Control of the Staphylococcus aureus toxic shock tst promoter by the global regulator SarA

Journal of Bacteriology

Volumn 192, Issue 22, 2010, Pages 6077-6085

  Andrey, Diego O ^a   Renzoni, Adriana ^a   Monod, Antoinette ^a   Lew, Daniel P ^a   Cheung, Ambrose L ^b   Kelley, William L ^a  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DEOXYRIBONUCLEASE I; DNA; PROTEIN TST; TOXIC SHOCK SYNDROME TOXIN 1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GENE LOCATION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SARA GENE; STAPHYLOCOCCUS AUREUS;

ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BACTERIAL TOXINS; BASE SEQUENCE; DNA, BACTERIAL; ENTEROTOXINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; LUCIFERASES; MOLECULAR SEQUENCE DATA; PLASMIDS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA, BACTERIAL; SEQUENCE DELETION; SHOCK, SEPTIC; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS;

STAPHYLOCOCCUS AUREUS;

EID: 78049430385     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00146-10     Document Type: Article

References (59)

1. Ballal, A., and A. C. Manna. 2010. Control of thioredoxin reductase gene (trxB) transcription by SarA in Staphylococcus aureus. J. Bacteriol. 192:336-345.
2. 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.
3. 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.
4. Chan, P. F., and S. J. Foster. 1998. The role of environmental factors in the regulation of virulence-determinant expression in Staphylococcus aureus 8325-4. Microbiology 144(Pt. 9):2469-2479.
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. 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.
7. Cheung, A. L., K. Nishina, and A. C. Manna. 2008. SarA of Staphylococcus aureus binds to the sarA promoter to regulate gene expression. J. Bacteriol. 190:2239-2243.
8. Cheung, A. L., K. A. Nishina, M. P. Trotonda, and S. Tamber. 2008. The SarA protein family of Staphylococcus aureus. Int. J. Biochem. Cell Biol. 40:355-361.
9. Cheung, A. L., K. Schmidt, B. Bateman, and A. C. Manna. 2001. SarS, a SarA homolog repressible by agr, is an activator of protein A synthesis in Staphylococcus aureus. Infect. Immun. 69:2448-2455.
10. Chien, Y., and A. L. Cheung. 1998. Molecular interactions between two global regulators, sar and agr, in Staphylococcus aureus. J. Biol. Chem. 273:2645-2652.
11. Chien, Y., A. C. Manna, S. J. Projan, and A. L. Cheung. 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.
12. DeLeo, F. R., and H. F. Chambers. 2009. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J. Clin. Invest. 119:2464-2474.
13. 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.
14. Foster, T. J. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3:948-958.
15. Fujimoto, D. F., R. H. Higginbotham, K. M. Sterba, S. J. Maleki, A. M. Segall, M. S. Smeltzer, and B. K. Hurlburt. 2009. Staphylococcus aureus SarA is a regulatory protein responsive to redox and pH that can support bacteriophage lambda integrase-mediated excision/recombination. Mol. Microbiol. 74:1445-1458.
16. Gao, R., and A. M. Stock. 2009. Biological insights from structures of two-component proteins. Annu. Rev. Microbiol. 63:133-154.
17. Hyyrylainen, H. L., M. Pietiainen, T. Lunden, A. Ekman, M. Gardemeister, S. Murtomaki-Repo, H. Antelmann, M. Hecker, L. Valmu, M. Sarvas, and V. P. Kontinen. 2007. The density of negative charge in the cell wall influences two-component signal transduction in Bacillus subtilis. Microbiology 153:2126-2136.
