Impact of manganese, copper and zinc ions on the transcriptome of the nosocomial pathogen Enterococcus faecalis V583

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Abrantes, Marta Coelho ^a,b   de Fátima Lopes, Maria ^a,c   Kok, Jan ^b  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; COPPER; MANGANESE; TRANSCRIPTOME; ZINC; HEAVY METAL; ION;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA MICROARRAY; ENERGY METABOLISM; ENTEROCOCCUS FAECALIS; GENE EXPRESSION; NONHUMAN; CROSS INFECTION; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MICROBIOLOGY; PHYSIOLOGICAL STRESS;

ENTEROCOCCUS; ENTEROCOCCUS FAECALIS;

COPPER; CROSS INFECTION; ENTEROCOCCUS FAECALIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; IONS; MANGANESE; METALS, HEAVY; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME; ZINC;

EID: 80055051126     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026519     Document Type: Article

References (53)

1. Agranoff DD, Krishna S, (1998) Metal ion homeostasis and intracellular parasitism. Mol Microbiol 28: 403-412.
2. Versieck J, (1985) Trace elements in human body fluids and tissues. Crit Rev Clin Lab Sci 22: 97-184.
3. Powell JJ, Greenfield SM, Thompson RP, (1992) Concentrations of metals in gastric juice in health and peptic ulcer disease. Gut 33: 1617-1620.
4. Chicharro JL, Serrano V, Urena R, Gutierrez AM, Carvajal A, et al. (1999) Trace elements and electrolytes in human resting mixed saliva after exercise. Br J Sports Med 33: 204-207.
5. Milanino R, Marrella M, Gasperini R, Pasqualicchio M, Velo G, (1993) Copper and zinc body levels in inflammation: an overview of the data obtained from animal and human studies. Agents Actions 39: 195-209.
6. Shankar AH, Prasad AS, (1998) Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr 68: 447S-463S.
7. Thurnham DI, Mburu AS, Mwaniki DL, De Wagt A, (2005) Micronutrients in childhood and the influence of subclinical inflammation. Proc Nutr Soc 64: 502-509.
8. Ibs KH, Rink L, (2003) Zinc-altered immune function. J Nutr 133: 1452S-1456S.
9. Jakubovics NS, Jenkinson HF, (2001) Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147: 1709-1718.
10. Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ, (2002) Manganese: elemental defence for a life with oxygen. Trends Microbiol 10: 496-501.
11. Jarvisalo J, Olkinuora M, Kiilunen M, Kivisto H, Ristola P, et al. (1992) Urinary and blood manganese in occupationally nonexposed populations and in manual metal arc welders of mild steel. Int Arch Occup Environ Health 63: 495-501.
12. Solioz M, Abicht HK, Mermod M, Mancini S, (2010) Response of gram-positive bacteria to copper stress. J Biol Inorg Chem 15: 3-14.
13. Sahm DF, Kissinger J, Gilmore MS, Murray PR, Mulder R, et al. (1989) In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis. Antimicrob Agents Chemother 33: 1588-1591.
14. Feldberg RS, Carew JA, Paradise R, (1985) Probing Cu(II)/H2O2 damage in DNA with a damage-specific DNA binding protein. J Free Radic Biol Med 1: 459-466.
15. Singh KV, Coque TM, Weinstock GM, Murray BE, (1998) In vivo testing of an Enterococcus faecalis efaA mutant and use of efaA homologs for species identification. FEMS Immunol Med Microbiol 21: 323-331.
16. Rich RL, Kreikemeyer B, Owens RT, LaBrenz S, Narayana SV, et al. (1999) Ace is a collagen-binding MSCRAMM from Enterococcus faecalis. J Biol Chem 274: 26939-26945.
17. Qin X, Singh KV, Weinstock GM, Murray BE, (2000) Effects of Enterococcus faecalis fsr genes on production of gelatinase and a serine protease and virulence. Infect Immun 68: 2579-2586.
18. Gilmore MS, Segarra RA, Booth MC, Bogie CP, Hall LR, et al. (1994) Genetic-Structure of the Enterococcus-Faecalis Plasmid Pad1-Encoded Cytolytic Toxin System and Its Relationship to Lantibiotic Determinants. Journal of Bacteriology 176: 7335-7344.
19. Hew CM, Korakli M, Vogel RF, (2007) Expression of virulence-related genes by Enterococcus faecalis in response to different environments. Syst Appl Microbiol 30: 257-267.
20. Arnold DL, Jackson RW, Waterfield NR, Mansfield JW, (2007) Evolution of microbial virulence: the benefits of stress. Trends Genet 23: 293-300.
21. 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.
22. 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.
23. 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.
24. Lenz CA, Hew Ferstl CM, Vogel RF, (2010) Sub-lethal stress effects on virulence gene expression in Enterococcus faecalis. Food Microbiol 27: 317-326.
25. Kloosterman TG, Witwicki RM, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP, (2008) Opposite effects of Mn2+ and Zn2+ on PsaR-mediated expression of the virulence genes pcpA, prtA, and psaBCA of Streptococcus pneumoniae. J Bacteriol 190: 5382-5393.
