AsrR Is an Oxidative Stress Sensing Regulator Modulating Enterococcus faecium Opportunistic Traits, Antimicrobial Resistance, and Pathogenicity

PLoS Pathogens

Volumn 8, Issue 8, 2012, Pages

  Lebreton, François ^a,e   van Schaik, Willem ^b   Sanguinetti, Maurizio ^c   Posteraro, Brunella ^c   Torelli, Riccardo ^c   Le Bras, Florian ^a   Verneuil, Nicolas ^a   Zhang, Xinglin ^b   Giard, Jean Christophe ^a   Dhalluin, Anne ^a   Willems, Rob J L ^b   Leclercq, Roland ^a,d   Cattoir, Vincent ^a,d  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c CATHOLIC UNIVERSITY   (Italy)

^d CAEN UNIVERSITY HOSPITAL   (France)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; AMPICILLIN; BETA LACTAM ANTIBIOTIC; CYSTEINE; ERYTHROMYCIN; FUSIDIC ACID; GENTAMICIN; KANAMYCIN; LINCOMYCIN; PENICILLIN BINDING PROTEIN; PENICILLIN G; PROTEIN ACM; PROTEIN ASRR; PROTEIN ECBA; REGULATOR PROTEIN; RIFAMPICIN; SPECTINOMYCIN; STREPTOMYCIN; TETRACYCLINE; TRANSCRIPTOME; UNCLASSIFIED DRUG; VANCOMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BIOSENSOR; CELL ADHESION; CONTROLLED STUDY; ENTEROCOCCUS FAECIUM; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MALE; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPPORTUNISTIC INFECTION; OXIDATIVE STRESS; PROTEIN DNA BINDING; REGULON;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; ENTEROCOCCUS FAECIUM; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; HYDROGEN PEROXIDE; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, INBRED BALB C; OXIDANTS; OXIDATION-REDUCTION; QUANTITATIVE TRAIT, HERITABLE; TRANSCRIPTION FACTORS;

ENTEROCOCCUS FAECIUM; GALLERIA MELLONELLA; MURINAE;

EID: 84866152324     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002834     Document Type: Article

References (91)

1. Hidron AI, Edwards JR, Patel J, Horan TC, Sievert DM, et al. (2008) NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect Control Hosp Epidemiol 29: 996-1011.
2. Murray BE, (1990) The life and times of the Enterococcus. Clin Microbiol Rev 3: 46-65.
3. Murray BE, (2000) Vancomycin-resistant enterococcal infections. N Engl J Med 342: 710-721.
4. Chang S, Sievert DM, Hageman JC, Boulton ML, Tenover FC, et al. (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 348: 1342-1347.
5. Tenover FC, Weigel LM, Appelbaum PC, McDougal LK, Chaitram J, et al. (2004) Vancomycin-resistant Staphylococcus aureus isolate from a patient in Pennsylvania. Antimicrob Agents Chemother 48: 275-280.
6. Dupont H, Vael C, Muller-Serieys C, Chosidow D, Mantz J, et al. (2008) Prospective evaluation of virulence factors of enterococci isolated from patients with peritonitis: impact on outcome. Diagn Microbiol Infect Dis 60: 247-253.
7. van Schaik W, Top J, Riley DR, Boekhorst J, Vrijenhoek JE, et al. (2010) Pyrosequencing-based comparative genome analysis of the nosocomial pathogen Enterococcus faecium and identification of a large transferable pathogenicity island. BMC Genomics 11: 239.
8. Leendertse M, Heikens E, Wijnands LM, van Luit-Asbroek M, Teske GJ, et al. (2009) Enterococcal surface protein transiently aggravates Enterococcus faecium-induced urinary tract infection in mice. J Infect Dis 200: 1162-1165.
9. Nallapareddy SR, Singh KV, Murray BE, (2008) Contribution of the collagen adhesin Acm to pathogenesis of Enterococcus faecium in experimental endocarditis. Infect Immun 76: 4120-4128.
