Comparison of OG1RF and an isogenic fsrB deletion mutant by transcriptional analysis: The Fsr system of Enterococcus faecalis is more than the activator of gelatinase and serine protease

Journal of Bacteriology

Volumn 188, Issue 8, 2006, Pages 2875-2884

  Bourgogne, Agathe ^a   Hilsenbeck, Susan G ^b   Dunny, Gary M ^c   Murray, Barbara E ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; ENZYME ACTIVATOR; FSR PROTEIN; GELATINASE; GELE PROTEIN; MEMBRANE PROTEIN; REGULATOR PROTEIN; SERINE PROTEINASE; SPRE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BIOFILM; DELETION MUTANT; ENTEROCOCCUA FAECALIS TX5266; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECALIS OG1RF; ENTEROCOCCUS FAECALIS V583; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; EUT PDU GENE; FSR SYSTEM; FSRB GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GROWTH CURVE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; QUORUM SENSING; REGULON; TRANSCRIPTIONAL PROFILING;

BACTERIAL PROTEINS; BIOFILMS; ENTEROCOCCUS FAECALIS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; MEMBRANE PROTEINS; METABOLISM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, BACTERIAL; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS;

EID: 33646011978     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.8.2875-2884.2006     Document Type: Article

References (54)

1. Aakra, A., H. Vebo, L. Snipen, H. Hirt, A. Aastveit, V. Kapur, G. Dunny, B. Murray, and I. F. Nes. 2005. Transcriptional response of Enterococcus faecalis V583 to erythromycin. Antimicrob. Agents Chemother. 49:2246-2259.
2. Aitchison, E. J., P. A. Lambert, and I. D. Farrell. 1986. Antigenic composition of an endocarditis-associated isolate of Streptococcus faecalis and identification of its glycoprotein antigens by ligand blotting with lectins. J. Med. Microbiol. 21:161-167.
3. Bischoff, M., P. Dunman, J. Kormanec, D. Macapagal, E. Murphy, W. Mounts, B. Berger-Bachi, and S. Projan. 2004. Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J. Bacteriol. 186:4085-4099.
4. Bourgogne, A., M. Drysdale, S. G. Hilsenbeck, S. N. Peterson, and T. M. Koehler. 2003. Global effects of virulence gene regulators in a Bacillus anthracis strain with both virulence plasmids. Infect. Immun. 71:2736-2743.
5. Brinsmade, S. R., T. Paldon, and J. C. Escalante-Semerena. 2005. Minimal functions and physiological conditions required for growth of Salmonella enterica on ethanolamine in the absence of the metabolosome. J. Bacteriol. 187:8039-8046.
6. Bronner, S., H. Monteil, and G. Prevost. 2004. Regulation of virulence determinants in Staphylococcus aureus: complexity and applications. FEMS Microbiol. Rev. 28:183-200.
7. Clewell, D. B., and G. M. Dunny. 2002. The Enterococci: pathogenesis, molecular biology, and antibiotic resistance. ASM Press, Washington, D.C.
8. Coburn, P. S., C. M. Pillar, B. D. Jett, W. Haas, and M. S. Gilmore. 2004. Enterococcus faecalis senses target cells and in response expresses cytolysin. Science 306:2270-2272.
9. Comenge, Y., R. Quintiliani, Jr., L. Li, L. Dubost, J. P. Brouard, J. E. Hugonnet, and M. Arthur. 2003. The CroRS two-component regulatory system is required for intrinsic beta-lactam resistance in Enterococcus faecalis. J. Bacteriol. 185:7184-7192.
10. Cruz-Ramos, H., G. M. Cook, G. Wu, M. W. Cleeter, and R. K. Poole. 2004. Membrane topology and mutational analysis of Escherichia coli CydDC, an ABC-type cysteine exporter required for cytochrome assembly. Microbiology 150:3415-3427.
11. Depardieu, F., B. Perichon, and P. Courvalin. 2004. Detection of the van alphabet and identification of enterococci and staphylococci at the species level by multiplex PCR. J. Clin. Microbiol. 42:5857-5860.
12. Deziel, E., S. Gopalan, A. P. Tampakaki, F. Lepine, K. E. Padfield, M. Saucier, G. Xiao, and L. G. Rahme. 2005. The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. Mol. Microbiol. 55:998-1014.
13. Dunman, P. M., E. Murphy, S. Haney, D. Palacios, G. Tucker-Kellogg, S. Wu, E. L. Brown, R. J. Zagursky, D. Shlaes, and S. J. Projan. 2001. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183:7341-7353.
14. Engelbert, M., E. Mylonakis, F. M. Ausubel, S. B. Calderwood, and M. S. Gilmore. 2004. Contribution of gelatinase, serine protease, and fsr to the pathogenesis of Enterococcus faecalis endophthalmitis. Infect. Immun. 72:3628-3633.
