Importance of the global regulators agr and SaeRS in the pathogenesis of CA-MRSA USA300 infection

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Montgomery, Christopher P ^a   Boyle Vavra, Susan ^a   Daum, Robert S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCESSORY GENE REGULATOR PROTEIN; ALPHA HEMOLYSIN; BACTERIAL PROTEIN; PANTON VALENTINE LEUKOCIDIN; REGULATOR PROTEIN; STAPHYLOCOCCUS AUREUS ACCESSORY ELEMENT RS PROTEIN; STAPHYLOCOCCUS PROTEIN A; TOXIN; UNCLASSIFIED DRUG; AGR PROTEIN, STAPHYLOCOCCUS AUREUS; BACTERIAL TOXIN; EXOTOXIN; HEMOLYSIN; LEUKOCIDIN; PANTON-VALENTINE LEUKOCIDIN; PROTEIN KINASE; SAER PROTEIN, STAPHYLOCOCCUS AUREUS; SAES PROTEIN, STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCAL ALPHA-TOXIN; STAPHYLOCOCCUS ALPHA TOXIN; TRANSACTIVATOR PROTEIN; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CONTROLLED STUDY; DELETION MUTANT; GENE DELETION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOUSE; NONHUMAN; PATHOGENESIS; PHENOTYPIC VARIATION; PNEUMONIA; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SKIN INFECTION; WESTERN BLOTTING; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; LUNG; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIOLOGY; PHENOTYPE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRULENCE;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; EXOTOXINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HEMOLYSIN PROTEINS; LEUKOCIDINS; LUNG; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; PHENOTYPE; PROTEIN KINASES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS; VIRULENCE; VIRULENCE FACTORS;

EID: 78649918595     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015177     Document Type: Article

References (51)

1. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, et al. (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298: 1763-1771.
2. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616-687.
3. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, et al. (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279: 593-598.
4. Mongkolrattanothai K, Boyle S, Kahana MD, Daum RS (2003) Severe Staphylococcus aureus infections caused by clonally related community-acquired methicillin-susceptible and methicillin-resistant isolates. Clin Infect Dis 37: 1050-1058.
5. Centers for Disease Control and Prevention (1999) Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus-Minnesota and North Dakota, 1997-1999. JAMA 282: 1123-1125.
6. Furtado N, Mangat PD, Frank AL, Janda W, Boyle-Vavra S, et al. (2006) Two clindamycin-susceptible (community-associated) MRSA (CA-MRSA) epidemics in Chicago. Toronto: Program and abstracts of the 44th meeting of the Infectious Diseases Society of America. 117 p.
7. Montgomery CP, Boyle-Vavra S, Adem PV, Lee JC, Husain AN, et al. (2008) Comparison of Virulence in Community-Associated Methicillin-Resistant Staphylococcus aureus Pulsotypes USA300 and USA400 in a Rat Model of Pneumonia. J Infect Dis 198: 561-570.
8. Voyich JM, Otto M, Mathema B, Braughton KR, Whitney AR, et al. (2006) Is Panton-Valentine leukocidin the major virulence determinant in communityassociated methicillin-resistant Staphylococcus aureus disease? J Infect Dis 194: 1761-1770.
9. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731-739.
10. Highlander SK, Hulten KG, Qin X, Jiang H, Yerrapragada S, et al. (2007) Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus. BMC Microbiol 7: 99.
11. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, et al. (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillinresistant Staphylococcus aureus. J Infect Dis 197: 1523-1530.
12. Montgomery CP, Boyle-Vavra S, Daum RS (2009) The Arginine Catabolic Mobile Element (ACME) is not associated with enhanced virulence in experimental invasive disease caused by the community-associated methicillinresistant Staphylococcus aureus (CA-MRSA) genetic background USA300. Infect Immun.
13. Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, et al. (2007) Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 315: 1130-1133.
14. Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O (2007) Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 13: 1405-1406.