10. Coburn PS, Baghdayan AS, Dolan GT, Shankar N, (2008) An AraC-type transcriptional regulator encoded on the Enterococcus faecalis pathogenicity island contributes to pathogenesis and intracellular macrophage survival. Infect Immun 76: 5668-5676.
11. Giard JC, Riboulet E, Verneuil N, Sanguinetti M, Auffray Y, et al. (2006) Characterization of Ers, a PrfA-like regulator of Enterococcus faecalis. FEMS Immunol Med Microbiol 46: 410-418.
12. Ogier JC, Serror P, (2008) Safety assessment of dairy microorganisms: the Enterococcus genus. Int J Food Microbiol 126: 291-301.
13. Michaux C, Sanguinetti M, Reffuveille F, Auffray Y, Posteraro B, et al. (2011) SlyA Is a Transcriptional Regulator Involved in the Virulence of Enterococcus faecalis. Infect Immun 79: 2638-2645.
14. Bronner S, Monteil H, Prevost G, (2004) Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol Rev 28: 183-200.
15. Chen PR, Bae T, Williams WA, Duguid EM, Rice PA, et al. (2006) An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat Chem Biol 2: 591-595.
16. Chen PR, Nishida S, Poor CB, Cheng A, Bae T, et al. (2009) A new oxidative sensing and regulation pathway mediated by the MgrA homologue SarZ in Staphylococcus aureus. Mol Microbiol 71: 198-211.
17. 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.
18. Cheung AL, Nishina KA, Trotonda MP, Tamber S, (2008) The SarA protein family of Staphylococcus aureus. Int J Biochem Cell Biol 40: 355-361.
19. Hong M, Fuangthong M, Helmann JD, Brennan RG, (2005) Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family. Mol Cell 20: 131-141.
20. Fuangthong M, Atichartpongkul S, Mongkolsuk S, Helmann JD, (2001) OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J Bacteriol 183: 4134-4141.
21. Mongkolsuk S, Helmann JD, (2002) Regulation of inducible peroxide stress responses. Mol Microbiol 45: 9-15.
22. Newberry KJ, Fuangthong M, Panmanee W, Mongkolsuk S, Brennan RG, (2007) Structural mechanism of organic hydroperoxide induction of the transcription regulator OhrR. Mol Cell 28: 652-664.
23. Sukchawalit R, Loprasert S, Atichartpongkul S, Mongkolsuk S, (2001) Complex regulation of the organic hydroperoxide resistance gene (ohr) from Xanthomonas involves OhrR, a novel organic peroxide-inducible negative regulator, and posttranscriptional modifications. J Bacteriol 183: 4405-4412.
24. 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.
25. Luong TT, Dunman PM, Murphy E, Projan SJ, Lee CY, (2006) Transcription Profiling of the MgrA Regulon in Staphylococcus aureus. J Bacteriol 188: 1899-1910.
26. Lan L, Murray TS, Kazmierczak BI, He C, (2010) Pseudomonas aeruginosa OspR is an oxidative stress sensing regulator that affects pigment production, antibiotic resistance and dissemination during infection. Mol Microbiol 75: 76-91.
27. Chuchue T, Tanboon W, Prapagdee B, Dubbs JM, Vattanaviboon P, et al. (2006) ohrR and ohr are the primary sensor/regulator and protective genes against organic hydroperoxide stress in Agrobacterium tumefaciens. J Bacteriol 188: 842-851.
28. Wilkinson SP, Grove A, (2006) Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr Issues Mol Biol 8: 51-62.
29. Abi Khattar Z, Rejasse A, Destoumieux-Garzon D, Escoubas JM, Sanchis V, et al. (2009) The dlt operon of Bacillus cereus is required for resistance to cationic antimicrobial peptides and for virulence in insects. J Bacteriol 191: 7063-7073.
30. Le Jeune A, Torelli R, Sanguinetti M, Giard JC, Hartke A, et al. (2010) The extracytoplasmic function sigma factor SigV plays a key role in the original model of lysozyme resistance and virulence of Enterococcus faecalis. PLoS One 5: e9658.
