Methicillin resistance reduces the virulence of healthcare-associated methicillin-resistant staphylococcus aureus by interfering with the agr quorum sensing system

Journal of Infectious Diseases

Volumn 205, Issue 5, 2012, Pages 798-806

  Rudkin, Justine K ^a   Edwards, Andrew M ^a   Bowden, Maria G ^b   Brown, Eric L ^c   Pozzi, Clarissa ^d   Waters, Elaine M ^d   Chan, Weng C ^e   Williams, Paul ^e   O'Gara, James P ^d   Massey, Ruth C ^a  

^a University of Bath   (United Kingdom)

^b TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^c UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; METICILLIN; PENICILLIN BINDING PROTEIN 2A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CLONE; COMMUNITY; COMMUNITY ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; CONTROLLED STUDY; CYTOTOXICITY; DISEASE MODEL; DISEASE TRANSMISSION; GENE EXPRESSION; GENE FUNCTION; HEALTHCARE ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MECA GENE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUORUM SENSING; SEPSIS; TOXIN SYNTHESIS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL SURVIVAL; CELL WALL; CROSS INFECTION; DISEASE MODELS, ANIMAL; GENE EXPRESSION; METHICILLIN RESISTANCE; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; PENICILLIN-BINDING PROTEINS; PEPTIDE SYNTHASES; QUORUM SENSING; SEPSIS; T-LYMPHOCYTES; TRANS-ACTIVATORS;

EID: 84856852784     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jir845     Document Type: Article

References (42)

