Alternative periplasmic copper-resistance mechanisms in Gram negative bacteria

Molecular Microbiology

Volumn 73, Issue 2, 2009, Pages 212-225

  Pontel, Lucas B ^a   Soncini, Fernando C ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIAL PROTEIN; CADMIUM; CHLORAMPHENICOL; COBALT; COPPER; COPPER SULFATE; CUEP PROTEIN; DNA FRAGMENT; GOLD; HYBRID PROTEIN; IRON; KANAMYCIN; METAL ION; OXYGEN; RNA; RNA POLYMERASE; SIGNAL PEPTIDE; SILVER; UNCLASSIFIED DRUG; ZINC;

AMINO ACID SEQUENCE; ANAEROBIC GROWTH; ARTICLE; BACTERIUM CULTURE; CELLULAR DISTRIBUTION; CITROBACTER KOSERI; CYTOSOL; DNA SEQUENCE; ESCHERICHIA COLI; GRAM NEGATIVE BACTERIUM; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; OPERON; PECTOBACTERIUM CAROTOVORUM; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA INTERACTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; REGULON; SALMONELLA; WESTERN BLOTTING; YERSINIA;

AMINO ACID SEQUENCE; ANAEROBIOSIS; BACTERIAL PROTEINS; COPPER; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; PERIPLASM; REGULON; RNA, BACTERIAL; SALMONELLA TYPHIMURIUM;

ESCHERICHIA COLI; NEGIBACTERIA; SALMONELLA;

EID: 67650436140     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06763.x     Document Type: Article

References (58)