31. Peschel A, Otto M, Jack RW, Kalbacher H, Jung G, et al. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J Biol Chem 274: 8405-8410.
32. Rice LB, Carias LL, Hutton-Thomas R, Sifaoui F, Gutmann L, et al. (2001) Penicillin-binding protein 5 and expression of ampicillin resistance in Enterococcus faecium. Antimicrob Agents Chemother 45: 1480-1486.
33. Nallapareddy SR, Weinstock GM, Murray BE, (2003) Clinical isolates of Enterococcus faecium exhibit strain-specific collagen binding mediated by Acm, a new member of the MSCRAMM family. Mol Microbiol 47: 1733-1747.
34. Hendrickx AP, Willems RJ, Bonten MJ, van Schaik W, (2009) LPxTG surface proteins of enterococci. Trends Microbiol 17: 423-430.
35. Purves J, Cockayne A, Moody PC, Morrissey JA, (2010) Comparison of the regulation, metabolic functions, and roles in virulence of the glyceraldehyde-3-phosphate dehydrogenase homologues gapA and gapB in Staphylococcus aureus. Infect Immun 78: 5223-5232.
36. Choudhury T, Singh KV, Sillanpaa J, Nallapareddy SR, Murray BE, (2011) Importance of two Enterococcus faecium loci encoding Gls-like proteins for in vitro bile salts stress response and virulence. J Infect Dis 203: 1147-1154.
37. Benachour A, Muller C, Dabrowski-Coton M, Le Breton Y, Giard JC, et al. (2005) The Enterococcus faecalis SigV protein is an extracytoplasmic function sigma factor contributing to survival following heat, acid, and ethanol treatments. J Bacteriol 187: 1022-1035.
38. Storch GA, Krogstad DJ, (1981) Antibiotic-induced lysis of enterococci. J Clin Invest 68: 639-645.
39. McBride SM, Sonenshein AL, (2011) The dlt operon confers resistance to cationic antimicrobial peptides in Clostridium difficile. Microbiology 157 (Pt 5):: 1457-1465.
40. Murli S, Walker GC, (1993) SOS mutagenesis. Curr Opin Genet Dev 3: 719-725.
41. Bergin D, Reeves EP, Renwick J, Wientjes FB, Kavanagh K, (2005) Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73: 4161-4170.
42. Lebreton F, Le Bras F, Reffuveille F, Ladjouzi R, Giard JC, et al. (2011) Galleria mellonella as a model for studying Enterococcus faecium host persistence. J Mol Microb Biotech 21: 191-196.
43. Imlay JA, (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776.
44. Poole LB, Nelson KJ, (2008) Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 12: 18-24.
45. Scandalios JG, (1997) Oxidative stress and defense mechanisms in plants: introduction. Free Radic Biol Med 23: 471-472.
46. Panmanee W, Vattanaviboon P, Poole LB, Mongkolsuk S, (2006) Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. J Bacteriol 188: 1389-1395.
47. Soonsanga S, Lee JW, Helmann JD, (2008) Conversion of Bacillus subtilis OhrR from a 1-Cys to a 2-Cys peroxide sensor. J Bacteriol 190: 5738-5745.
48. Frankenberg L, Brugna M, Hederstedt L, (2002) An Enterococcus faecalis heme-dependent catalase. J Bacteriol 184: 6351-6356.
49. Baureder M, Reimann R, Hederstedt L, (2012) Contribution of catalase to hydrogen peroxide resistance in Enterococcus faecalis. FEMS Microbiol Lett 331: 160-164.
50. La Carbona S, Sauvageot N, Giard JC, Benachour A, Posteraro B, et al. (2007) Comparative study of the physiological roles of three peroxidases (NADH peroxidase, Alkylhydroperoxide reductase and Thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 66: 1148-1163.
51. Riboulet E, Verneuil N, La Carbona S, Sauvageot N, Auffray Y, et al. (2007) Relationships between oxidative stress response and virulence in Enterococcus faecalis. J Mol Microbiol Biotechnol 13: 140-146.
