Epidemiology, variable genetic organization and regulation of the EDIN-B toxin in Staphylococcus aureus from bacteraemic patients

Microbiology

Volumn 156, Issue 3, 2010, Pages 860-872

  Franke, Gefion C ^a   Böckenholt, Alexandra ^a   Sugai, Motoyuki ^b   Rohde, Holger ^a   Aepfelbacher, Martin ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 2 MACROGLOBULIN; EXOTOXIN; PROTEIN AGR; PROTEIN EDIN B; PROTEINASE; SMAD ANCHOR FOR RECEPTOR ACTIVATION; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTEREMIA; BLOOD CULTURE; CONTROLLED STUDY; GENE CONTROL; GENETIC ORGANIZATION; HUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN SECRETION; STAPHYLOCOCCUS AUREUS;

ADP RIBOSE TRANSFERASES; ANTIBODIES, BACTERIAL; DNA, BACTERIAL; EXFOLIATINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOMIC ISLANDS; GENOTYPE; HUMANS; REGULON; SEQUENCE ANALYSIS, DNA; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 77749252681     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.030304-0     Document Type: Article

References (75)

1. Aepfelbacher, M., Essler, M., Huber, E., Sugai, M. & Weber, P. C. (1997). Bacterial toxins block endothelial wound repair. Evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler Thromb Vasc Biol 17, 1623-1629.
2. Aepfelbacher, M., Trasak, C. & Ruckdeschel, K. (2007). Effector functions of pathogenic Yersinia species. Thromb Haemost 98, 521-529.
3. Aktories, K. & Barbieri, J. T. (2005). Bacterial cytotoxins: targeting eukaryotic switches. Nat Rev Microbiol 3, 397-410.
4. Arvidson, S. & Tegmark, K. (2001). Regulation of virulence determinants in Staphylococcus aureus. Int J Med Microbiol 291, 159-170.
5. Augustin, J. & Gotz, F. (1990). Transformation of Staphylococcus epidermidis and other staphylococcal species with plasmid DNA by electroporation. FEMS Microbiol Lett 54, 203-207.
6. Ben Nejma, M., Mastouri, M., Bel Hadj Jrad, B. & Nour, M. (2008). Characterization of ST80 Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone in Tunisia. Diagn Microbiol Infect Dis (in press), doi:10.1016/j. diagmicrobio.2008.02.010.
7. B regulon. J Bacteriol 186, 4085-4099.
8. Blevins, J. S., Beenken, K. E., Elasri, M. O., Hurlburt, B. K. & Smeltzer, M. S. (2002). Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect Immun 70, 470-480.
9. Bokoch, G. M. (2005). Regulation of innate immunity by Rho GTPases. Trends Cell Biol 15, 163-171.
10. Boyer, L., Doye, A., Rolando, M., Flatau, G., Munro, P., Gounon, P., Clément, R., Pulcini, C., Popoff, M. R. & other authors (2006). Induction of transient macroapertures in endothelial cells through RhoA inhibition by Staphylococcus aureus factors. J Cell Biol 173, 809-819.
11. Bronner, S., Monteil, H. & Prevost, G. (2004). Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 28, 183-200.
12. Bruckner, R. (1992). A series of shuttle vectors for Bacillus subtilis and Escherichia coli. Gene 122, 187-192.
13. Cassat, J., Dunman, P. M., Murphy, E., Projan, S. J., Beenken, K. E., Palm, K. J., Yang, S. J., Rice, K. C., Bayles, K. W. & Smeltzer, M. S. (2006). Transcriptional profiling of a Staphylococcus aureus clinical isolate and its isogenic agr and sarA mutants reveals global differences in comparison to the laboratory strain RN6390. Microbiology 152, 3075-3090.
14. Chan, P. F. & Foster, S. J. (1998). Role of SarA in virulence determinant production and environmental signal transduction in Staphylococcus aureus. J Bacteriol 180, 6232-6241.
15. Cheung, A. L., Eberhardt, K. & Heinrichs, J. H. (1997). Regulation of protein A synthesis by the sar and agr loci of Staphylococcus aureus. Infect Immun 65, 2243-2249.