15. Garsin, D. A., J. Urbach, J. C. Huguet-Tapia, J. E. Peters, and F. M. Ausubel. 2004. Construction of an Enterococcus faecalis Tn917-mediated-gene- disruption library offers insight into Tn917 insertion patterns. J. Bacteriol. 186:7280-7289.
16. Haas, W., B. D. Shepard, and M. S. Gilmore. 2002. Two-component regulator of Enterococcus faecalis cytolysin responds to quorum-sensing autoinduction. Nature 415:84-87.
17. Hancock, L., and M. Perego. 2002. Two-component signal transduction in Enterococcus faecalis. J. Bacteriol. 184:5819-5825.
18. Hancock, L. E., and M. Perego. 2004. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J. Bacteriol. 186:5629-5639.
19. Hancock, L. E., and M. Perego. 2004. Systematic inactivation and phenotypic characterization of two-component signal transduction systems of Enterococcus faecalis V583. J. Bacteriol. 186:7951-7958.
20. Hufnagel, M., S. Koch, R. Creti, L. Baldassarri, and J. Huebner. 2004. A putative sugar-binding transcriptional regulator in a novel gene locus in Enterococcus faecalis contributes to production of biofilm and prolonged bacteremia in mice. J. Infect. Dis. 189:420-430.
21. Jha, A. K., H. P. Bais, and J. M. Vivanco. 2005. Enterococcus faecalis mammalian virulence-related factors exhibit potent pathogenicity in the Arabidopsis thaliana plant model. Infect. Immun. 73:464-475.
22. Kawalec, M., J. Potempa, J. L. Moon, J. Travis, and B. E. Murray. 2005. Molecular diversity of a putative virulence factor: purification and characterization of isoforms of an extracellular serine glutamyl endopeptidase of Enterococcus faecalis with different enzymatic activities. J. Bacteriol. 187:266-275.
23. Korem, M., Y. Gov, M. D. Kiran, and N. Balaban. 2005. Transcriptional profiling of target of RNAIII-activating protein, a master regulator of staphylococcal virulence. Infect. Immun. 73:6220-6228.
24. Le Breton, Y., V. Pichereau, N. Sauvageot, Y. Auffray, and A. Rince. 2005. Maltose utilization in Enterococcus faecalis. J. Appl. Microbiol. 98:806-813.
25. Low, Y. L., N. S. Jakubovics, J. C. Flatman, H. F. Jenkinson, and A. W. Smith. 2003. Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis. J. Med. Microbiol. 52:113-119.
26. Lowe, A. M., P. A. Lambert, and A. W. Smith. 1995. Cloning of an Enterococcus faecalis endocarditis antigen: homology with adhesins from some oral streptococci. Infect. Immun. 63:703-706.
27. Mohamed, J. A., W. Huang, S. R. Nallapareddy, F. Teng, and B. E. Murray. 2004. Influence of origin of isolates, especially endocarditis isolates, and various genes on biofilm formation by Enterococcus faecalis. Infect. Immun. 72:3658-3663.
28. Murray, B. E., K. V. Singh, R. P. Ross, J. D. Heath, G. M. Dunny, and G. M. Weinstock. 1993. Generation of restriction map of Enterococcus faecalis OG1 and investigation of growth requirements and regions encoding biosynthetic function. J. Bacteriol. 175:5216-5223.
29. Mylonakis, E., M. Engelbert, X. Qin, C. D. Sifri, B. E. Murray, F. M. Ausubel, M. S. Gilmore, and S. B. Calderwood. 2002. The Enterococcus faecalis fsrB gene, a key component of the fsr quorum-sensing system, is associated with virulence in the rabbit endophthalmitis model. Infect. Immun. 70:4678-4681.
30. Nakayama, J., Y. Cao, T. Horii, S. Sakuda, A. D. Akkermans, W. M. de Vos, and H. Nagasawa. 2001. Gelatinase biosynthesis-activating pheromone: a peptide lactone that mediates a quorum sensing in Enterococcus faecalis. Mol. Microbiol. 41:145-154.
31. Nakayama, J., Y. Cao, T. Horii, S. Sakuda, and H. Nagasawa. 2001. Chemical synthesis and biological activity of the gelatinase biosynthesis-activating pheromone of Enterococcus faecalis and its analogs. Biosci. Biotechnol. Biochem. 65:2322-2325.
32. Nakayama, J., R. Kariyama, and H. Kumon. 2002. Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine. Appl. Environ. Microbiol. 68:3152-3155.
33. Paulsen, I. T., L. Banerjei, G. S. Myers, K. E. Nelson, R. Seshadri, T. D. Read, D. E. Fouts, J. A. Eisen, S. R. Gill, J. F. Heidelberg, H. Tettelin, R. J. Dodson, L. Umayam, L. Brinkac, M. Beanan, S. Daugherty, R. T. DeBoy, S. Durkin, J. Kolonay, R. Madupu, W. Nelson, J. Vamathevan, B. Tran, J. Upton, T. Hansen, J. Shetty, H. Khouri, T. Utterback, D. Radune, K. A. Ketchum, B. A. Dougherty, and C. M. Fraser. 2003. Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299:2071-2074.
34. Qin, X., K. V. Singh, G. M. Weinstock, and B. E. Murray. 2000. Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect. Immun. 68:2579-2586.