52. Imlay JA, Linn S, (1986) Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide. J Bacteriol 166: 519-527.
53. Thibessard A, Borges F, Fernandez A, Gintz B, Decaris B, et al. (2004) Identification of Streptococcus thermophilus CNRZ368 genes involved in defense against superoxide stress. Appl Environ Microbiol 70: 2220-2229.
54. Fontana R, Cerini R, Longoni P, Grossato A, Canepari P, (1983) Identification of a streptococcal penicillin-binding protein that reacts very slowly with penicillin. J Bacteriol 155: 1343-1350.
55. Fontana R, (1985) Penicillin-binding proteins and the intrinsic resistance to beta-lactams in gram-positive cocci. J Antimicrob Chemother 16: 412-416.
56. Trotonda MP, Xiong YQ, Memmi G, Bayer AS, Cheung AL, (2009) Role of mgrA and sarA in methicillin-resistant Staphylococcus aureus autolysis and resistance to cell wall-active antibiotics. J Infect Dis 199: 209-218.
57. Truong-Bolduc QC, Hooper DC, (2007) The transcriptional regulators NorG and MgrA modulate resistance to both quinolones and beta-lactams in Staphylococcus aureus. J Bacteriol 189: 2996-3005.
58. Sahm DF, Marsilio MK, Piazza G, (1999) Antimicrobial resistance in key bloodstream bacterial isolates: electronic surveillance with the Surveillance Network Database-USA. Clin Infect Dis 29: 259-263.
59. Rice KC, Bayles KW, (2008) Molecular Control of Bacterial Death and Lysis. Microbiol Mol Biol 72: 85-109.
60. Hendrickx AP, van Luit-Asbroek M, Schapendonk CM, van Wamel WJ, Braat JC, et al. (2009) SgrA, a nidogen-binding LPXTG surface adhesin implicated in biofilm formation, and EcbA, a collagen binding MSCRAMM, are two novel adhesins of hospital-acquired Enterococcus faecium. Infect Immun 77: 5097-5106.
61. Nallapareddy SR, Singh KV, Murray BE, (2006) Construction of improved temperature-sensitive and mobilizable vectors and their use for constructing mutations in the adhesin-encoding acm gene of poorly transformable clinical Enterococcus faecium strains. Appl Environ Microbiol 72: 334-345.
62. Sillanpaa J, Nallapareddy SR, Prakash VP, Qin X, Hook M, et al. (2008) Identification and phenotypic characterization of a second collagen adhesin, Scm, and genome-based identification and analysis of 13 other predicted MSCRAMMs, including four distinct pilus loci, in Enterococcus faecium. Microbiology 154 (Pt 10):: 3199-3211.
63. Trotonda MP, Tamber S, Memmi G, Cheung AL, (2008) MgrA represses biofilm formation in Staphylococcus aureus. Infect Immun 76: 5645-5654.
64. Fedtke I, Gotz F, Peschel A, (2004) Bacterial evasion of innate host defenses-the Staphylococcus aureus lesson. Int J Med Microbiol 294: 189-194.
65. Kavanagh K, Reeves EP, (2004) Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev 28: 101-112.
66. Lebreton F, Riboulet-Bisson E, Serror P, Sanguinetti M, Posteraro B, et al. (2009) ace, Which encodes an adhesin in Enterococcus faecalis, is regulated by Ers and is involved in virulence. Infect Immun 77: 2832-2839.
67. Olsen RJ, Watkins ME, Cantu CC, Beres SB, Musser JM, (2011) Virulence of serotype M3 Group A Streptococcus strains in wax worms (Galleria mellonella larvae). Virulence 2: 111-119.
68. Jander G, Rahme LG, Ausubel FM, (2000) Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182: 3843-3845.
69. Ozawa Y, Tanimoto K, Fujimoto S, Tomita H, Ike Y, (1997) Cloning and genetic analysis of the UV resistance determinant (uvr) encoded on the Enterococcus faecalis pheromone-responsive conjugative plasmid pAD1. J Bacteriol 179: 7468-7475.