1. Adaikkalam, V. Swarup, S. (2002) Molecular characterization of an operon, cueAR, encoding a putative P1-type ATPase and a MerR-type regulatory protein involved in copper homeostasis in Pseudomonas putida. Microbiology 148 : 2857 2867. (Pubitemid 35050197)
2. Aguirre, A., Cabeza, M.L., Spinelli, S.V., McClelland, M., García Véscovi, E. Soncini, F.C. (2006) PhoP-induced genes within Salmonella pathogenicity island 1. J Bacteriol 188 : 6889 6898. (Pubitemid 44497902)
3. Bachamann, B.J. (1996) Derivations and genotypes of some mutant derivatives of E. coli K12. In Escherichia coli and Salmonella typhimurium. Neidhart, F.C. (ed.). Washington, DC : American Society for Microbiology, pp. 2460 2488.
4. Bagai, I., Liu, W., Rensing, C., Blackburn, N.J. McEvoy, M.M. (2007) Substrate-linked conformational change in the periplasmic component of a Cu(I)/Ag(I) efflux system. J Biol Chem 282 : 35695 35702. (Pubitemid 350277135)
5. Bagai, I., Rensing, C., Blackburn, N.J. McEvoy, M.M. (2008) Direct metal transfer between periplasmic proteins identifies a bacterial copper chaperone. Biochemistry 47 : 11408 11414.
6. Bailey, T.L. Elkan, C. (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3 : 21 29.
7. Bailey, T.L. Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14 : 48 54. (Pubitemid 28395676)
8. Barchiesi, J., Castelli, M.E., Soncini, F.C. García Véscovi, E. (2008) mgtA Expression is induced by rob overexpression and mediates a Salmonella enterica resistance phenotype. J Bacteriol 190 : 4951 4958. (Pubitemid 351991063)
9. Bendtsen, J.D., Nielsen, H., von Heijne, G. Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 : 783 795. (Pubitemid 38829638)
10. Beswick, P.H., Hall, G.H., Hook, A.J., Little, K., McBrien, D.C. Lott, K.A. (1976) Copper toxicity: evidence for the conversion of cupric to cuprous copper in vivo under anaerobic conditions. Chem Biol Interact 14 : 347 356.
11. + for all three chromosomally located systems of DNA restriction and modification. J Bacteriol 156 : 471 474.
12. 2+-sensor in the recognition of its partner PhoP. J Biol Chem 278 : 23579 23585. (Pubitemid 36830178)
13. 2+ regulation of the sensor protein PhoQ in Salmonella. J Biol Chem 275 : 22948 22954. (Pubitemid 30646182)
14. Changela, A., Chen, K., Xue, Y., Holschen, J., Outten, C.E., O'Halloran, T.V. Mondragon, A. (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR. Science 301 : 1383 1387. (Pubitemid 37075815)
15. Checa, S.K., Espariz, M., Audero, M.E., Botta, P.E., Spinelli, S.V. Soncini, F.C. (2007) Bacterial sensing of and resistance to gold salts. Mol Microbiol 63 : 1307 1318. (Pubitemid 46257161)
16. R cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 : 9 14.
17. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645. (Pubitemid 30412767)
18. Davis, A.V. O'Halloran, T.V. (2008) A place for thioether chemistry in cellular copper ion recognition and trafficking. Nat Chem Biol 4 : 148 151. (Pubitemid 351265328)
19. Ellermeier, C.D., Janakiraman, A. Slauch, J.M. (2002) Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290 : 153 161. (Pubitemid 34615918)
20. Espariz, M., Checa, S.K., Audero, M.E., Pontel, L.B. Soncini, F.C. (2007) Dissecting the Salmonella response to copper. Microbiology 153 : 2989 2997. (Pubitemid 47517060)
21. Franke, S., Grass, G. Nies, D.H. (2001) The product of the ybdE gene of the Escherichia coli chromosome is involved in detoxification of silver ions. Microbiology 147 : 965 972. (Pubitemid 32401336)
22. Franke, S., Grass, G., Rensing, C. Nies, D.H. (2003) Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J Bacteriol 185 : 3804 3812. (Pubitemid 36735931)
23. + to transmembrane transport sites. Proc Natl Acad Sci USA 105 : 5992 5997. (Pubitemid 351758387)
24. Grass, G. Rensing, C. (2001a) Genes involved in copper homeostasis in Escherichia coli. J Bacteriol 183 : 2145 2147. (Pubitemid 32226015)
25. Grass, G. Rensing, C. (2001b) CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem Biophys Res Commun 286 : 902 908. (Pubitemid 32924857)
26. Gupta, A., Matsui, K., Lo, J.F. Silver, S. (1999) Molecular basis for resistance to silver cations in Salmonella. Nat Med 5 : 183 188. (Pubitemid 29068525)
27. Hakemian, A.S., Kondapalli, K.C., Telser, J., Hoffman, B.M., Stemmler, T.L. Rosenzweig, A.C. (2008) The metal centers of particulate methane monooxygenase from Methylosinus trichosporium OB3b. Biochemistry 47 : 6793 6801. (Pubitemid 351898934)
28. Hiniker, A., Collet, J.F. Bardwell, J.C. (2005) Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC. J Biol Chem 280 : 33785 33791. (Pubitemid 41443097)
29. Hussain, F., Olson, J.S. Wittung-Stafshede, P. (2008) Conserved residues modulate copper release in human copper chaperone Atox1. Proc Natl Acad Sci USA 105 : 11158 11163.