26. Guedon E, Moore CM, Que Q, Wang T, Ye RW, et al. (2003) The global transcriptional response of Bacillus subtilis to manganese involves the MntR, Fur, TnrA and sigmaB regulons. Mol Microbiol 49: 1477-1491.
27. Ward SK, Hoye EA, Talaat AM, (2008) The global responses of Mycobacterium tuberculosis to physiological levels of copper. J Bacteriol 190: 2939-2946.
28. Shafeeq S, Kloosterman TG, Kuipers OP, (2011) Transcriptional response of Streptococcus pneumoniae to Zn(2+) limitation and the repressor/activator function of AdcR. Metallomics 3: 609-618.
29. Shafeeq S, Yesilkaya H, Kloosterman TG, Narayanan G, Andrew PW, et al. (2011) The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Mol Microbiol doi:10.1111/j.1365-2958.2011.07758.x.
30. Solioz M, Stoyanov JV, (2003) Copper homeostasis in Enterococcus hirae. FEMS Microbiol Rev 27: 183-195.
31. Magnani D, Solioz M, (2005) Copper chaperone cycling and degradation in the regulation of the cop operon of Enterococcus hirae. Biometals 18: 407-412.
32. Lubben M, Portmann R, Kock G, Stoll R, Young MM, et al. (2009) Structural model of the CopA copper ATPase of Enterococcus hirae based on chemical cross-linking. Biometals 22: 363-375.
33. Reyes-Jara A, Latorre M, Lopez G, Bourgogne A, Murray BE, et al. (2010) Genome-wide transcriptome analysis of the adaptive response of Enterococcus faecalis to copper exposure. Biometals 23: 1105-1112.
34. Low YL, Jakubovics NS, Flatman JC, Jenkinson HF, Smith AW, (2003) Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis. J Med Microbiol 52: 113-119.
35. Carvalho AS, Silva J, Ho P, Teixeira P, Malcata FX, et al. (2003) Effect of various growth media upon survival during storage of freeze-dried Enterococcus faecalis and Enterococcus durans. J Appl Microbiol 94: 947-952.
36. van Hijum SA, Garcia de la Nava J, Trelles O, Kok J, Kuipers OP, (2003) MicroPreP: a cDNA microarray data pre-processing framework. Appl Bioinformatics 2: 241-244.
37. Kloosterman TG, Hendriksen WT, Bijlsma JJ, Bootsma HJ, van Hijum SA, et al. (2006) Regulation of glutamine and glutamate metabolism by GlnR and GlnA in Streptococcus pneumoniae. J Biol Chem 281: 25097-25109.
38. 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.
39. Larsen R, Buist G, Kuipers OP, Kok J, (2004) ArgR and AhrC are both required for regulation of arginine metabolism in Lactococcus lactis. J Bacteriol 186: 1147-1157.
40. Miller J, eds. (1972) Experiments in Molecular Genetics Cold Spring Harbor, NY. Cold Spring Harbor Press pp. 352-355.
41. 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.
42. Hancock L, Perego M, (2002) Two-component signal transduction in Enterococcus faecalis. J Bacteriol 184: 5819-5825.
43. Patzer SI, Hantke K, (1998) The ZnuABC high-affinity zinc uptake system and its regulator Zur in Escherichia coli. Mol Microbiol 28: 1199-1210.
44. Jakubovics NS, Valentine RA, (2009) A new direction for manganese homeostasis in bacteria: identification of a novel efflux system in Streptococcus pneumoniae. Mol Microbiol 72: 1-4.
45. Kloosterman TG, van der Kooi-Pol MM, Bijlsma JJ, Kuipers OP, (2007) The novel transcriptional regulator SczA mediates protection against Zn2+ stress by activation of the Zn2+-resistance gene czcD in Streptococcus pneumoniae. Mol Microbiol 65: 1049-1063.
46. Grimble RF, (1994) Nutritional antioxidants and the modulation of inflammation: theory and practice. New Horiz 2: 175-185.
47. Eckmann L, Laurent F, Langford TD, Hetsko ML, Smith JR, et al. (2000) Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J Immunol 164: 1478-1487.
48. Galkin A, Kulakova L, Sarikaya E, Lim K, Howard A, et al. (2004) Structural insight into arginine degradation by arginine deiminase, an antibacterial and parasite drug target. J Biol Chem 279: 14001-14008.
49. Moore CM, Helmann JD, (2005) Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8: 188-195.
50. Fabretti F, Theilacker C, Baldassarri L, Kaczynski Z, Kropec A, et al. (2006) Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect Immun 74: 4164-4171.
51. Neuhaus FC, Baddiley J, (2003) A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67: 686-723.
52. Creti R, Fabretti F, Koch S, Huebner J, Garsin DA, et al. (2009) Surface protein EF3314 contributes to virulence properties of Enterococcus faecalis. Int J Artif Organs 32: 611-620.
53. Shankar N, Baghdayan AS, Gilmore MS, (2002) Modulation of virulence within a pathogenicity island in vancomycin-resistant Enterococcus faecalis. Nature 417: 746-750.