A multicopper oxidase (Cj1516) and a CopA homologue (Cj1161) are major components of the copper homeostasis system of Campylobacter jejuni

Journal of Bacteriology

Volumn 190, Issue 24, 2008, Pages 8075-8085

  Hall, Stephen J ^a   Hitchcock, Andrew ^a   Butler, Clive S ^b   Kelly, David J ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CERULOPLASMIN; COPPER; COPPER PROTEIN; MONOPHENOL MONOOXYGENASE; PROTOCATECHUIC ACID;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CAMPYLOBACTER JEJUNI; CJ1516 GENE; ELECTRON SPIN RESONANCE; ENZYME KINETICS; GENE EXPRESSION; HOMEOSTASIS; IRON TRANSPORT; MASS SPECTROMETRY; PRIORITY JOURNAL; WILD TYPE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CERULOPLASMIN; COPPER; DNA, BACTERIAL; ELECTRON SPIN RESONANCE SPECTROSCOPY; GENES, BACTERIAL; MOLECULAR SEQUENCE DATA; MONOPHENOL MONOOXYGENASE; MUTAGENESIS, INSERTIONAL; MUTATION; OXIDATION-REDUCTION; OXIDOREDUCTASES; OXYGEN CONSUMPTION; PERIPLASM; PLASMIDS; SEQUENCE ALIGNMENT; SIDEROPHORES;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI;

EID: 57349087130     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00821-08     Document Type: Article

References (65)