18. Janzon, L., and S. Arvidson. 1990. The role of the delta-lysin gene (hld) in the regulation of virulence genes by the accessory gene regulator (agr) in Staphylococcus aureus. EMBO J. 9:1391-1399.
19. Kass, E. H. 1989. Magnesium and the pathogenesis of toxic shock syndrome. Rev. Infect. Dis. 11(Suppl. 1):S167-S175.
20. Katayama, Y., H. Murakami-Kuroda, L. Cui, and K. Hiramatsu. 2009. Selection of heterogeneous vancomycin-intermediate Staphylococcus aureus by imipenem. Antimicrob. Agents Chemother. 53:3190-3196.
21. 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.
22. Kreiswirth, B. N., M. O'Reilly, and R. P. Novick. 1984. Genetic characterization and cloning of the toxic shock syndrome exotoxin. Surv. Synth. Pathol. Res. 3:73-82.
23. Lappin, E., and A. J. Ferguson. 2009. Gram-positive toxic shock syndromes. Lancet Infect. Dis. 9:281-290.
24. Lindsay, J. A., A. Ruzin, H. F. Ross, N. Kurepina, and R. P. Novick. 1998. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29:527-543.
25. Liu, Y., A. Manna, R. Li, W. E. Martin, R. C. Murphy, A. L. Cheung, and G. Zhang. 2001. Crystal structure of the SarR protein from Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 98:6877-6882.
26. Liu, Y., A. C. Manna, C. H. Pan, I. A. Kriksunov, D. J. Thiel, A. L. Cheung, and G. Zhang. 2006. Structural and function analyses of the global regulatory protein SarA from Staphylococcus aureus. Proc. Natl. Acad. Sci. U. S. A. 103:2392-2397.
27. Luong, T. T., P. M. Dunman, E. Murphy, S. J. Projan, and C. Y. Lee. 2006. Transcription profiling of the mgrA regulon in Staphylococcus aureus. J. Bacteriol. 188:1899-1910.
28. Manna, A., and A. L. Cheung. 2001. Characterization of sarR, a modulator of sar expression in Staphylococcus aureus. Infect. Immun. 69:885-896.
29. 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.
30. Manna, A. C., and B. Ray. 2007. Regulation and characterization of rot transcription in Staphylococcus aureus. Microbiology 153:1538-1545.
31. McCormick, J. K., J. M. Yarwood, and P. M. Schlievert. 2001. Toxic shock syndrome and bacterial superantigens: an update. Annu. Rev. Microbiol. 55:77-104.
32. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429-1449.
33. Novick, R. P. 2003. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49:93-105. (Pubitemid 36506566)
34. Pamp, S. J., D. Frees, S. Engelmann, M. Hecker, and H. Ingmer. 2006. Spx is a global effector impacting stress tolerance and biofilm formation in Staphylococcus aureus. J. Bacteriol. 188:4861-4870.
35. Pragman, A. A., L. Herron-Olson, L. C. Case, S. M. Vetter, E. E. Henke, V. Kapur, and P. M. Schlievert. 2007. Sequence analysis of the Staphylococcus aureus srrAB loci reveals that truncation of srrA affects growth and virulence factor expression. J. Bacteriol. 189:7515-7519.
36. Pragman, A. A., Y. Ji, and P. M. Schlievert. 2007. Repression of Staphylococcus aureus SrrAB using inducible antisense srrA alters growth and virulence factor transcript levels. Biochemistry 46:314-321.
37. 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.
38. 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.
39. Rechtin, T. M., A. F. Gillaspy, M. A. Schumacher, R. G. Brennan, M. S. Smeltzer, and B. K. Hurlburt. 1999. Characterization of the SarA virulence gene regulator of Staphylococcus aureus. Mol. Microbiol. 33:307-316.
40. Recsei, P., B. Kreiswirth, M. O'Reilly, P. Schlievert, A. Gruss, and R. P. Novick. 1986. Regulation of exoprotein gene expression in Staphylococcus aureus by agar. Mol. Gen. Genet. 202:58-61.
