The Cell Wall-Targeting Antibiotic Stimulon of Enterococcus faecalis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Abranches, Jacqueline ^a   Tijerina, Pamella ^a   Avilés Reyes, Alejandro ^a   Gaca, Anthony O ^a   Kajfasz, Jessica K ^a   Lemos, José A ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACITRACIN; CEFALOTIN; VANCOMYCIN; ANTIINFECTIVE AGENT; TRANSCRIPTOME;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DOWN REGULATION; ENERGY METABOLISM; ENTEROCOCCUS FAECALIS; GALLERIA MELLONELLA; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STIMULON; UPREGULATION; ANIMAL; CELL WALL; CYTOLOGY; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; KINETICS; LEPIDOPTERA; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MUTATION; PATHOGENICITY; VIRULENCE;

ENTEROCOCCUS FAECALIS; GALLERIA MELLONELLA;

ANIMALS; ANTI-BACTERIAL AGENTS; CELL WALL; ENTEROCOCCUS FAECALIS; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC LOCI; KINETICS; LEPIDOPTERA; MICROBIAL SENSITIVITY TESTS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTOME; UP-REGULATION; VIRULENCE;

EID: 84878623459     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064875     Document Type: Article

References (56)

1. Arias CA, Murray BE, (2012) The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 10: 266-278.
2. Murray BE, (1990) The life and times of the Enterococcus. Clin Microbiol Rev 3: 46-65.
3. Hollenbeck BL, Rice LB, (2012) Intrinsic and acquired resistance mechanisms in Enterococcus. Virulence 3: 421-433.
4. Bearman GM, Wenzel RP, (2005) Bacteremias: a leading cause of death. Arch Med Res 36: 646-659.
5. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, et al. (2003) Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science 302: 1569-1571.
6. Pallares R, Pujol M, Pena C, Ariza J, Martin R, et al. (1993) Cephalosporins as risk factor for nosocomial Enterococcus faecalis bacteremia. A matched case-control study. Arch Intern Med 153: 1581-1586.
7. Fontana R, Ligozzi M, Pittaluga F, Satta G, (1996) Intrinsic penicillin resistance in enterococci. Microb Drug Resist 2: 209-213.
8. McAleese F, Wu SW, Sieradzki K, Dunman P, Murphy E, et al. (2006) Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate- S. aureus-type resistance to vancomycin. J Bacteriol 188: 1120-1133.
9. Muthaiyan A, Silverman JA, Jayaswal RK, Wilkinson BJ, (2008) Transcriptional profiling reveals that daptomycin induces the Staphylococcus aureus cell wall stress stimulon and genes responsive to membrane depolarization. Antimicrob Agents Chemother 52: 980-990.
10. Song Y, Lunde CS, Benton BM, Wilkinson BJ, (2012) Further insights into the mode of action of the lipoglycopeptide telavancin through global gene expression studies. Antimicrob Agents Chemother 56: 3157-3164.
11. Breidenstein EB, Bains M, Hancock RE, (2012) Involvement of the lon protease in the SOS response triggered by ciprofloxacin in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 56: 2879-2887.
12. Aakra A, Vebo H, Snipen L, Hirt H, Aastveit A, et al. (2005) Transcriptional response of Enterococcus faecalis V583 to erythromycin. Antimicrob Agents Chemother 49: 2246-2259.
13. Vebo HC, Snipen L, Nes IF, Brede DA, (2009) The transcriptome of the nosocomial pathogen Enterococcus faecalis V583 reveals adaptive responses to growth in blood. PLoS One 4: e7660.
14. Vebo HC, Solheim M, Snipen L, Nes IF, Brede DA, (2010) Comparative genomic analysis of pathogenic and probiotic Enterococcus faecalis isolates, and their transcriptional responses to growth in human urine. PLoS One 5: e12489.