16. Cheung, A. L., Bayer, A. S., Zhang, G., Gresham, H. & Xiong, Y. Q. (2004). Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol 40, 1-9.
17. Cheung, A. L., Nishina, K. A., Trotonda, M. P. & Tamber, S. (2008). The SarA protein family of Staphylococcus aureus. Int J Biochem Cell Biol 40, 355-361.
18. Chien, Y., Manna, A. C., Projan, S. J. & Cheung, A. L. (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.
19. Chongtrakool, P., Ito, T., Ma, X. X., Kondo, Y., Trakulsomboon, S., Tiensasitorn, C., Jamklang,M., Chavalit, T., Song, J. H. & Hiramatsu, K. (2006). Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother 50, 1001-1012.
20. Clarke, S. R., Brummell, K. J., Horsburgh, M. J., McDowell, P. W., Mohamad, S. A., Stapleton, M. R., Acevedo, J., Read, R. C., Day, N. P. & other authors (2006). Identification of in vivo-expressed antigens of Staphylococcus aureus and their use in vaccinations for protection against nasal carriage. J Infect Dis 193, 1098-1108.
21. Czech, A., Yamaguchi, T., Bader, L., Linder, S., Kaminski, K., Sugai, M. & Aepfelbacher, M. (2001). Prevalence of Rho-inactivating epidermal cell differentiation inhibitor toxins in clinical Staphylococcus aureus isolates. J Infect Dis 184, 785-788.
22. Deurenberg, R. H. & Stobberingh, E. E. (2008). The evolution of Staphylococcus aureus. Infect Genet Evol 8, 747-763.
23. Deurenberg, R. H., Vink, C., Kalenic, S., Friedrich, A. W., Bruggeman, C. A. & Stobberingh, E. E. (2007). The molecular evolution of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 13, 222-235.
24. Dunman, P. M., Murphy, E., Haney, S., Palacios, D., Tucker-Kellogg, G., Wu, S., Brown, E. L., Zagursky, R. J., Shlaes, D. & Projan, S. J. (2001). Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183, 7341-7353.
25. Duthie, E. S. & Lorenz, L. L. (1952). Staphylococcal coagulase; mode of action and antigenicity. J Gen Microbiol 6, 95-107.
26. Fitzgerald, J. R.,Reid, S. D.,Ruotsalainen, E., Tripp, T. J., Liu, M.,Cole, R., Kuusela, P., Schlievert, P. M., Järvinen, A. & Musser, J. M. (2003). Genome diversification in Staphylococcus aureus: molecular evolution of a highly variable chromosomal region encoding the staphylococcal exotoxin-like family of proteins. Infect Immun 71, 2827-2838.
27. Genth, H., Dreger, S. C., Huelsenbeck, J. & Just, I. (2008). Clostridium difficile toxins: more than mere inhibitors of Rho proteins. Int J Biochem Cell Biol 40, 592-597.
28. B activity depends on RsbU in Staphylococcus aureus. J Bacteriol 183, 1843-1852.
29. Goerke, C. & Wolz, C. (2004). Regulatory and genomic plasticity of Staphylococcus aureus during persistent colonization and infection. Int J Med Microbiol 294, 195-202.
30. Goerke, C., Fluckiger, U., Steinhuber, A., Zimmerli, W. & Wolz, C. (2001). Impact of the regulatory loci agr, sarA and sae of Staphylococcus aureus on the induction of α-toxin during device-related infection resolved by direct quantitative transcript analysis. Mol Microbiol 40, 1439-1447.
31. Gordon, J. J., Towsey, M. W., Hogan, J. M., Mathews, S. A. & Timms, P. (2006). Improved prediction of bacterial transcription start sites. Bioinformatics 22, 142-148.
32. Hacker, J. & Kaper, J. B. (2000). Pathogenicity islands and the evolution of microbes. Annu Rev Microbiol 54, 641-679.
33. Harmsen, D., Claus, H., Witte, W., Rothganger, J., Turnwald, D. & Vogel, U. (2003). Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41, 5442-5448.
34. Harraghy, N., Kormanec, J., Wolz, C., Homerova, D., Goerke, C., Ohlsen, K., Qazi, S., Hill, P. & Herrmann, M. (2005). sae is essential for expression of the staphylococcal adhesins Eap and Emp. Microbiology 151, 1789-1800.
