Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection

Molecular Microbiology

Volumn 61, Issue 6, 2006, Pages 1673-1685

  Goerke, Christiane ^a   Wirtz, Christiane ^a   Flückiger, Ursula ^b   Wolz, Christiane ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYSIN; INTEGRASE; VIRULENCE FACTOR;

ARTICLE; BACTEREMIA; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL SURVIVAL; BACTERIAL TRANSLOCATION; BACTERIOPHAGE; BACTERIUM ISOLATE; BLOOD GROUP TYPING; CHROMOSOME; CONTROLLED STUDY; CYSTIC FIBROSIS; EVOLUTIONARY ADAPTATION; GENE DUPLICATION; GENE MAPPING; GENE TRANSFER; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; GENOTYPE; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; LIFE CYCLE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; VIRULENCE;

ATTACHMENT SITES, MICROBIOLOGICAL; BACTERIAL TOXINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, VIRAL; HEMOLYSIN PROTEINS; HUMANS; SPHINGOMYELIN PHOSPHODIESTERASE; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS PHAGES; VIRAL PROTEINS; VIRULENCE; VIRUS INTEGRATION;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 33748483660     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05354.x     Document Type: Article

References (53)

1. de Azavedo, J.C., Foster, T.J., Hartigan, P.J., Arbuthnott, J.P., O'Reilly, M., Kreiswirth, B.N., and Novick, R.P. (1985) Expression of the cloned toxic shock syndrome toxin 1 gene (tst) in vivo with a rabbit uterine model. Infect Immun 50: 304-309.
2. Baba, T., Takeuchi, F., Kuroda, M., Yuzawa, H., Aoki, K., Oguchi, A., et al. (2002) Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359: 1819-1827.
3. Betley, M.J., and Mekalanos, J.J. (1985) Staphylococcal enterotoxin A is encoded by phage. Science 229: 185-187.
4. Bohach, G.A., and Foster, T.J. (2000) Staphylococcus aureus exotoxins. In Gram-Positve Pathogens. Fischetti, V.A., Novick, R.P., Ferretti, J.J., Portnoy, D.A., and Rood, J.I. (eds). Washington, DC: American Society for Microbiology Press, pp. 367-378.
5. Breitbart, M., Rohwer, F., and Abedon, S.T. (2006) Phage ecology and bacterial pathogenesis. In Phages. Their Role in Bacterial Pathogenesis and Biotechnology. Waldor, M.K., Friedman, D.I., and Adhya, S.L. (eds). Washington, DC: American Society for Microbiology Press, pp. 66-91.
6. Brendel, V., and Trifonov, E.N. (1984) A computer algorithm for testing potential prokaryotic terminators. Nucleic Acids Res 12: 4411-4427.
7. Broudy, T.B., Pancholi, V., and Fischetti, V.A. (2002) The in vitro interaction of Streptococcus pyogenes with human pharyngeal cells induces a phage-encoded extracellular DNase. Infect Immun 70: 2805-2811.
8. Christner, R.B., and Boyle, M.D. (1996) Role of staphylokinase in the acquisition of plasmin (ogen)-dependent enzymatic activity by staphylococci. J Infect Dis 173: 104-112.
9. Coleman, D.C., Sullivan, D.J., Russell, R.J., Arbuthnott, J.P., Carey, B.F., and Pomeroy, H.M. (1989) Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of beta-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J Gen Microbiol 135: 1679-1697.
10. Collen, D. (1998) Staphylokinase: a potent, uniquely fibrin-selective thrombolytic agent. Nat Med 4: 279-284.
11. De Haas, C.J., Veldkamp, K.E., Peschel, A., Weerkamp, F., van Wamel, W.J., Heezius, E.C., et al. (2004) Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J Exp Med 199: 687-695.
12. Foster, T.J., O'Reilly, M., Phonimdaeng, P., Cooney, J., Patel, A.H., and Bramley, A.J. (1990) Genetic studies of virulence factors of Staphylococcus aureus. Poperties of coagulase and gamma-toxin and the role of alpha-toxin, beta-toxin and protein A in the pathogenesis of S. aureus infections. In Molecular Biology of the Staphylococci. Novick, R.P. (ed.). Cambridge: VCH Publishers, pp. 403-417.