1. Lowy FD. Staphylococcus aureus infections. N Engl J Med 1998; 339:520-32.
2. Gordon RJ, Lowy FD. Pathogenesis of methicillin-resistant Staphylococcus aureus infection. Clin Infect Dis 2008; 46:S350-9. (Pubitemid 351717322)
3. Deleo FR, Otto M, Kreiswirth BN, Chambers HF. Communityassociated meticillin-resistant Staphylococcus aureus. Lancet 2010; 375:1557-68.
4. Ito T, Katayama Y, Hiramatsu K. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 1999; 43:1449-58. (Pubitemid 29259342)
5. Hiramatsu K, Cui L, Kuroda M, Ito T. The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 2001; 9:486-93. (Pubitemid 32939356)
6. Hiramatsu K, Katayama Y, Yuzawa H, Ito T. Molecular genetics of methicillin-resistant Staphylococcus aureus. Int J Med Microbiol 2002; 292:67-74. (Pubitemid 34842177)
7. Sun Y, Bauer MD, Lu W. Identification of the active site serine of penicillin-binding protein 2a from methicillin-resistant Staphylococcus aureus by electrospray mass spectrometry. J Mass Spectrom 1998; 33:1009-16. (Pubitemid 28499670)
8. Schulthess B, Meier S, Homerova D, et al. Functional characterization of the sigmaB-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob Agents Chemother 2009; 53:1832-9.
9. Berger-Bächi B, Rohrer S. Factors influencing methicillin resistance in staphylococci. Arch Microbiol 2002; 178:165-71. (Pubitemid 34985297)
10. de Lencastre H, Wu SW, Pinho MG, et al. Antibiotic resistance as a stress response: complete sequencing of a large number of chromosomal loci in Staphylococcus aureus strain COL that impact on the expression of resistance to methicillin. Microb Drug Resist 1999; 5:163-75. (Pubitemid 29519892)
11. Cosgrove SE, Sakoulas G, Perencevich EN, et al. Comparison ofmortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003; 36:53-9. (Pubitemid 36099097)
12. Gastmeier P, Sohr D, Geffers C, et al. Mortality risk factors with nosocomial Staphylococcus aureus infections in intensive care units: results from the German Nosocomial Infection Surveillance System (KISS). Infection 2005; 33:50-5. (Pubitemid 40590991)
13. Reed SD, Friedman JY, Engemann JJ, et al. Costs and outcomes among hemodialysis-dependent patients with methicillin-resistant or methicillin-susceptible Staphylococcus aureus bacteremia. Infect Control Hosp Epidemiol 2005; 26:175-83. (Pubitemid 40445023)
14. Otto M. Basis of virulence in community-associated methicillin-resistant Staphylococcus aureus. Annu Rev Microbiol 2010; 64:143-62.
15. Li M, Diep BA, Villaruz AE, et al. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci USA 2009; 106:5883-8.
16. Vardakas KZ, Matthaiou DK, Falagas ME. Comparison of communityacquired pneumonia due to methicillin-resistant and methicillinsusceptible Staphylococcus aureus producing the Panton-Valentine leukocidin. Int J Tuberc Lung Dis 2009; 13:1476-85.
17. Miller LG, Quan C, Shay A, et al. A prospective investigation of outcomes after hospital discharge for endemic, community-acquired methicillin-resistant and-susceptible Staphylococcus aureus skin infection. Clin Infect Dis 2007; 44:483-92. (Pubitemid 46233248)
18. Collins J, Rudkin J, Recker M, et al. Offsetting virulence and antibiotic resistance costs by MRSA. ISME J 2010; 4:577-84.
19. O'Neill E, Pozzi C, Houston P, et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol 2008; 190:3835-50. (Pubitemid 351732862)
20. Novick RP, Geisinger E. Quorum sensing in staphylococci. Annu Rev Genet 2008; 42:541-64.
21. Peng HL, Novick RP, Kreiswirth B, Kornblum J, Schlievert P. Cloning, characterization, and sequencing of an accessory gene regulator (agr) in Staphylococcus aureus. J Bacteriol 1988; 170:4365-72.
22. Novick RP, Ross HF, Projan SJ, et al. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 1993; 12:3967-75. (Pubitemid 23282772)
23. Novick RP. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 1967; 33:155-66.
24. Enright MC, Day NP, Davies CE, et al. Multilocus sequence typing for characterization of methicillin-resistant and methicillinsusceptible clones of Staphylococcus aureus. J Clin Microbiol 2000; 38:1008-15. (Pubitemid 30140551)
25. Cookson BD, Robinson DA, Monk AB, et al. Evaluation of molecular typing methods in characterizing a European collection of epidemic methicillin- resistant Staphylococcus aureus strains: the HARMONY collection. J Clin Microbiol 2007; 45:1830-7. (Pubitemid 46933914)
26. Price J, Baker G, Heath I, et al. Clinical and microbiological determinants of outcome in Staphylococcus aureus bacteraemia. Int J Microbiol 2010: 654858.
27. Corrigan RM, Foster TJ. An improved tetracycline-inducible expression vector for Staphylococcus aureus. Plasmid 2009; 61:126-9.
28. Bruckner R. A series of shuttle vectors for Bacillus subtilis and Escherichia coli. Gene 1992; 122:187-92.
29. Qazi SN, Counil E, Morrissey J, et al. Agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect Immun 2001; 69:7074-82. (Pubitemid 32995468)
30. Collins J, Buckling A, Massey RC. Identification of factors contributing to T-cell toxicity of Staphylococcus aureus clinical isolates. J Clin Microbiol 2008; 46:2112-4. (Pubitemid 351831857)
31. McDowell P, Affas Z, Reynolds C, et al. Structure, activity and evolution of the group I thiolactone peptide quorum-sensing system of Staphylococcus aureus. Mol Microbiol 2001; 41:503-12. (Pubitemid 32730547)
32. Fowler VG, Sakoulas G, McIntyre LM, et al. Persistent bacteremia due to methicillin-resistant Staphylococcus aureus infection is associated with agr dysfunction and low-level in vitro resistance to thrombininduced platelet microbicidal protein. J Infect Dis 2004; 190:1140-9. (Pubitemid 39186802)
33. Recsei P, Kreiswirth B, O'Reilly M, et al. Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol Gen Genet 1986; 202: 58-61. (Pubitemid 16150393)
34. Haque R, Baldwin JN. Purification and properties of staphylococcal beta-hemolysin. J Bacteriol 1964; 88:1304-9.
35. Queck SY, Khan BA, Wang R, et al. Mobile genetic element-encoded cytolysin connects virulence to methicillin resistance in MRSA. PLoS Pathog 2009; 5:e1000533.
36. Kaito C, Saito Y, Nagano G, et al. Transcription and translation products of the cytolysin gene psm-mec on the mobile genetic element SCCmec regulate Staphylococcus aureus virulence. PLoS Pathog 2011; 7:e1001267.
37. Traber K, Novick R. 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 2006; 59:1519-30.
38. Shopsin B, Eaton C, Wasserman GA, et al. Mutations in agr do not persist in natural populations of methicillin-resistant Staphylococcus aureus. J Infect Dis 2010; 202:1593-9.
39. de Jonge BLM, Tomasz T. Abnormal peptidoglycan produced in a methicillin-resistant strain of Staphylococcus aureus grown in the presence of methicillin: functional role for penicillin-binding protein 2A in cell wall synthesis. Antimicrob Agents Chemother 1993; 37:342-6.
40. de Jonge BLM, Chang YS, Gage D, Tomasz A. Peptidoglycan composition of a highly methicillin-resistant Staphylococcus aureus strain. J Biol Chem 1992; 267:11248-64.
41. Okuma K, Iwakawa K, Turnidge JD, et al. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol 2002; 40:4289-94. (Pubitemid 35285827)
42. Kreiswirth BN, Löfdahl S, Betley MJ, et al. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 1983; 305:709-12. (Pubitemid 13021519)