1. Alexandre, G., and I. B. Zhulin. 2000. Laccases are widespread in bacteria. Trends Biotechnol. 18:41-42.
2. Arguello, J. M., E. Eren, and M. Gonzalez-Guerrero. 2007. The structure and function of heavy metal transport P1B-ATPases. Biometals 20:233-248.
3. Askwith, C., D. Eide, A. Van Ho, P. S. Bernard, L. Li, S. Davis-Kaplan, D. M. Sipe, and J. Kaplan. 1994. The FET3 gene of Saccharomyces cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76:403-410.
4. Bayle, D., S. Wangler, T. Weitzenegger, W. Steinhilber, J. Volz, M. Przybylski, K. P. Schafer, G. Sachs, and K. Melchers. 1998. Properties of the P-type ATPases encoded by the copAP operons of Helicobacter pylori and Helicobacter felis. J. Bacteriol. 180:317-329.
5. Bender, C. L., and D. A. Cooksey. 1986. Indigenous plasmids in Pseudomonas syringae pv. tomato: conjugative transfer and role in copper resistance. J. Bacteriol. 165:534-541.
6. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
7. Bendtsen, J. D., H. Nielsen, D. Widdick, T. Palmer, and S. Brunak. 2005. Prediction of twin-arginine signal peptides. BMC Bioinformatics 6:167.
8. Berks, B. C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. 2+ oxidation in Pseudomonas putida GB-1. Appl. Environ. Microbiol. 65:1762-1768.
11. Brown, N. L., S. R. Barrett, J. Camakaris, B. T. Lee, and D. A. Rouch. 1995. Molecular genetics and transport analysis of the copper-resistance determinant (pco) from Escherichia coli plasmid pRJ1004. Mol. Microbiol. 17:1153-1166.
12. Bull, P. C., and D. W. Cox. 1994. Wilson disease and Menkes disease: new handles on heavy-metal transport. Trends Genet. 10:246-252.
13. Carniel, E. 2001. The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect. 3:561-569.
14. Chou, S. P., R. Dular, and S. Kasatiya. 1983. Effect of ferrous sulfate, sodium metabisulfite, and sodium pyruvate on survival of Campylobacter jejuni. J. Clin. Microbiol. 18:986-987.
15. De Silva, D. M., C. C. Askwith, D. Eide, and J. Kaplan. 1995. The FET3 gene product required for high affinity iron transport in yeast is a cell surface ferroxidase. J. Biol. Chem. 270:1098-1101.
16. Dubbels, B. L., A. A. DiSpirito, J. D. Morton, J. D. Semrau, J. N. Neto, and D. A. Bazylinski. 2004. Evidence for a copper-dependent iron transport system in the marine, magnetotactic bacterium strain MV-1. Microbiology 150:2931-2945.
17. Field, L. H., V. L. Headley, S. M. Payne, and L. J. Berry. 1986. Influence of iron on growth, morphology, outer membrane protein composition, and synthesis of siderophores in Campylobacter jejuni. Infect. Immun. 54:126-132.
18. Field, L. H., V. L. Headley, J. L. Underwood, S. M. Payne, and L. J. Berry. 1986. The chicken embryo as a model for Campylobacter invasion: comparative virulence of human isolates of Campylobacter jejuni and Campylobacter coli. Infect. Immun. 54:118-125.
19. Fouts, D. E., E. F. Mongodin, R. E. Mandrell, W. G. Miller, D. A. Rasko, J. Ravel, L. M. Brinkac, R. T. DeBoy, C. T. Parker, S. C. Daugherty, R. J. Dodson, A. S. Durkin, R. Madupu, S. A. Sullivan, J. U. Shetty, M. A. Ayodeji, A. Shvartsbeyn, M. C. Schatz, J. H. Badger, C. M. Fraser, and K. E. Nelson. 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biol. 3:e15.
20. Francis, C. A., K. L. Casciotti, and B. M. Tebo. 2002. Localization of Mn(II)-oxidizing activity and the putative multicopper oxidase, MnxG, to the exosporium of the marine Bacillus sp. strain SG-1. Arch. Microbiol. 178:450-456.
21. Francis, C. A., and B. M. Tebo. 2001. cumA multicopper oxidase genes from diverse Mn(II)-oxidizing and non-Mn(II)-oxidizing Pseudomonas strains. Appl. Environ. Microbiol. 67:4272-4278.
22. Franke, S., G. Grass, C. Rensing, and D. H. Nies. 2003. Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 185:3804-3812.
23. Friedman, C. R., J. Neimann, H. C. Wegener, and R. V. Tauxe. 2000. Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations, p. 121-138. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
24. Grass, G., and C. Rensing. 2001. CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem. Biophys. Res. Commun. 286:902-908.
25. Grass, G., and C. Rensing. 2001. Genes involved in copper homeostasis in Escherichia coli. J. Bacteriol. 183:2145-2147.
26. Harris, Z. L., A. P. Durley, T. K. Man, and J. D. Gitlin. 1999. Targeted gene disruption reveals an essential role for ceruloplasmin in cellular iron efflux. Proc. Natl. Acad. Sci. USA 96:10812-10817.
27. Hofreuter, D., J. Tsai, R. O. Watson, V. Novik, B. Altman, M. Benitez, C. Clark, C. Perbost, T. Jarvie, L. Du, and J. E. Galan. 2006. Unique features of a highly pathogenic Campylobacter jejuni strain. Infect. Immun. 74:4694-4707.
28. Holmes, K., F. Mulholland, B. M. Pearson, C. Pin, J. McNicholl-Kennedy, J. M. Ketley, and J. M. Wells. 2005. Campylobacter jejuni gene expression in response to iron limitation and the role of Fur. Microbiology 151:243-257.
29. Huston, W. M., M. P. Jennings, and A. G. McEwan. 2002. The multicopper oxidase of Pseudomonas aeruginosa is a ferroxidase with a central role in iron acquisition. Mol. Microbiol. 45:1741-1750.
30. Kim, C., W. W. Lorenz, J. T. Hoopes, and J. F. Dean. 2001. Oxidation of phenolate siderophores by the multicopper oxidase encoded by the Escherichia coli yacK gene. J. Bacteriol. 183:4866-4875.
31. (3)-type cytochrome c oxidase. J. Mol. Biol. 297:49-65.
32. Kuper, J., A. Llamas, H. J. Hecht, R. R. Mendel, and G. Schwarz. 2004. Structure of the molybdopterin-bound Cnx1G domain links molybdenum and copper metabolism. Nature 430:803-806.