30. Karlsen, O.A., Lillehaug, J.R. Jensen, H.B. (2008) The presence of multiple c-type cytochromes at the surface of the methanotrophic bacterium Methylococcus capsulatus (Bath) is regulated by copper. Mol Microbiol 70 : 15 26.
31. 2+- responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol 185 : 6287 6294. (Pubitemid 37305528)
32. Lejona, S., Castelli, M.E., Cabeza, M.L., Kenney, L.J., García Véscovi, E. Soncini, F.C. (2004) PhoP can activate its target genes in a PhoQ-independent manner. J Bacteriol 186 : 2476 2480. (Pubitemid 38451851)
33. Lim, S.Y., Joe, M.H., Song, S.S., Lee, M.H., Foster, J.W., Park, Y.K., et al. (2002) CuiD is a crucial gene for survival at high copper environment in Salmonella enterica serovar Typhimurium. Mol Cells 14 : 177 184. (Pubitemid 41594970)
34. Macomber, L., Rensing, C. Imlay, J.A. (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 189 : 1616 1626. (Pubitemid 46446123)
35. MacPherson, I.S. Murphy, M.E. (2007) Type-2 copper-containing enzymes. Cell Mol Life Sci 64 : 2887 2899. (Pubitemid 351152251)
36. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
37. Munson, G.P., Lam, D.L., Outten, F.W. O'Halloran, T.V. (2000) Identification of a copper-responsive two-component system on the chromosome of Escherichia coli K-12. J Bacteriol 182 : 5864 5871. (Pubitemid 30746535)
38. Narindrasorasak, S., Kulkarni, P., Deschamps, P., She, Y.M. Sarkar, B. (2007) Characterization and copper binding properties of human COMMD1 (MURR1). Biochemistry 46 : 3116 3128. (Pubitemid 46449134)
39. Neu, H.C. Heppel, L.A. (1964) The release of ribonuclease into the medium when Escherichia coli cells are converted to speroplasts. J Biol Chem 239 : 3893 3900.
40. Neu, H.C. Heppel, L.A. (1965) The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J Biol Chem 240 : 3685 3692.
41. Osman, D. Cavet, J.S. (2008) Copper homeostasis in bacteria. Adv Appl Microbiol 65 : 217 247.
42. Outten, F.W., Outten, C.E., Hale, J. O'Halloran, T.V. (2000) Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue. Cuer J Biol Chem 275 : 31024 31029. (Pubitemid 30757760)
43. Outten, F.W., Huffman, D.L., Hale, J.A. O'Halloran, T.V. (2001) The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J Biol Chem 276 : 30670 30677.
44. Pontel, L.B., Audero, M.E., Espariz, M., Checa, S.K. Soncini, F.C. (2007) GolS controls the response to gold by the hierarchical induction of Salmonella-specific genes that include a CBA efflux-coding operon. Mol Microbiol 66 : 814 825. (Pubitemid 47621865)
45. 0 reductase in Pseudomonas putida KT2440. J Bacteriol 189 : 5361 5371. (Pubitemid 47076081)
46. Rensing, C., Fan, B., Sharma, R., Mitra, B. Rosen, B.P. (2000) CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proc Natl Acad Sci USA 97 : 652 656. (Pubitemid 30070364)
47. Ridge, P.G., Zhang, Y. Gladyshev, V.N. (2008) Comparative genomic analyses of copper transporters and cuproproteomes reveal evolutionary dynamics of copper utilization and its link to oxygen. PLoS ONE 3 : e1378.
48. von Rozycki, T. Nies, D.H. (2008) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Antonie Van Leeuwenhoek doi: 10.1007/s10482-008- 9284-5
49. Singh, S.K., Grass, G., Rensing, C. Montfort, W.R. (2004) Cuprous oxidase activity of CueO from Escherichia coli. J Bacteriol 186 : 7815 7817. (Pubitemid 39463750)
50. Soncini, F.C., García Véscovi, E. Groisman, E.A. (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177 : 4364 4371.
51. Stoyanov, J.V. Brown, N.L. (2003) The Escherichia coli copper-responsive copA promoter is activated by gold. J Biol Chem 278 : 1407 1410. (Pubitemid 36801364)
52. Stoyanov, J.V., Hobman, J.L. Brown, N.L. (2001) CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol Microbiol 39 : 502 511. (Pubitemid 32113519)
53. Thieme, D., Neubauer, P., Nies, D.H. Grass, G. (2008) Sandwich hybridization assay for sensitive detection of dynamic changes in mRNA transcript levels in crude Escherichia coli cell extracts in response to copper ions. Appl Environ Microbiol 74 : 7463 7470.
54. Uzzau, S., Figueroa-Bossi, N., Rubino, S. Bossi, L. (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA 98 : 15264 15269. (Pubitemid 34014003)
55. Waldron, K.J. Robinson, N.J. (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7 : 25 35.
56. Waldron, K.J., Tottey, S., Yanagisawa, S., Dennison, C. Robinson, N.J. (2007) A periplasmic iron-binding protein contributes toward inward copper supply. J Biol Chem 282 : 3837 3846. (Pubitemid 47084464)
57. Wiethaus, J., Wildner, G.F. Masepohl, B. (2006) The multicopper oxidase CutO confers copper tolerance to Rhodobacter capsulatus. FEMS Microbiol Lett 256 : 67 74.
58. Zhang, X.X. Rainey, P.B. (2008) Regulation of copper homeostasis in Pseudomonas fluorescens SBW25. Environ Microbiol 10 : 3284 3294.