15. Bubeck Wardenburg J, Palazzolo-Ballance AM, Otto M, Schneewind O, DeLeo FR (2008) Panton-Valentine leukocidin is not a virulence determinant in murine models of community-associated methicillin-resistant Staphylococcus aureus disease. J Infect Dis 198: 1166-1170.
16. Brown EL, Dumitrescu O, Thomas D, Badiou C, Koers EM, et al. (2009) The Panton-Valentine leukocidin vaccine protects mice against lung and skin infections caused by Staphylococcus aureus USA300. Clin Microbiol Infect 15: 156-164.
17. Montgomery CP, Daum RS (2009) Transcription of inflammatory genes in the lung after infection with community-associated methicillin-resistant Staphylococcus aureus: A role for Panton-Valentine Leukocidin? Infect Immun.
18. Tseng CW, Kyme P, Low J, Rocha MA, Alsabeh R, et al. (2009) Staphylococcus aureus Panton-Valentine leukocidin contributes to inflammation and muscle tissue injury. PLoS One 4: e6387.
19. Diep BA, Chan L, Tattevin P, Kajikawa O, Martin TR, et al. (2010) Polymorphonuclear leukocytes mediate Staphylococcus aureus Panton-Valentine leukocidin-induced lung inflammation and injury. Proc Natl Acad Sci U S A 107: 5587-5592.
20. Boyle-Vavra S, Daum RS (2007) Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 87: 3-9.
21. Kennedy AD, Wardenburg JB, Gardner DJ, Long D, Whitney AR, et al. (2010) Targeting of Alpha-Hemolysin by Active or Passive Immunization Decreases Severity of USA300 Skin Infection in a Mouse Model. J Infect Dis 202: 1050-1058.
22. Cheung AL, Bayer AS, Zhang G, Gresham H, Xiong YQ (2004) Regulation of virulence determinants in vitro and in vivo in Staphylococcus aureus. FEMS Immunol Med Microbiol 40: 1-9.
23. Kornblum J, Kreisworth B, Projan SJ, Ross H, Novick RP (1990) Agr: A polycistronic locus regulating exoprotein synthesis in Staphylococcus aureus. In: Novick R, ed. Molecular Biology of the Staphylococci. New York: VCH Publishers.
24. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, et al. (1993) Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12: 3967-3975.
25. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G, et al. (2001) Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J Bacteriol 183: 7341-7353.
26. Bronner S, Stoessel P, Gravet A, Monteil H, Prevost G (2000) Variable expressions of Staphylococcus aureus bicomponent leucotoxins semiquantified by competitive reverse transcription-PCR. Appl Environ Microbiol 66: 3931-3938.
27. Vandenesch F, Kornblum J, Novick RP (1991) A temporal signal, independent of agr, is required for hla but not spa transcription in Staphylococcus aureus. J Bacteriol 173: 6313-6320.
28. Recsei P, Kreiswirth B, O'Reilly M, Schlievert P, Gruss A, et al. (1986) Regulation of exoprotein gene expression in Staphylococcus aureus by agr. Mol Gen Genet 202: 58-61.
29. Giraudo AT, Calzolari A, Cataldi AA, Bogni C, Nagel R (1999) The sae locus of Staphylococcus aureus encodes a two-component regulatory system. FEMS Microbiol Lett 177: 15-22.
30. Adhikari RP, Novick RP (2008) Regulatory organization of the staphylococcal sae locus. Microbiology 154: 949-959.
31. Voyich JM, Braughton KR, Sturdevant DE, Whitney AR, Said-Salim B, et al. (2005) Insights into mechanisms used by Staphylococcus aureus to avoid destruction by human neutrophils. J Immunol 175: 3907-3919.
32. Rogasch K, Ruhmling V, Pane-Farre J, Hoper D, Weinberg C, et al. (2006) Influence of the two-component system SaeRS on global gene expression in two different Staphylococcus aureus strains. J Bacteriol 188: 7742-7758.