35. Qin, X., K. V. Singh, G. M. Weinstock, and B. E. Murray. 2001. Characterization of fsr, a regulator controlling expression of gelatinase and serine protease in Enterococcus faecalis OG1RF. J. Bacteriol. 183:3372-3382.
36. fm, predominates in Enterococcus faecium of clinical origin. J. Infect. Dis. 187:508-512.
37. Roberts, J. C., K. V. Singh, P. C. Okhuysen, and B. E. Murray. 2004. Molecular epidemiology of the fsr locus and of gelatinase production among different subsets of Enterococcus faecalis isolates. J. Clin. Microbiol. 42:2317-2320.
38. Roof, D. M., and J. R. Roth. 1992. Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J. Bacteriol. 174:6634-6643.
39. Rosinha, G. M., D. A. Freitas, A. Miyoshi, V. Azevedo, E. Campos, S. L. Cravero, O. Rossetti, G. Splitter, and S. C. Oliveira. 2002. Identification and characterization of a Brucella abortus ATP-binding cassette transporter homolog to Rhizobium meliloti ExsA and its role in virulence and protection in mice. Infect. Immun. 70:5036-5044.
40. Said-Salim, B., P. M. Dunman, F. M. McAleese, D. Macapagal, E. Murphy, P. J. McNamara, S. Arvidson, T. J. Foster, S. J. Projan, and B. N. Kreiswirth. 2003. Global regulation of Staphylococcus aureus genes by Rot. J. Bacteriol. 185:610-619.
41. Sapolsky, R. 2005. Presented at the 13th International Conference on Bacilli, San Diego, California.
42. Sheppard, D. E., J. T. Penrod, T. Bobik, E. Kofoid, and J. R. Roth. 2004. Evidence that a B12-adenosyl transferase is encoded within the ethanolamine operon of Salmonella enterica. J. Bacteriol. 186:7635-7644.
43. Sifri, C. D., E. Mylonakis, K. V. Singh, X. Qin, D. A. Garsin, B. E. Murray, F. M. Ausubel, and S. B. Calderwood. 2002. Virulence effect of Enterococcus faecalis protease genes and the quorum-sensing locus fsr in Caenorhabditis elegans and mice. Infect. Immun. 70:5647-5650.
44. Singh, K. V., S. R. Nallapareddy, E. C. Nannini, and B. E. Murray. 2005. Fsr-independent production of protease(s) may explain the lack of attenuation of an Enterococcus faecalis fsr mutant versus a gelE-sprE mutant in induction of endocarditis. Infect. Immun. 73:4888-4894.
45. Sturme, M. H., J. Nakayama, D. Molenaar, Y. Murakami, R. Kunugi, T. Fujii, E. E. Vaughan, M. Kleerebezem, and W. M. de Vos. 2005. An agr-like two-component regulatory system in Lactobacillus plantarum is involved in production of a novel cyclic peptide and regulation of adherence. J. Bacteriol. 187:5224-5235.
46. Teng, F., L. Wang, K. V. Singh, B. E. Murray, and G. M. Weinstock. 2002. Involvement of PhoP-PhoS homologs in Enterococcus faecalis virulence. Infect. Immun. 70:1991-1996.
47. Verneuil, N., M. Sanguinetti, Y. Le Breton, B. Posteraro, G. Fadda, Y. Auffray, A. Hartke, and J. C. Giard. 2004. Effects of the Enterococcus faecalis hypR gene encoding a new transcriptional regulator on oxidative stress response and intracellular survival within macrophages. Infect. Immun. 72:4424-4431.
48. Waters, C. M., M. H. Antiporta, B. E. Murray, and G. M. Dunny. 2003. Role of the Enterococcus faecalis GelE protease in determination of cellular chain length, supernatant pheromone levels, and degradation of fibrin and misfolded surface proteins. J. Bacteriol. 185:3613-3623.
49. Way, S. S., A. C. Borczuk, and M. B. Goldberg. 1999. Adaptive immune response to Shigella flexneri 2a cydC in immunocompetent mice and mice lacking immunoglobulin A. Infect. Immun. 67:2001-2004.
50. Way, S. S., S. Sallustio, R. S. Magliozzo, and M. B. Goldberg. 1999. Impact of either elevated or decreased levels of cytochrome bd expression on Shigella flexneri virulence. J. Bacteriol. 181:1229-1237.
51. White, D. A. 1973. Phospholipid composition of mammalian tissues. Elsevier Scientific Publishing Company, New York, N.Y.
52. Winstedt, L., K. Yoshida, Y. Fujita, and C. von Wachenfeldt. 1998. Cytochrome bd biosynthesis in Bacillus subtilis: characterization of the cydABCD operon. J. Bacteriol. 180:6571-6580.
53. Xu, Y., J. M. Rivas, E. L. Brown, X. Liang, and M. Hook. 2004. Virulence potential of the staphylococcal adhesin CNA in experimental arthritis is determined by its affinity for collagen. J. Infect. Dis. 189:2323-2333.
54. Zeng, J., F. Teng, and B. E. Murray. 2005. Gelatinase is important for translocation of Enterococcus faecalis across polarized human enterocyte-like T84 cells. Infect. Immun. 73:1606-1612.