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http://dx.doi.org/10.14348/molcells.2014.2238

Direct ROS Scavenging Activity of CueP from Salmonella enterica serovar Typhimurium  

Yoon, Bo-Young (College of Pharmacy and Research Institute for Drug Development, Pusan National University)
Yeom, Ji-Hyun (Department of Life Science, Chung-Ang University)
Kim, Jin-Sik (College of Pharmacy and Research Institute for Drug Development, Pusan National University)
Um, Si-Hyeon (College of Pharmacy and Research Institute for Drug Development, Pusan National University)
Jo, Inseong (College of Pharmacy and Research Institute for Drug Development, Pusan National University)
Lee, Kangseok (Department of Life Science, Chung-Ang University)
Kim, Yong-Hak (Department of Microbiology, Catholic University of Daegu, School of Medicine)
Ha, Nam-Chul (College of Pharmacy and Research Institute for Drug Development, Pusan National University)
Abstract
Salmonella enterica serovar Typhimurium (S. Typhimurium) is an intracellular pathogen that has evolved to survive in the phagosome of macrophages. The periplasmic copper-binding protein CueP was initially known to confer copper resistance to S. Typhimurium. Crystal structure and biochemical studies on CueP revealed a putative copper binding site surrounded by the conserved cysteine and histidine residues. A recent study reported that CueP supplies copper ions to periplasmic Cu,Zn-superoxide dismutase (SodCII) at a low copper concentration and thus enables the sustained SodCII activity in the periplasm. In this study, we investigated the role of CueP in copper resistance at a high copper concentration. We observed that the survival of a cueP-deleted strain of Salmonella in macrophage phagosome was significantly reduced. Subsequent biochemical experiments revealed that CueP specifically mediates the reduction of copper ion using electrons released during the formation of the disulfide bond. We observed that the copper ion-mediated Fenton reaction in the presence of hydrogen peroxide was blocked by CueP. This study provides insight into how CueP confers copper resistance to S. Typhimurium in copper-rich environments such as the phagosome of macrophages.
Keywords
copper resistance; CueP; Fenton reaction; Salmonella;
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1 Eng, J.K., McCormack, A.L., and Yates, J.R. (1995). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom 5, 976-989.
2 Achard, M.E., Stafford, S.L., Bokil, N.J., Chartres, J., Bernhardt, P.V., Schembri, M.A., Sweet, M.J., and McEwan, A.G. (2012). Copper redistribution in murine macrophages in response to Salmonella infection. Biochem. J. 444, 51-57.   DOI   ScienceOn
3 Bae, Y.S., Oh, H., Rhee, S.G., and Yoo, Y.D. (2011). Regulation of reactive oxygen species generation in cell signaling. Mol. Cells 32, 491-509.   DOI   ScienceOn
4 Coburn, B., Grassl, G.A., and Finlay, B.B. (2007). Salmonella, the host and disease: a brief review. Immunol. Cell Biol. 85, 112-118.   DOI   ScienceOn
5 Crichton, R.R., and Pierre, J.L. (2001). Old iron, young copper: from Mars to Venus. Biometals 14, 99-112.   DOI   ScienceOn
6 Datsenko, K.A., and 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.   DOI   ScienceOn
7 Dupont, C.L., Grass, G., and Rensing, C. (2011). Copper toxicity and the origin of bacterial resistance--new insights and applications. Metallomics 3, 1109-1118.   DOI   ScienceOn
8 Ellman, G.L. (1959). Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.   DOI   ScienceOn
9 Espariz, M., Checa, S.K., Audero, M.E., Pontel, L.B., and Soncini, F.C. (2007). Dissecting the Salmonella response to copper. Microbiology 153, 2989-2997.   DOI   ScienceOn
10 Fields, P.I., Swanson, R.V., Haidaris, C.G., and Heffron, F. (1986). Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. USA 83, 5189-5193.   DOI   ScienceOn
11 Franke, S., Grass, G., Rensing, C., and Nies, D.H. (2003). Molecular analysis of the copper-transporting efflux system CusCFBA of Escherichia coli. J. Bacteriol. 185, 3804-3812.   DOI   ScienceOn
12 Grass, G., and Rensing, C. (2001). CueO is a multi-copper oxidase that confers copper tolerance in Escherichia coli. Biochem. Biophys. Res. Commun. 286, 902-908.   DOI   ScienceOn
13 Halliwell, B., and Gutteridge, J.M. (1984). Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219, 1-14.   DOI
14 Hodgkinson, V., and Petris, M.J. (2012). Copper homeostasis at the host-pathogen interface. J. Biol. Chem. 287, 13549-13555.   DOI
15 O'Halloran, T.V., and Culotta, V.C. (2000). Metallochaperones, an intracellular shuttle service for metal ions. J. Biol. Chem. 275, 25057-25060.   DOI   ScienceOn
16 Landt, O., Grunert, H.P., and Hahn, U. (1990). A general method for rapid site-directed mutagenesis using the polymerase chain reaction. Gene 96, 125-128.   DOI   ScienceOn
17 Leary, S.C., and Winge, D.R. (2007). The Janus face of copper: its expanding roles in biology and the pathophysiology of disease. Meeting on Copper and Related Metals in Biology. EMBO Rep. 8, 224-227.