35. Holmes, A., Ganner, M., McGuane, S., Pitt, T. L., Cookson, B. D. & Kearns, A. M. (2005). Staphylococcus aureus isolates carrying Panton-Valentine leucocidin genes in England and Wales: frequency, characterization, and association with clinical disease. J Clin Microbiol 43, 2384-2390.
36. Holtfreter, S., Grumann, D., Schmudde, M., Nguyen, H. T., Eichler, P., Strommenger, B., Kopron, K., Kolata, J., Giedrys-Kalemba, S. & other authors (2007). Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45, 2669-2680.
37. 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.
38. Jaffe, A. B. & Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21, 247-269.
39. Karlsson, A. & Arvidson, S. (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.
40. B by repression of the negative regulator gene icaR. Infect Immun 72, 3838-3848.
41. Ladhani, S., Joannou, C. L., Lochrie, D. P., Evans, R. W. & Poston, S. M. (1999). Clinical, microbial, and biochemical aspects of the exfoliative toxins causing staphylococcal scalded-skin syndrome. Clin Microbiol Rev 12, 224-242.
42. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
43. Lindsay, J. A. & Foster, S. J. (1999). Interactive regulatory pathways control virulence determinant production and stability in response to environmental conditions in Staphylococcus aureus. Mol Gen Genet 262, 323-331.
44. Lindsay, J. A. & Holden, M. T. (2006). Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus. Funct Integr Genomics 6, 186-201.
45. CT method. Methods 25, 402-408.
46. Lowy, F. D. (1998). Staphylococcus aureus infections. N Engl J Med 339, 520-532.
47. Mack, D., Bartscht, K., Fischer, C., Rohde, H., de Grahl, C., Dobinsky, S., Horstkotte, M. A., Kiel, K. & Knobloch, J. K. (2001). Genetic and biochemical analysis of Staphylococcus epidermidis biofilm accumulation. Methods Enzymol 336, 215-239.
48. McAleese, F. M., Walsh, E. J., Sieprawska, M., Potempa, J. & Foster, T. J. (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.
49. Mellmann, A., Weniger, T., Berssenbrugge, C., Rothganger, J., Sammeth, M., Stoye, J. & Harmsen, D. (2007). Based Upon Repeat Pattern (BURP): an algorithm to characterize the long-term evolution of Staphylococcus aureus populations based on spa polymorphisms. BMC Microbiol 7, 98.
50. Monecke, S., Slickers, P., Hotzel, H., Richter-Huhn, G., Pohle, M., Weber, S., Witte, W. & Ehricht, R. (2006). Microarray-based characterisation of a Panton-Valentine leukocidin-positive community-acquired strain of methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 12, 718-728.
51. Morfeldt, E., Janzon, L., Arvidson, S. & Lofdahl, S. (1988). Cloning of a chromosomal locus (exp) which regulates the expression of several exoprotein genes in Staphylococcus aureus. Mol Gen Genet 211, 435-440.
52. Murchan, S., Kaufmann, M. E., Deplano, A., de Ryck, R., Struelens, M., Zinn, C. E., Fussing, V., Salmenlinna, S., Vuopio-Varkila, J. & other authors (2003). Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol 41, 1574-1585.
53. Novick, R. P. (1991). Genetic systems in staphylococci. Methods Enzymol 204, 587-636.
54. Novick, R. P. (2003). Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48, 1429-1449.
55. Novick, R. P., Ross, H. F., Projan, S. J., Kornblum, J., Kreiswirth, B. & Moghazeh, S. (1993). Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12, 3967-3975.
56. Oscarsson, J., Kanth, A., Tegmark-Wisell, K. & Arvidson, S. (2006a). 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. J Bacteriol 188, 8526-8533.
57. Oscarsson, J., Tegmark-Wisell, K. & Arvidson, S. (2006b). 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. Peacock, S. J., Moore, C. E., Justice, A., Kantzanou, M., Story, L., Mackie, K., O'Neill, G. & Day, N. P. (2002). Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 70, 4987-4996.