33. Voyich JM, Vuong C, Dewald M, Nygaard TK, Kocianova S, et al. (2009) The SaeR/S Gene Regulatory System Is Essential for Innate Immune Evasion by Staphylococcus aureus. J Infect Dis 199: 1698-1706.
34. Nygaard TK, Pallister KB, Ruzevich P, Griffith S, Vuong C, et al. (2010) SaeR binds a consensus sequence within virulence gene promoters to advance USA300 pathogenesis. J Infect Dis 201: 241-254.
35. Boyle-Vavra S, Yin S, Daum RS (2006) The VraS/VraR two-component regulatory system required for oxacillin resistance in community-acquired methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 262: 163-171.
36. Arnaud M, Chastanet A, Debarbouille M (2004) New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl Environ Microbiol 70: 6887-6891.
37. Bubeck Wardenburg J, Patel RJ, Schneewind O (2007) Surface proteins and exotoxins are required for the pathogenesis of Staphylococcus aureus pneumonia. Infect Immun 75: 1040-1044.
38. Heyer G, Saba S, Adamo R, Rush W, Soong G, et al. (2002) Staphylococcus aureus agr and sarA functions are required for invasive infection but not inflammatory responses in the lung. Infect Immun 70: 127-133.
39. Wright JS, 3rd, Jin R, Novick RP (2005) Transient interference with staphylococcal quorum sensing blocks abscess formation. Proc Natl Acad Sci U S A 102: 1691-1696.
40. Park J, Jagasia R, Kaufmann GF, Mathison JC, Ruiz DI, et al. (2007) Infection control by antibody disruption of bacterial quorum sensing signaling. Chem Biol 14: 1119-1127.
41. Abdelnour A, Arvidson S, Bremell T, Ryden C, Tarkowski A (1993) The accessory gene regulator (agr) controls Staphylococcus aureus virulence in a murine arthritis model. Infect Immun 61: 3879-3885.
42. Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, et al. (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63: 3373-3380.
43. Xiong YQ, Willard J, Yeaman MR, Cheung AL, Bayer AS (2006) Regulation of Staphylococcus aureus alpha-toxin gene (hla) expression by agr, sarA, and sae in vitro and in experimental infective endocarditis. J Infect Dis 194: 1267-1275.
44. Balaban N, Novick RP (1995) Translation of RNAIII, the Staphylococcus aureus agr regulatory RNA molecule, can be activated by a 39-end deletion. FEMS Microbiol Lett 133: 155-161.
45. Diep BA, Palazzolo-Ballance AM, Tattevin P, Basuino L, Braughton KR, et al. (2008) Contribution of Panton-Valentine leukocidin in community-associated methicillin-resistant Staphylococcus aureus pathogenesis. PLoS ONE 3: e3198.
46. Loffler B, Hussain M, Grundmeier M, Bruck M, Holzinger D, et al. (2010) Staphylococcus aureus panton-valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog 6: e1000715.
47. Gomez MI, Lee A, Reddy B, Muir A, Soong G, et al. (2004) Staphylococcus aureus protein A induces airway epithelial inflammatory responses by activating TNFR1. Nat Med 10: 842-848.
48. Liang X, Yu C, Sun J, Liu H, Landwehr C, et al. (2006) Inactivation of a twocomponent signal transduction system, SaeRS, eliminates adherence and attenuates virulence of Staphylococcus aureus. Infect Immun 74: 4655-4665.
49. Li M, Diep BA, Villaruz AE, Braughton KR, Jiang X, et al. (2009) Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 106: 5883-5888.
50. Said-Salim B, Mathema B, Braughton K, Davis S, Sinsimer D, et al. (2005) Differential distribution and expression of Panton-Valentine leucocidin among community-acquired methicillin-resistant Staphylococcus aureus strains. J Clin Microbiol 43: 3373-3379.
51. Lee MH, Arrecubieta C, Martin FJ, Prince A, Borczuk AC, et al. (2010) A postinfluenza model of Staphylococcus aureus pneumonia. J Infect Dis 201: 508-515.