15. Aakra A, Vebo H, Indahl U, Snipen L, Gjerstad O, et al. (2010) The Response of Enterococcus faecalis V583 to Chloramphenicol Treatment. Int J Microbiol 2010: 483048.
16. Gaca AO, Abranches J, Kajfasz JK, Lemos JA, (2012) Global transcriptional analysis of the stringent response in Enterococcus faecalis. Microbiology 158: 1994-2004.
17. Lopez G, Latorre M, Reyes-Jara A, Cambiazo V, Gonzalez M, (2012) Transcriptomic response of Enterococcus faecalis to iron excess. Biometals 25: 737-747.
18. Solheim M, Aakra A, Vebo H, Snipen L, Nes IF, (2007) Transcriptional responses of Enterococcus faecalis V583 to bovine bile and sodium dodecyl sulfate. Appl Environ Microbiol 73: 5767-5774.
19. Zhang X, Paganelli FL, Bierschenk D, Kuipers A, Bonten MJ, et al. (2012) Genome-wide identification of ampicillin resistance determinants in Enterococcus faecium. PLoS Genet 8: e1002804.
20. Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, et al. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299: 2071-2074.
21. Bourgogne A, Garsin DA, Qin X, Singh KV, Sillanpaa J, et al. (2008) Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol 9: R110.
22. Stone KJ, Strominger JL, (1972) Inhibition of sterol biosynthesis by bacitracin. Proc Natl Acad Sci U S A 69: 1287-1289.
23. Doun SS, Burgner JW 2nd, Briggs SD, Rodwell VW (2005) Enterococcus faecalis phosphomevalonate kinase. Protein Sci 14: 1134-1139.
24. Heuston S, Begley M, Gahan CG, Hill C, (2012) Isoprenoid biosynthesis in bacterial pathogens. Microbiology 158: 1389-1401.
25. Ramarao N, Nielsen-Leroux C, Lereclus D (2012) The Insect Galleria mellonella as a Powerful Infection Model to Investigate Bacterial Pathogenesis. J Vis Exp.
26. de Oliveira NE, Abranches J, Gaca AO, Laport MS, Damaso CR, et al. (2011) clpB, a class III heat-shock gene regulated by CtsR, is involved in thermotolerance and virulence of Enterococcus faecalis. Microbiology 157: 656-665.
27. Rigottier-Gois L, Alberti A, Houel A, Taly JF, Palcy P, et al. (2011) Large-scale screening of a targeted Enterococcus faecalis mutant library identifies envelope fitness factors. PLoS One 6: e29023.
28. 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.
29. Peschel A, Vuong C, Otto M, Gotz F, (2000) The D-alanine residues of Staphylococcus aureus teichoic acids alter the susceptibility to vancomycin and the activity of autolytic enzymes. Antimicrob Agents Chemother 44: 2845-2847.
30. Gutmann L, Al-Obeid S, Billot-Klein D, Ebnet E, Fischer W, (1996) Penicillin tolerance and modification of lipoteichoic acid associated with expression of vancomycin resistance in VanB-type Enterococcus faecium D366. Antimicrob Agents Chemother 40: 257-259.
31. 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.
32. Bizzini A, Zhao C, Auffray Y, Hartke A, (2009) The Enterococcus faecalis superoxide dismutase is essential for its tolerance to vancomycin and penicillin. J Antimicrob Chemother 64: 1196-1202.
33. Liu Y, Imlay JA, (2013) Cell death from antibiotics without the involvement of reactive oxygen species. Science 339: 1210-1213.
34. Keren I, Wu Y, Inocencio J, Mulcahy LR, Lewis K, (2013) Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339: 1213-1216.
35. Cao M, Wang T, Ye R, Helmann JD, (2002) Antibiotics that inhibit cell wall biosynthesis induce expression of the Bacillus subtilis sigma(W) and sigma(M) regulons. Mol Microbiol 45: 1267-1276.
36. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ, et al. (2003) Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149: 2719-2732.
37. Rogers PD, Liu TT, Barker KS, Hilliard GM, English BK, et al. (2007) Gene expression profiling of the response of Streptococcus pneumoniae to penicillin. J Antimicrob Chemother 59: 616-626.