13. Gladysheva, I.P., Turner, R.B., Sazonova, I.Y., Liu, L., and Reed, G.L. (2003) Coevolutionary patterns in plasminogen activation. Proc Natl Acad Sci USA 100: 9168-9172.
14. Goerke, C., Kraning, K., Stern, M., Döring, G., Botzenhart, K., and Wolz, C. (2000a) Molecular epidemiology of community-aquired Staphylococcus aureus in families with and without cystic fibrosis patients. J Infect Dis 181: 984-989.
15. Goerke, C., Campana, S., Bayer, M.G., Döring, G., Botzenhart, K., and Wolz, C. (2000b) Direct quantitative transcript analysis of the agr regulon of Staphylococcus aureus during human infection in comparison to the expression profile in vitro. Infect Immun 68: 1304-1311.
16. Goerke, C., Matias y Papenberg, S., Dasbach, S., Dietz, K., Ziebach, R., Kahl, B.C., and Wolz, C. (2004) Increased frequency of genomic alterations in Staphylococcus aureus during chronic infection is in part due to phage mobilization. J Infect Dis 189: 724-734.
17. Goerke, C., Koller, J., and Wolz, C. (2006) Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother 50: 171-177.
18. Gulbins, E., Dreschers, S., Wilker, B., and Grassme, H. (2004) Ceramide, membrane rafts and infections. J Mol Med 82: 357-363.
19. 2 inhibition in vitro and in vivo. J Infect Dis 176: 431-438.
20. Holden, M.T., Feil, E.J., Lindsay, J.A., Peacock, S.J., Day, N.P., Enright, M.C., et al. (2004) Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc Natl Acad Sci USA 101: 9786-9791.
21. Iandolo, J.J., Worrell, V., Groicher, K.H., Qian, Y., Tian, R., Kenton, S., et al. (2002) Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene 289: 109-118.
22. Jin, T., Bokarewa, M., McIntyre, L., Tarkowski, A., Corey, G.R., Reller, L.B., and Fowler, V.G., Jr (2003) Fatal outcome of bacteraemic patients caused by infection with staphylokinase-deficient Staphylococcus aureus strains. J Med Microbiol 52: 919-923.
23. Jin, T., Bokarewa, M., Foster, T., Mitchell, J., Higgins, J., and Tarkowski, A. (2004) Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol 172: 1169-1176.
24. Kahl, B.C., Duebbers, A., Lubritz, G., Haeberle, J., Koch, H.G., Ritzerfeld, B., et al. (2003) Population dynamics of persistent Staphylococcus aureus Isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J Clin Microbiol 41: 4424-4427.
25. Kaneko, J., Kimura, T., Narita, S., Tomita, T., and Kamio, Y. (1998) Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene 215: 57-67.
26. Kondo, I., and Fujise, K. (1977) Serotype B staphylococcal bacteriophage singly converting staphylokinase. Infect Immun 18: 266-272.
27. Kondo, I., Itoh, S., and Yoshizawa, Y. (1981) Staphylococcal phages mediating the lysogenic conversion of staphylokinase. In Staphylococci and Staphylococcal Infections. Jeljaszewicz, J. (ed.). Stuttgart, New York: Gustav Fischer Verlag, pp. 357-362.
28. Kuroda, M., Ohta, T., Uchiyama, I., Baba, T., Yuzawa, H., Kobayashi, I., et al. (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357: 1225-1240.
29. Kuusela, P., and Saksela, O. (1990) Binding and activation of plasminogen at the surface of Staphylococcus aureus. Increase in affinity after conversion to the Lys form of the ligand. Eur J Biochem 193: 759-765.
30. Lindsay, J.A., Moore, C.E., Day, N.P., Peacock, S.J., Witney, A.A., Stabler, R.A., et al. (2006) Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J Bacteriol 188: 669-676.
31. Luchansky, J.B., and Pattee, P.A. (1984) Isolation of transposon Tn551 insertions near chromosomal markers of interest in Staphylococcus aureus. J Bacteriol 159: 894-899.
32. Maiques, E., Ubeda, C., Campoy, S., Salvador, N., Lasa, I., Novick, R.P., et al. (2006) Beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J Bacteriol 188: 2726-2729.
33. Matthews, A.M., and Novick, R.P. (2005) Staphylococcal phages. In Phages. Their Role in Bacterial Pathogenesis and Biotechnology. Waldor, M.K., Friedman, D.I., and Adhya, S.L. (eds). Washington, DC: American Society for Microbiology Press, pp. 297-318.