70. Woodgate R, Sedgwick SG, (1992) Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues. Mol Microbiol 6: 2213-2218.
71. Hall BG, (1995) Genetics of selection-induced mutations: I. uvrA, uvrB, uvrC, and uvrD are selection-induced specific mutator loci. J Mol Evol 40: 86-93.
72. van der Meer JR, Sentchilo V, (2003) Genomic islands and the evolution of catabolic pathways in bacteria. Curr Opin Biotechnol 14: 248-254.
73. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD, (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci U S A 102: 12554-12559.
74. Ingavale S, van Wamel W, Luong TT, Lee CY, Cheung AL, (2005) Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus. Infect Immun 73: 1423-1431.
75. Navarre WW, Halsey TA, Walthers D, Frye J, McClelland M, et al. (2005) Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 56: 492-508.
76. Shatalin K, Gusarov I, Avetissova E, Shatalina Y, McQuade LE, et al. (2008) Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc Natl Acad Sci U S A 105: 1009-1013.
77. Maguin E, Prevost H, Ehrlich SD, Gruss A, (1996) Efficient insertional mutagenesis in lactococci and other gram-positive bacteria. J Bacteriol 178: 931-935.
78. Que YA, Haefliger JA, Francioli P, Moreillon P, (2000) Expression of Staphylococcus aureus clumping factor A in Lactococcus lactis subsp. cremoris using a new shuttle vector. Infect Immun 68: 3516-3522.
79. Bozdogan B, Leclercq R, (1999) Effects of genes encoding resistance to streptogramins A and B on the activity of quinupristin-dalfopristin against Enterococcus faecium. Antimicrob Agents Chemother 43: 2720-2725.
80. Celli J, Poyart C, Trieu-Cuot P, (1997) Use of an excision reporter plasmid to study the intracellular mobility of the conjugative transposon Tn916 in gram-positive bacteria. Microbiology 143: 1253-1261.
81. Trzcinski K, Cooper BS, Hryniewicz W, Dowson CG, (2000) Expression of resistance to tetracyclines in strains of methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 45: 763-770.
82. Riboulet-Bisson E, Sanguinetti M, Budin-Verneuil A, Auffray Y, Hartke A, et al. (2008) Characterization of the Ers regulon of Enterococcus faecalis. Infect Immun 76: 3064-3074.
83. Zhang X, Paganelli FL, Bierschenk D, Kuipers A, Bonten MJM, et al. (2012) Genome-wide identification of ampicillin resistance determinants in Enterococcus faecium. PLoS Genet 8: e1002804.
84. Hsiao A, Worrall DS, Olefsky JM, Subramaniam S, (2004) Variance-modeled posterior inference of microarray data: detecting gene-expression changes in 3T3-L1 adipocytes. Bioinformatics 20: 3108-3127.
85. Hsiao A, Ideker T, Olefsky JM, Subramaniam S, (2005) VAMPIRE microarray suite: a web-based platform for the interpretation of gene expression data. Nucleic Acids Res 33: W627-632.
86. Comité de l'Antibiogramme de la Société Française de Microbiologie (1996) Technical recommendations for in vitro susceptibility testing. Clin Microbiol Infect 2: S11-S25.
87. Moellering RC Jr, Wennersten C, Weinberg AN, (1971) Studies on antibiotic synergism against enterococci. I. Bacteriologic studies. J Lab Clin Med 77: 821-828.
88. Verneuil N, Maze A, Sanguinetti M, Laplace JM, Benachour A, et al. (2006) Implication of (Mn)superoxide dismutase of Enterococcus faecalis in oxidative stress responses and survival inside macrophages. Microbiology 152: 2579-2589.
89. Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ, (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130: 797-810.
90. Gentry-Weeks CR, Karkhoff-Schweizer R, Pikis A, Estay M, Keith JM, (1999) Survival of Enterococcus faecalis in mouse peritoneal macrophages. Infect Immun 67: 2160-2165.
91. Zhao C, Hartke A, La Sorda M, Posteraro B, Laplace JM, et al. (2010) Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect Immun 78: 3889-3897.