59. Peng, H. L., Novick, R. P., Kreiswirth, B., Kornblum, J. & Schlievert, P. (1988). Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 170, 4365-4372.
60. Recsei, P., Kreiswirth, B., O'Reilly, M., Schlievert, P., Gruss, A. & Novick, R. P. (1986). Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol Gen Genet 202, 58-61.
61. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
62. Shaw, L., Golonka, E., Potempa, J. & Foster, S. J. (2004). The role and regulation of the extracellular proteases of Staphylococcus aureus. Microbiology 150, 217-228.
63. Sugai, M., Enomoto, T., Hashimoto, K., Matsumoto, K., Matsuo, Y., Ohgai, H., Hong, Y. M., Inoue, S., Yoshikawa, K. & Suginaka, H. (1990). A novel epidermal cell differentiation inhibitor (EDIN): purification and characterization from Staphylococcus aureus. Biochem Biophys Res Commun 173, 92-98.
64. Sugai, M., Hashimoto, K., Kikuchi, A., Inoue, S., Okumura, H., Matsumoto, K., Goto, Y., Ohgai, H., Moriishi, K. & other authors (1992). Epidermal cell differentiation inhibitor ADP-ribosylates small GTP-binding proteins and induces hyperplasia of epidermis. J Biol Chem 267, 2600-2604.
65. Sung, J. M., Lloyd, D. H. & Lindsay, J. A. (2008). Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology 154, 1949-1959.
66. Tenover, F. C., Arbeit, R. D., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H. & Swaminathan, B. (1995). Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33, 2233-2239.
67. Vandenesch, F., Naimi, T., Enright, M. C., Lina, G., Nimmo, G. R., Heffernan, H., Liassine, N., Bes, M., Greenland, T. & other authors (2003). Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9, 978-984.
68. Wilde, C., Chhatwal, G. S., Schmalzing, G., Aktories, K. & Just, I. (2001). A novel C3-like ADP-ribosyltransferase from Staphylococcus aureus modifying RhoE and Rnd3. J Biol Chem 276, 9537-9542.
69. Witte, W., Strommenger, B., Cuny, C., Heuck, D. & Nuebel, U. (2007). Methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leucocidin gene in Germany in 2005 and 2006. J Antimicrob Chemother 60, 1258-1263.
70. Wolz, C., McDevitt, D., Foster, T. J. & Cheung, A. L. (1996). Influence of agr on fibrinogen binding in Staphylococcus aureus Newman. Infect Immun 64, 3142-3147.
71. Wolz, C., Pohlmann-Dietze, P., Steinhuber, A., Chien, Y. T., Manna, A., van Wamel, W. & Cheung, A. (2000). agr-independent regulation of fibronectin-binding protein(s) by the regulatory locus sar in Staphylococcus aureus. Mol Microbiol 36, 230-243.
72. Yamaguchi, T., Hayashi, T., Takami, H., Ohnishi, M., Murata, T., Nakayama, K., Asakawa, K., Ohara, M., Komatsuzawa, H. & Sugai, M. (2001). Complete nucleotide sequence of a Staphylococcus aureus exfoliative toxin B plasmid and identification of a novel ADP- ribosyltransferase, EDIN-C. Infect Immun 69, 7760-7771.
73. Yamaguchi, T., Nishifuji, K., Sasaki, M., Fudaba, Y., Aepfelbacher, M., Takata, T., Ohara, M., Komatsuzawa, H., Amagai, M. & Sugai, M. (2002a). Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect Immun 70, 5835-5845.
74. Yamaguchi, T., Yokota, Y., Terajima, J., Hayashi, T., Aepfelbacher, M., Ohara, M., Komatsuzawa, H., Watanabe, H. & Sugai, M. (2002b). Clonal association of Staphylococcus aureus causing bullous impetigo and the emergence of new methicillin-resistant clonal groups in Kansai district in Japan. J Infect Dis 185, 1511-1516.
75. Yamasaki, O., Tristan, A., Yamaguchi, T., Sugai, M., Lina, G., Bes, M., Vandenesch, F. & Etienne, J. (2006). Distribution of the exfoliative toxin D gene in clinical Staphylococcus aureus isolates in France. Clin Microbiol Infect 12, 585-588.