38. Reynolds PE, Courvalin P, (2005) Vancomycin resistance in enterococci due to synthesis of precursors terminating in D-alanyl-D-serine. Antimicrob Agents Chemother 49: 21-25.
39. McCormick NE, Halperin SA, Lee SFm, (2011) Regulation of D-alanylation of lipoteichoic acid in Streptococcus gordonii. Microbiology 157: 2248-2256.
40. Fritsch F, Mauder N, Williams T, Weiser J, Oberle M, et al. (2011) The cell envelope stress response mediated by the LiaFSRLm three-component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaSLm. Microbiology 157: 373-386.
41. Collins B, Guinane CM, Cotter PD, Hill C, Ross RP, (2012) Assessing the contributions of the LiaS histidine kinase to the innate resistance of Listeria monocytogenes to nisin, cephalosporins, and disinfectants. Appl Environ Microbiol 78: 2923-2929.
42. Haas W, Kaushal D, Sublett J, Obert C, Tuomanen EI, (2005) Vancomycin stress response in a sensitive and a tolerant strain of Streptococcus pneumoniae. J Bacteriol 187: 8205-8210.
43. Brunskill EW, Bayles KW, (1996) Identification of LytSR-regulated genes from Staphylococcus aureus. J Bacteriol 178: 5810-5812.
44. Zhang Y, Yang Z, Huang X, Peng J, Fei X, et al. (2008) Cloning, expression, and characterization of a thermostable PAP2L2, a new member of the type-2 phosphatidic acid phosphatase family from Geobacillus toebii T-85. Biosci Biotechnol Biochem 72: 3134-3141.
45. Waggoner DW, Gomez-Munoz A, Dewald J, Brindley DN, (1996) Phosphatidate phosphohydrolase catalyzes the hydrolysis of ceramide 1-phosphate, lysophosphatidate, and sphingosine 1-phosphate. J Biol Chem 271: 16506-16509.
46. Sigal YJ, McDermott MI, Morris AJ, (2005) Integral membrane lipid phosphatases/phosphotransferases: common structure and diverse functions. Biochem J 387: 281-293.
47. Bernard R, El Ghachi M, Mengin-Lecreulx D, Chippaux M, Denizot F, (2005) BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J Biol Chem 280: 28852-28857.
48. Hubscher J, Luthy L, Berger-Bachi B, Stutzmann Meier P, (2008) Phylogenetic distribution and membrane topology of the LytR-CpsA-Psr protein family. BMC Genomics 9: 617.
49. Wen ZT, Baker HV, Burne RA, (2006) Influence of BrpA on critical virulence attributes of Streptococcus mutans. J Bacteriol 188: 2983-2992.
50. Chatfield CH, Koo H, Quivey RG Jr, (2005) The putative autolysin regulator LytR in Streptococcus mutans plays a role in cell division and is growth-phase regulated. Microbiology 151: 625-631.
51. Bitoun JP, Liao S, Yao X, Ahn SJ, Isoda R, et al. (2012) BrpA is involved in regulation of cell envelope stress responses in Streptococcus mutans. Appl Environ Microbiol 78: 2914-2922.
52. Rossi J, Bischoff M, Wada A, Berger-Bachi B, (2003) MsrR, a putative cell envelope-associated element involved in Staphylococcus aureus sarA attenuation. Antimicrob Agents Chemother 47: 2558-2564.
53. Terleckyj B, Willett NP, Shockman GD, (1975) Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun 11: 649-655.
54. Shi L, Reid LH, Jones WD, Shippy R, Warrington JA, et al. (2006) The MicroArray Quality Control (MAQC) project shows inter- and intraplatform reproducibility of gene expression measurements. Nat Biotechnol 24: 1151-1161.
55. Kristich CJ, Chandler JR, Dunny GM, (2007) Development of a host-genotype-independent counterselectable marker and a high-frequency conjugative delivery system and their use in genetic analysis of Enterococcus faecalis. Plasmid 57: 131-144.
56. Leenhout K, Buist G, Bolhuis A, ten Berge A, Kiel J, et al. (1996) A general system for generating unlabelled gene replacements in bacterial chromosomes. Mol Gen Genet 253: 217-224.