H. Humphreys, and J. P. O'Gara. 2002. Regulation of icaR gene expression in Staphylococcus epidermidis. FEMS Microbiol. Lett. 216:171-177.
9. Cramton, S. E., C. Gerke, N. F. Schnell, W. W. Michels, and F. Götz. 1999. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect. Immun. 67:5427-5433.
10. Cramton, S. E., M. Ulrich, F. Götz, and G. Doring. 2001. Anaerobic conditions induce expression of polysaccharide intercellular adhesin in Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69:4079-4085.
11. Cucarella, C., C. Solano, J. Valle, B. Amorena, I. Lasa, and J. R. Penadés. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-2896.
12. Dobinsky, S., K. Kiel, H. Rohde, K. Bartscht, J. K. Knobloch, M. A. Horstkotte, and D. Mack. 2003. Glucose-related dissociation between icaADBC transcription and biofilm expression by Staphylococcus epidermidis: evidence for an additional factor required for polysaccharide intercellular adhesin synthesis. J. Bacteriol. 185:2879-2886.
13. Dubin, G., D. Chmiel, P. Mak, M. Rakwalska, M. Rzychon, and A. Dubin. 2001. Molecular cloning and biochemical characterisation of proteases from Staphylococcus epidermidis. Biol. Chem. 382:1575-1582.
14. Fluckiger, U., C. Wolz, and A. L. Cheung. 1998. Characterization of a sar homolog of Staphylococcus epidermidis. Infect. Immun. 66:2871-2878.
15. Frebourg, N. B., S. Lefebvre, S. Baert, and J. F. Lemeland. 2000. PCR-based assay for discrimination between invasive and contaminating Staphylococcus epidermidis strains. J. Clin. Microbiol. 38:877-880.
16. Galdbart, J. O., J. Allignet, H. S. Tung, C. Ryden, and N. El Solh. 2000. Screening for Staphylococcus epidermidis markers discriminating between skin-flora strains and those responsible for infections of joint prostheses. J. Infect. Dis. 182:351-355.
17. Ghigo, J. M. 2001. Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442-445.
18. Götz, F. 2002. Staphylococcus and biofilms. Mol. Microbiol. 43:1367-1378.
19. Götz, F., B. Kreutz, and K. H. Schleifer. 1983. Protoplast transformation of Staphylococcus camosus by plasmid DNA. Mol. Gen. Genet. 189:340-342.
20. Götz, F., and B. Schumaker. 1987. Improvements of protoplast transformation in Staphylococcus camosus. FEMS Microbiol. Lett. 40:285-288.
21. Hancock, L. E., and M. Perego. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186:5629-5639.
22. Heilmann, C., C. Gerke, F. Perdreau-Remington, and F. Götz. 1996. Characterization of Tn917 insertion mutants of Staphylococcus epidermidis affected in biofilm formation. Infect. Immun. 64:277-282.
23. Heilmann, C., O. Schweitzer, C. Gerke, N. Vanittanakom, D. Mack, and F. Götz. 1996. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol. Microbiol. 20:1083-1091.
24. Jefferson, K. K., S. E. Cramton, F. Götz, and G. B. Pier. 2003. Identification of a 5-nucleotide sequence that controls expression of the ica locus in Staphylococcus aureus and characterization of the DNA-binding properties of IcaR. Mol. Microbiol. 48:889-899.
25. Jefferson, K. K., D. B. Pier, D. A. Goldmann, and G. B. Pier. 2004. The teicoplanin-associated locus regulator (TcaR) and the intercellular adhesin locus regulator (IcaR) are transcriptional inhibitors of the ica locus in Staphylococcus aureus. J. Bacteriol. 186:2449-2456.
26. 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 upregulation of extracellular proteases. Infect. Immun. 69:4742-4748.
27. B by repression of the negative regulator gene icaR. Infect. Immun. 72:3838-3848.
28. Knobloch, J. K. M., K. Bartscht, A. Sabottke, H. Rohde, H. H. Feucht, and D. Mack. 2001. Biofilm formation by Staphylococcus epidermidis depends on functional RsbU, an activator of the sigB operon: differential activation mechanisms due to ethanol and salt stress. J. Bacteriol. 183:2624-2633.
29. Kreiswirth, B. N., S. Lofdahl, M. J. Betley, M. O'Reilly, P. M. Schlievert, M. S. Bergdoll, and R. P. Novick. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712.
30. 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.
31. Livak, K. J., and T. D. Scbmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
32. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339:520-532.
33. Mack, D., W. Fischer, A. Krokotsch, K. Leopold, R. Hartmann, H. Egge, and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178:175-183.
34. Maira-Litran, T., A. Kropec, C. Abeygunawardana, J. Joyce, G. Mark, 3rd, D. A. Goldmann, and G. B. Pier. 2002. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect. Immun. 70:4433-4440.
35. Manna, A., and A. L. Cheung. 2001. Characterization of sarR, a modulator of sar expression in Staphylococcus aureus. Infect. Immun. 69:885-896.
36. 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.
37. McAleese, F. M., E. J. Walsh, M. Sieprawska, J. Potempa, and T. J. Foster. 2001. Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J. Biol. Chem. 276:29969-29978.
38. 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.
39. Novick, R. P. 1991. Genetic systems in staphylococci. Methods Enzymol. 204:587-636.
40. Pattee, P. A. 1981. Distribution of Tru551 insertion sites responsible for auxotrophy on the Staphylococcus aureus chromosome. J. Bacteriol. 145:479-488.
41. +) phenotype of Yersinia pestis is posttranscriptional. J. Bacteriol. 186: 1638-1647.
42. B is involved in regulation of biofilm expression in a Staphylococcus aureus mucosal isolate. J. Bacteriol. 182:6824-6826.
43. Rupp, M. E., P. D. Fey, C. Heilmann, and F. Götz. 2001. 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. 183:1038-1042.
44. Rupp, M. E., J. S. Ulphani, P. D. Fey, K. Bartscht, and D. Mack. 1999. 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. 67:2627-2632.
45. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
46. Shaw, L., E. Golonka, J. Potempa, and S. J. Foster. 2004. The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology 150:217-228.
47. B is essential for biofilm development by Staphylococcus aureus. Mol. Microbiol. 48:1075-1087.
48. Vuong, C., C. Gerke, G. A. Somerville, E. R. Fischer, and M. Otto. 2003. Quorum-sensing control of biofilm factors in Staphylococcus epidermidis. J. Infect. Dis. 188:706-718.
49. Vuong, C., F. Götz, and M. Otto. 2000. Construction and characterization of an agr deletion mutant of Staphylococcus epidermidis. Infect. Immun. 68:1048-1053.
50. Zhang, Y. Q., S. X. Ren, H. L. Li, Y. X. Wang, G. Fu, J. Yang, Z. Q. Qin, Y. G. Miao, W. Y. Wang, R. S. Chen, Y. Shen, Z. Chen, Z. H. Yuan, G. P. Zhao, D. Qu, A. Danchin, and Y. M. Wen. 2003. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49:1577-1593.
51. Ziebuhr, W., V. Krimmer, S. Rachid, I. Löbner, F. Götz, and J. Hacker. 1999. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol. Microbiol. 32:345-356.