18 Netto, L.E.S., Chae, H.Z., Kang, S.W., Rhee, S.G., and Stadtman, E.R. (1996). Removal of hydrogen peroxide by thiol-specific antioxidant enzyme (TSA) is involved with its antioxidant properties. TSA possesses thiol peroxidase activity. J. Biol. Chem. 271, 15315-15321.   DOI
19 Osman, D., Patterson, C.J., Bailey, K., Fisher, K., Robinson, N.J., Rigby, S.E., and Cavet, J.S. (2013). The copper supply pathway to a Salmonella Cu,Zn-superoxide dismutase (SodCII) involves P(1B)-type ATPase copper efflux and periplasmic CueP. Mol. Microbiol. 87, 466-477.   DOI   ScienceOn
20 Osman, D., and Cavet, J.S. (2008). Copper homeostasis in bacteria. Adv. Appl. Microbiol. 65, 217-247.   DOI   ScienceOn
21 Pontel, L.B., and Soncini, F.C. (2009). Alternative periplasmic copper- resistance mechanisms in Gram negative bacteria. Mol. Microbiol. 73, 212-225.   DOI   ScienceOn
22 Prohaska, J.R., and Lukasewycz, O.A. (1981). Copper deficiency suppresses the immune response of mice. Science 213, 559-561.   DOI
23 White, C., Kambe, T., Fulcher, Y.G., Sachdev, S.W., Bush, A.I., Fritsche, K., Lee, J., Quinn, T.P., and Petris, M.J. (2009a). Copper transport into the secretory pathway is regulated by oxygen in macrophages. J. Cell Sci. 122, 1315-1321.   DOI   ScienceOn
24 Rensing, C., Fan, B., Sharma, R., Mitra, B., and Rosen, B.P. (2000). CopA: An Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 97, 652-656.   DOI   ScienceOn
25 Rigo, A., Corazza, A., di Paolo, M.L., Rossetto, M., Ugolini, R., and Scarpa, M. (2004). Interaction of copper with cysteine: stability of cuprous complexes and catalytic role of cupric ions in anaerobic thiol oxidation. J. Inorg. Biochem. 98, 1495-1501.   DOI   ScienceOn
26 Schaible, U.E., and Kaufmann, S.H. (2004). Iron and microbial infection. Nat. Rev. Microbiol. 2, 946-953.   DOI   ScienceOn
27 White, C., Lee, J., Kambe, T., Fritsche, K., and Petris, M.J. (2009b). A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949-33956.   DOI   ScienceOn
28 Yun, B.Y., Piao, S., Kim, Y.G., Moon, H.R., Choi, E.J., Kim, Y.O., Nam, B.H., Lee, S.J., and Ha, N.C. (2011). Crystallization and preliminary X-ray crystallographic analysis of Salmonella Typhimurium CueP. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 675-677.   DOI   ScienceOn
29 Wolschendorf, F., Ackart, D., Shrestha, T.B., Hascall-Dove, L., Nolan, S., Lamichhane, G., Wang, Y., Bossmann, S.H., Basaraba, R.J., and Niederweis, M. (2011). Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 108, 1621-1626.   DOI   ScienceOn
30 Yamamoto, N., Nakahigashi, K., Nakamichi, T., Yoshino, M., Takai, Y., Touda, Y., Furubayashi, A., Kinjyo, S., Dose, H., Hasegawa, M., et al. (2009). Update on the Keio collection of Escherichia coli single-gene deletion mutants. Mol. Syst. Biol. 5, 335.
31 Czech, M.P., Lawrence, J.C., Jr., and Lynn, W.S. (1974). Evidence for electron transfer reactions involved in the $Ca^{2+}$-dependent thiol activation of fat cell glucose utilization. J. Biol. Chem. 249, 1001-1006.
32 Yoon, B.Y., Kim, Y.H., Kim, N., Yun, B.Y., Kim, J.S., Lee, J.H., Cho, H.S., Lee, K., and Ha, N.C. (2013). Structure of the periplasmic copper-binding protein CueP from Salmonella enterica serovar Typhimurium. Acta Crystallogr. D Biol. Crystallogr. 69, 1867-1875.   DOI   ScienceOn
33 Osman, D., Waldron, K.J., Denton, H., Taylor, C.M., Grant, A.J., Mastroeni, P., Robinson, N.J., and Cavet, J.S. (2010). Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J. Biol. Chem. 285, 25259-25268.   DOI   ScienceOn