SarA is a repressor of hla (α-Hemolysin) transcription in Staphylococcus aureus: Its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS

Journal of Bacteriology

Volumn 188, Issue 24, 2006, Pages 8526-8533

  Oscarsson, Jan ^a   Kanth, Anna ^a   Tegmark Wisell, Karin ^a,b   Arvidson, Staffan ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; ERYTHROMYCIN; HEMOLYSIN; KANAMYCIN; LINCOMYCIN; MESSENGER RNA; NEOMYCIN; SIGMA FACTOR; TETRACYCLINE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; ESCHERICHIA COLI; GENE MUTATION; GENE REPRESSION; GENETIC TRANSCRIPTION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; OPERON; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RSBU GENE; SARA GENE; SARS GENE; SKIN INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION;

STAPHYLOCOCCUS AUREUS;

EID: 33845388892     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00866-06     Document Type: Article

References (70)

1. Arvidson, S. 2004. Virulence gene regulation and their role in pathogenesis of disease, p. 154-176. In D. Ala' Aldeen and K. Hiramatsu (ed.), Staphylococcus aureus, molecular and clinical aspects. Horwood Publishing, Chichester, United Kingdom.
2. Arvidson, S., and K. Tegmark. 2001. Regulation of virulence determinants in Staphylococcus aureus. Int. J. Med. Microbiol. 291:159-170.
3. Benson, A. K., and W. G. Haldenwang. 1993. Bacillus subtilis σB is regulated by a binding protein (RsbW) that blocks its association with core RNA polymerase. Proc. Natl. Acad. Sci. USA 90:2330-2334.
4. B regulon. J. Bacteriol. 186:4085-4099.
5. Björklind, A., and S. Arvidson. 1980. Mutants of Staphylococcus aureus affected in the regulation of exoprotein synthesis. FEMS Microbiol. Lett. 7:202-206.
6. Björklind, A., and S. Arvidson. 1977. Occurrence of an extracellular serineproteinase among Staphylococcus aureus strains. Acta Pathol. Microbiol. Scand. 85:277-280.
7. Blevins, J., A. Gillaspy, T. Rechtin, B. Hurlburt, and M. 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.
8. 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.
9. Bronner, S., H. Monteil, and G. Prevost. 2004. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol. Rev. 28:183-200.
10. Caiazza, N. C., and G. A. O'Toole. 2003. Alpha-toxin is required for biofilm formation by Staphylococcus aureus. J. Bacteriol. 185:3214-3217.
11. 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.
12. B controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. J. Bacteriol. 180:6082-6089.
13. 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.
14. Cheung, A. L., J. M. Koomey, C. A. Butler, S. J. Projan, and V. A. Fischetti. 1992. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl. Acad. Sci. USA 89:6462-6466.
15. 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.
16. Cheung, A. L., and P. Ying. 1994. Regulation of α- and β-hemolysins by the sar locus of Staphyhcoccus aureus. J. Bacteriol. 176:580-585.
17. 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.
18. Chien, Y., A. Manna, and A. Cheung. 1998. SarA level is a determinant of agr activation in Staphylococcus aureus. Mol. Microbiol. 30:991-1001.
19. Chien, Y. T., 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.
20. SB of Staphylococcus aureus: characterization and role in transcription of the global regulatory locus sar. J. Bacteriol. 179:6355-6359.
21. Dinges, M. M., P. M. Orwin, and P. M. Schlievert. 2000. Exotoxins of Staphylococcus aureus. Gin. Microbiol. Rev. 13:16-34.
22. Dufour, A., and W. G. Haldenwang. 1994. Interactions between a Bacillus subtilis anti-σ factor (RsbW) and its antagonist (RsbV). J. Bacteriol. 176:1813-1820.