33. Lee, S. M., G. Grass, C. Rensing, S. R. Barrett, C. J. Yates, J. V. Stoyanov, and N. L. Brown. 2002. The Pco proteins are involved in periplasmic copper handling in Escherichia coli. Biochem. Biophys. Res. Commun. 295:616-620.
34. Melchers, K., T. Weitzenegger, A. Buhmann, W. Steinhilber, G. Sachs, and K. P. Schafer. 1996. Cloning and membrane topology of a P type ATPase from Helicobacter pylori. J. Biol. Chem. 271:446-457.
35. Myers, J. D., and D. J. Kelly. 2005. A sulphite respiration system in the chemoheterotrophic human pathogen Campylobacter jejuni. Microbiology 151:233-242.
36. Naikare, H., K. Palyada, R. Panciera, D. Marlow, and A. Stintzi. 2006. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect. Immun. 74:5433-5444.
37. Odermatt, A., H. Suter, R. Krapf, and M. Solioz. 1993. Primary structure of two P-type ATPases involved in copper homeostasis in Enterococcus hirae. J. Biol. Chem. 268:12775-12779.
38. Outten, F. W., D. L. Huffman, J. A. Hale, and T. V. O'Halloran. 2001. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276:30670-30677.
39. Outten, F. W., C. E. Outten, J. Hale, and T. V. O'Halloran. 2000. Transcriptional activation of an Escherichia coli copper efflux regulon by the chromosomal MerR homologue, cueR. J. Biol. Chem. 275:31024-31029.
40. Parkhill, J., B. W. Wren, K. Mungall, J. M. Ketley, C. Churcher, D. Basham, T. Chillingworth, R. M. Davies, T. Feltwell, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Moule, M. J. Pallen, C. W. Penn, M. A. Quail, M. A. Rajandream, K. M. Rutherford, A. H. van Vliet, S. Whitehead, and B. G. Barrell. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-668.
41. Pesci, E. C., and C. L. Pickett. 1994. Genetic organization and enzymatic activity of a superoxide dismutase from the microaerophilic human pathogen, Helicobacter pylori. Gene 143:111-116.
42. Petersen, C., and L. B. Moller. 2000. Control of copper homeostasis in Escherichia coli by a P-type ATPase, CopA, and a MerR-like transcriptional activator, CopR. Gene 261:289-298.
43. Pickett, C. L., T. Auffenberg, E. C. Pesci, V. L. Sheen, and S. S. Jusuf. 1992. Iron acquisition and hemolysin production by Campylobacter jejuni. Infect. Immun. 60:3872-3877.
44. 3 oxidases. Biochim. Biophys. Acta 1655:388-399.
45. Pittman, M. S., K. T. Elvers, L. Lee, M. A. Jones, R. K. Poole, S. F. Park, and D. J. Kelly. 2007. Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 63:575-590.
46. Portmann, R., D. Magnani, J. V. Stoyanov, A. Schmechel, G. Multhaup, and M. Solioz. 2004. Interaction kinetics of the copper-responsive CopY repressor with the cop promoter of Enterococcus hirae. J. Biol. Inorg. Chem. 9:396-402.
47. Raphael, B. H., and L. A. Joens. 2003. FeoB is not required for ferrous iron uptake in Campylobacter jejuni. Can. J. Microbiol. 49:727-731.
48. Rensing, C., B. Fan, R. Sharma, B. Mitra, and B. P. Rosen. 2000. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 97:652-656.
49. Rensing, C., and G. Grass. 2003. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 27:197-213.
50. Roberts, S. A., A. Weichsel, G. Grass, K. Thakali, J. T. Hazzard, G. Tollin, C. Rensing, and W. R. Montfort. 2002. Crystal structure and electron transfer kinetics of CueO, a multicopper oxidase required for copper homeostasis in Escherichia coli. Proc. Natl. Acad. Sci. USA 99:2766-2771.
51. Roberts, S. A., G. F. Wildner, G. Grass, A. Weichsel, A. Ambrus, C. Rensing, and W. R. Montfort. 2003. A labile regulatory copper ion lies near the T1 copper site in the multicopper oxidase CueO. J. Biol. Chem. 278:31958-31963.
52. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
53. Sellars, M. J., S. J. Hall, and D. J. Kelly. 2002. Growth of Campylobacter jejuni supported by respiration of fumarate, nitrate, nitrite, trimethylamine-N-oxide, or dimethyl sulfoxide requires oxygen. J. Bacteriol. 184:4187-4196.
54. Singh, S. K., G. Grass, C. Rensing, and W. R. Montfort. 2004. Cuprous oxidase activity of CueO from Escherichia coli. J. Bacteriol. 186:7815-7817.
55. Skirrow, M. B., and M. J. Blaser. 2000. Clinical aspects of Campylobacter infection, p. 69-88. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, DC.
56. Solioz, M., and J. V. Stoyanov. 2003. Copper homeostasis in Enterococcus hirae. FEMS Microbiol. Rev. 27:183-195.
57. Solioz, M., and C. Vulpe. 1996. CPx-type ATPases: a class of P-type ATPases that pump heavy metals. Trends Biochem. Sci. 21:237-241.
58. Solomon, E. I., U. M. Sundaram, and T. E. Machonkin. 1996. Multicopper oxidases and oxygenases. Chem. Rev. 96:2563-2606.
59. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
60. Stoyanov, J. V., J. L. Hobman, and N. L. Brown. 2001. CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Mol. Microbiol. 39:502-511.
61. Stoyanov, J. V., D. Magnani, and M. Solioz. 2003. Measurement of cytoplasmic copper, silver, and gold with a lux biosensor shows copper and silver, but not gold, efflux by the CopA ATPase of Escherichia coli. FEBS Lett. 546:391-394.
62. Tsai, K. J., Y. F. Lin, M. D. Wong, H. H. Yang, H. L. Fu, and B. P. Rosen. 2002. Membrane topology of the p1258 CadA Cd(II)/Pb(II)/Zn(II)- translocating P-type ATPase. J. Bioenerg. Biomembr. 34:147-156.
63. van Vliet, A. H., J. M. Ketley, S. F. Park, and C. W. Penn. 2002. The role of iron in Campylobacter gene regulation, metabolism and oxidative stress defense. FEMS Microbiol. Rev. 26:173-186.
64. van Vliet, A. H., K. G. Wooldridge, and J. M. Ketley. 1998. Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J. Bacteriol. 180:5291-5298.
65. Yamamoto, K., and A. Ishihama. 2006. Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli. Biosci. Biotechnol. Biochem. 70:1688-1695.