34. Mellmann, A., Bielaszewska, M., Zimmerhackl, L.B., Prager, R., Harmsen, D., Tschape, H., and Karch, H. (2005) Enterohemorrhagic Escherichia coli in human infection: in vivo evolution of a bacterial pathogen. Clin Infect Dis 41: 785-792.
35. Moore, P.C.L., and Lindsay, J.A. (2001) Genetic variation among hospital isolates of methicillin-sensitive Staphylococcus aureus: evidence for horizontal transfer of virulence genes. J Clin Microbiol 39: 2760-2767.
36. Narita, S., Kaneko, J., Chiba, J., Piemont, Y., Jarraud, S., Etienne, J., and Kamio, Y. (2001) Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. Gene 268: 195-206.
37. Novick, R.P. (1967) Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33: 155-166.
38. Novick, R.P. (2003) Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49: 93-105.
39. O'Callaghan, R.J., Callegan, M.C., Moreau, J.M., Green, L.C., Foster, T.J., Hartford, O.M., et al. (1997) Specific roles of alpha-toxin and beta-toxin during Staphylococcus aureus corneal infection. J Biol Chem 265: 4652-4656.
40. Okada, K., Ueshima, S., Tanaka, M., Fukao, H., and Matsuo, O. (2000) Analysis of plasminogen activation by the plasmin-staphylokinase complex in plasma of alpha2-antiplasmin-deficient mice. Blood Coagul Fibrinolysis 11: 645-655.
41. Pantucek, R., Doskar, J., Ruzickova, V., Kasparek, P., Oracova, E., Kvardova, V., and Rosypal, S. (2004) Identification of bacteriophage types and their carriage in Staphylococcus aureus. Arch Virol 149: 1689-1703.
42. Peng, H.L., Novick, R.P., Kreiswirth, B.N., Kornblum, J., and Schlievert, P. (1988) Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 170: 4365-4372.
43. Rooijakkers, S.H., Ruyken, M., Roos, A., Daha, M.R., Presanis, J.S., Sim, R.B., et al. (2005) Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol 6: 920-927.
44. Sumby, P., andWaldor, M.K. (2003) Transcription of the toxin genes present within the Staphylococcal phage phiSa3ms is intimately linked with the phage's life cycle. J Bacteriol 185: 6841-6851.
45. Sun, H., Ringdahl, U., Homeister, J.W., Fay, W.P., Engleberg, N.C., Yang, A.Y., et al. (2004) Plasminogen is a critical host pathogenicity factor for group A streptococcal infection. Science 305: 1283-1286.
46. Tenover, F.C., Arbeit, R.D., Goering, R.V., Mickelsen, P.A., Murray, B.E., Persing, D.H., and Swaminathan, B. (1995) Interpreting chromosomal DMA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33: 2233-2239.
47. Wagner, P.L., andWaldor, M.K. (2002) Bacteriophage control of bacterial virulence. Infect Immun 70: 3985-3993.
48. Walev, I., Weller, U., Strauch, S., Foster, T.J., and Bhakdi, S. (1996) Selective killing of human monocytes and cytokine release provoked by sphingomyelinase (beta-toxin) of Staphylococcus aureus. Infect Immun 64: 2974-2979.
49. van Wamel, W.J.B., Rooijakkers, S.H.M., Ruyken, M., van Kessel, K.P.M., and van Strijp, J.A.G. (2006) The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on {beta}-hemolysin-converting bacteriophages. J Bacteriol 188: 1310-1315.
50. Wilkinson, D.M., Andrews, S., and Stewart, P.R. (1987) Bacteriophages associated with multiresistant Staphylococcus aureus in Australia. J Med Microbiol 23: 119-126.
51. Winkler, K.C., de, W.J., and Grootsen, C. (1965) Lysogenic conversion of staphylococci to loss of beta-toxin. J Gen Microbiol 39: 321-333.
52. Yamaguchi, T., Hayashi, T., Takami, H., Nakasone, K., Ohnishi, M., Nakayama, K., et al. (2000) Phage conversion of exfoliative toxin A production in Staphylococcus aureus. Mol Microbiol 38: 694-705.
53. Zou, D., Kaneko, J., Narita, S., and Kamio, Y. (2000) Prophage, phiPV83-pro, carrying panton-valentine leukocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of phiPV83-pro, phiPVL, phi11, and other phages. Biosci Biotechnol Biochem 64: 2631-2643.