23. Frees, D., K. Serensen, and H. Ingmer. 2005. Global virulence regulation in Staphylococcus aureus: pinpointing the roles of CIpP and ClpX in the sarlagr regulatory network. Infect. Immun. 73:8100-8108.
24. B activity depends on RsbU in Staphylococcus aureus. J. Bacteriol. 183:1843-1852.
25. Giraudo, A. T., A. L. Cheung, and R. Nagel. 1997. The sae locus of Staphylococcus aureus controls exoprotein synthesis at the transcriptional level. Arch. Microbiol. 168:53-58.
26. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
27. Heinrichs, J. H., M. G. Bayer, and A. L. Cheung. 1996. Characterization of the sar locus and its interaction with agr in Staphylococcus aureus. J. Bacteriol. 178:418-423.
28. Horsburgh, M. J., J. L. Aish, I. J. White, L. Shaw, J. K. Lithgow, and S. J. Foster. 2002. σB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphyhcoccus aureus 8325-4. J. Bacteriol. 184:5457-5467.
29. Janzon, L., S. Löfdahl, and S. Arvidson. 1986. Evidence for a coordinate transcriptional control of alpha-toxin and protein A in Staphylococcus aureus. FEMS Microbiol. Lett. 33:193-198.
30. Ji, G., R. C. Beavis, and R. P. Novick. 1995. Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. Proc. Natl. Acad. Sci. USA 92:12055-12059.
31. Jonas, D., I. Walev, T. Berger, M. Liebetrau, M. Palmer, and S. Bhakdi. 1994. Novel path to apoptosis: small transmembrane pores created by staphylococcal alpha-toxin in T lymphocytes evoke intemucleosomal DNA degradation. Infect. Immun. 62:1304-1312.
32. 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 represser sarA. Infect. Immun. 70:4239-4246.
33. 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.
34. Karlsson-Kanth, A., K. Tegmark-Wisell, S. Arvidson, and J. Oscarsson. 2006. Natural human isolates of Staphylococcus aureus selected for high production of proteases and alpha-hemolysin are sigma B-deficient. Int. J. Med. Microbiol. 296:229-236.
35. Khan, S. A., G. K. Adler, and R. P. Novick. 1982. Functional origin of replication of pT181 plasmid DNA is contained within a 168-base-pair segment. Proc. Natl. Acad. Sci. USA 79:4580-4584.
36. Kreiswirth, B., S. Löfdahl, M. J. Betley, M. O'Reilly, M. P. Schleivert, 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.
37. Kullik, I., and P. Giachino. 1997. The alternative sigma factor σB in Staphylococcus aureus: regulation of the sigB operon in response to growth and heat shock. Arch. Microbiol. 167:151-159.
38. B in Staphylococcus aureus reveals its function as a global regulator of virulence genes. J. Bacteriol. 180:4814-4820.
39. Lina, G., S. Jarraud, G. Ji, T. Greenland, A. Pedraza, J. Etienne, R. P. Novick, and F. Vandenesch. 1998. Transmembrane topology and histidine protein kinase activity of AgrC, the agr signal receptor in Staphylococcus aureus. Mol. Microbiol. 28:655-662.
40. Lindsay, J., and S. Foster. 1999. Interactive regulatory pathways control virulence determinant production and stability in response to environmental conditions in Staphylococcus aureus. Mol. Gen. Genet. 262:323-331.
41. Manna, A. C., and A. L. Cbeung. 2003. sarU, a sarA homolog, is repressed by SarT and regulates virulence genes in Staphylococcus aureus. Infect. Immun. 71:343-353.
42. Mayville, P., G. Ji, R. Beavis, H. Yang, M. Goger, R. P. Novick, and T. W. Muir. 1999. Structure-activity analysis of synthetic autoinducing thiolactone peptides from Staphylococcus aureus responsible for virulence. Proc. Natl. Acad. Sci. USA 96:1218-1223.
43. McCallum, N., M. Bischoff, H. Maki, A. Wada, and B. Berger-Bachi. 2004. TcaR, a putative MarR-like regulator of sarS expression. J. Bacteriol. 186:2966-2972.
44. McNamara, P. J., and A. S. Bayer. 2005. A rot mutation restores parental virulence to an agr-null Staphylococcus aureus strain in a rabbit model of endocarditis. Infect. Immun. 73:3806-3809.