41. Renzoni, A., C. Barras, P. Francois, Y. Charbonnier, E. Huggler, C. Garzoni, W. L. Kelley, P. Majcherczyk, J. Schrenzel, D. P. Lew, and P. Vaudaux. 2006. Transcriptomic and functional analysis of an autolysis-deficient, teicoplanin-resistant derivative of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 50:3048-3061.
42. 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. (Pubitemid 38989161)
43. Rohs, R., S. M. West, A. Sosinsky, P. Liu, R. S. Mann, and B. Honig. 2009. The role of DNA shape in protein-DNA recognition. Nature 461:1248-1253.
44. Rooijakkers, S. H., K. P. van Kessel, and J. A. van Strijp. 2005. Staphylococcal innate immune evasion. Trends Microbiol. 13:596-601.
45. Schlag, S., S. Fuchs, C. Nerz, R. Gaupp, S. Engelmann, M. Liebeke, M. Lalk, M. Hecker, and F. Gotz. 2008. Characterization of the oxygen-responsive NreABC regulon of Staphylococcus aureus. J. Bacteriol. 190:7847-7858.
46. Schlievert, P. M., L. C. Case, K. A. Nemeth, C. C. Davis, Y. Sun, W. Qin, F. Wang, A. J. Brosnahan, J. A. Mleziva, M. L. Peterson, and B. E. Jones. 2007. Alpha and beta chains of hemoglobin inhibit production of Staphylococcus aureus exotoxins. Biochemistry 46:14349-14358.
47. Schumacher, M. A., B. K. Hurlburt, and R. G. Brennan. 2001. Crystal structures of SarA, a pleiotropic regulator of virulence genes in S. aureus. Nature 409:215-219.
48. Seidl, K., M. Bischoff, and B. Berger-Bachi. 2008. CcpA mediates the catabolite repression of tst in Staphylococcus aureus. Infect. Immun. 76:5093-5099.
49. Somerville, G. A., S. B. Beres, J. R. Fitzgerald, F. R. DeLeo, R. L. Cole, J. S. Hoff, and J. M. Musser. 2002. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence. J. Bacteriol. 184:1430-1437.
50. Subedi, A., C. Ubeda, R. P. Adhikari, J. R. Penades, and R. P. Novick. 2007. Sequence analysis reveals genetic exchanges and intraspecific spread of SaPI2, a pathogenicity island involved in menstrual toxic shock. Microbiology 153:3235-3245.
51. Sullivan, M. A., R. E. Yasbin, and F. E. Young. 1984. New shuttle vectors for Bacillus subtilis and Escherichia coli which allow rapid detection of inserted fragments. Gene 29:21-26.
52. Tormo, M. A., M. Marti, J. Valle, A. C. Manna, A. L. Cheung, I. Lasa, and J. R. Penades. 2005. SarA is an essential positive regulator of Staphylococcus epidermidis biofilm development. J. Bacteriol. 187:2348-2356.
53. Traber, K., and R. Novick. 2006. A slipped-mispairing mutation in AgrA of laboratory strains and clinical isolates results in delayed activation of agr and failure to translate delta- and alpha-haemolysins. Mol. Microbiol. 59:1519-1530.
54. Tu Quoc, P. H., P. Genevaux, M. Pajunen, H. Savilahti, C. Georgopoulos, J. Schrenzel, and W. L. Kelley. 2007. Isolation and characterization of biofilm formation-defective mutants of Staphylococcus aureus. Infect. Immun. 75:1079-1088.
55. 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.
56. Vojtov, N., H. F. Ross, and R. P. Novick. 2002. Global repression of exotoxin synthesis by staphylococcal superantigens. Proc. Natl. Acad. Sci. U. S. A. 99:10102-10107.
57. Yarwood, J. M., J. K. McCormick, M. L. Paustian, V. Kapur, and P. M. Schlievert. 2002. Repression of the Staphylococcus aureus accessory gene regulator in serum and in vivo. J. Bacteriol. 184:1095-1101.
58. 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.
59. Yarwood, J. M., and P. M. Schlievert. 2000. Oxygen and carbon dioxide regulation of toxic shock syndrome toxin 1 production by Staphylococcus aureus MN8. J. Clin. Microbiol. 38:1797-1803.