45. 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.
46. 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.
47. Morfeldt, E., L. Janzon, S. Arvidson, and S. Löfdahl. 1988. Cloning of a chromosomal locus (exp) which regulates the expression of several exoprotein genes in Staphylococcus aureus. Mol. Gen. Genet. 211:435-440.
48. Morfeldt, E., D. Taylor, A. von Gabain, and S. Aridson. 1995. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14:4569-4577.
49. 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.
50. Novick, R. P. 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol. Microbiol. 48:1429-1449.
51. Novick, R. P. 1991. Genetic systems in staphylococci. Methods Enzymol. 204:587-636.
52. Novick, R. P. 1967. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33:155-166.
53. Novick, R. P., and D. Jiang. 2003. The staphylococcal saeRS system coordinates environmental signals with agr quorum sensing. Microbiology 149:2709-2717.
54. Novick, R. P., H. F. Ross, S. J. Projan, J. Kornblum, B. Kreiswirth, and S. Moghazeh. 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12:3967-3975.
55. O'Reilly, M., J. C. de Azavedo, S. Kennedy, and T. J. Foster. 1986. Inactivation of the alpha-haemolysin gene of Staphylococcus aureus 8325-4 by site-directed mutagenesis and studies on the expression of its haemolysins. Microb. Pathog. 1:125-138.
56. Oscarsson, J., C. Harlos, and S. Arvidson. 2005. Regulatory role of proteins binding to the spa (protein A) and sarS (staphylococcal accessory regulator) in Staphylococcus aureus NCTC 8325-4. Int. J. Med. Microbiol. 295:253-266.
57. Oscarsson, J., K. Tegmark-Wisell, and S. Arvidson. 2006. Coordinated and differential control of aureolysin (aur) and serine protease (sspA) transcription in Staphylococcus aureus by sarA, rot and agr (RNAIII). Int. J. Med. Microbiol. 296:365-380.
58. 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 agr. Mol. Gen. Genet. 202:58-61.
59. 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.
60. Sambrook, J. E., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
61. Schenk, S., and R. A. Laddaga. 1992. Improved methods for electroporation of Staphylococcus aureus. FEMS Microbiol. Lett. 94:133-138.
62. Schmidt, K. A., A. C. Manna, and A. L. Cheung. 2003. SarT influences sarS expression in Staphylococcus aureus. Infect. Immun. 71:5139-5148.
63. Schmidt, K. A., A. C. Manna, S. Gill, and A. L. Cheung. 2001. SarT, a repressor of α-hemolysin in Staphylococcus aureus. Infect. Immun. 69:4749-4758.
64. Söderquist, B., P. Colque-Navarro, L. Blomqvist, P. Olcén, H. Holmberg, and R. Möllby. 1993. Staphylococcal á-toxin in septicémie patients; detection in serum, antibody response and production in isolated strains. Serodiagn. Immunother. Infect. Dis. 5:139-144.
65. Sterba, K. M., S. G. Mackintosh, J. S. Blevins, B. K. Hurlburt, and M. S. Smeltzer. 2003. Characterization of Staphylococcus aureus SarA binding sites. J. Bacteriol. 185:4410-4417.
66. Tegmark, K. 2000. Regulation of virulence gene expression in Staphylococcus aureus. Karolinska Institutet Stockholm, Sweden.
67. Tegmark, K., A. Karlsson, and S. Arvidson. 2000. Identification and characterization of SarH1 a new global regulator of virulence gene expression in Staphylococcus aureus. Mol. Microbiol. 37:398-409.
68. B. J. Bacteriol. 177:114-122.
69. Walev, I., E. Martin, D. Jonas, M. Mohamadzadeh, W. Müller-Klieser, L. Kunz, and S. Bhakdi. 1993. Staphylococcal alpha-toxin kills human keratinocytes by permeabilizing the plasma membrane for monovalent ions. Infect. Immun. 61:4972-4979.
70. B in response to environmental signals. J. Bacteriol. 177:123-133.