The role of copper and zinc toxicity in innate immune defense against bacterial pathogens

Journal of Biological Chemistry

Volumn 290, Issue 31, 2015, Pages 1854-1861

  Djoko, Karrera Y ^a   Y Ong, Cheryl Lynn ^a   Walker, Mark J ^a   McEwan, Alastair G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DETOXIFICATION; ZINC;

ANIMAL MODEL; BACTERIAL INFECTIONS; BACTERIAL PATHOGENS; COPPER AND ZINC; INNATE IMMUNES; INTRACELLULAR SURVIVAL;

COPPER;

COPPER EXPORTING ADENOSINE TRIPHOSPHATASE; COPPER ION; TRACE ELEMENT; WILSON DISEASE PROTEIN; ZINC ION; COPPER; ZINC;

ARTICLE; BACTERIAL CLEARANCE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; ESCHERICHIA COLI; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; INFECTION CONTROL; INNATE IMMUNITY; INTRACELLULAR SPACE; LISTERIA MONOCYTOGENES; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; ANIMAL; BACTERIAL INFECTION; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BACTERIAL INFECTIONS; BIOLOGICAL TRANSPORT; COPPER; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; ZINC;

EID: 84964696571     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.647099     Document Type: Article

References (99)

1. Flo, T. H., Smith, K. D., Sato, S., Rodriguez, D. J., Holmes, M. A., Strong, R. K., Akira, S., and Aderem, A. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917-921
2. Kehl-Fie, T. E., and Skaar, E. P. (2010) Nutritional immunity beyond iron: A role for manganese and zinc. Curr. Opin. Chem. Biol. 14, 218-224
3. Dunlap, W. M., James, G. W., 3rd, and Hume, D. M. (1974) Anemia and neutropenia caused by copper deficiency. Ann. Int. Med. 80, 470-476
4. Zidar, B. L., Shadduck, R. K., Zeigler, Z., and Winkelstein, A. (1977) Observations on the anemia and neutropenia of human copper deficiency. Am. J. Hematol. 3, 177-185
5. Percival, S. S. (1995) Neutropenia caused by copper deficiency: Possible mechanisms of action. Nutr. Rev. 53, 59-66
6. Heresi, G., Castillo-Durán, C., Mun?oz, C., Arévalo, M., and Schlesinger, L. (1985) Phagocytosis and immunoglobulin levels in hypocupremic infants. Nutr. Res. 5, 1327-1334
7. Xin, Z., Waterman, D. F., Hemken, R. W., and Harmon, R. J. (1991) Effects of copper status on neutrophil function, superoxide dismutase, and copper distribution in steers. J. Dairy Sci. 74, 3078-3085
8. Babu, U., and Failla, M. L. (1990) Respiratory burst and candidacidal activity of peritoneal macrophages are impaired in copper-deficient rats. J. Nutr. 120, 1692-1699
9. Jones, D. G., and Suttle, N. F. (1983) The effect of copper deficiency on the resistance of mice to infection with Pasteurella haemolytica. J. Comp. Pathol. 93, 143-149
10. Newberne, P. M., Hunt, C. E., and Young, V. R. (1968) The role of diet and the reticuloendothelial system in the response of rats to Salmonella typhimurium infection. Br. J. Exp. Pathol. 49, 448-457
11. Crocker, A., Lee, C., Aboko-Cole, G., and Durham, C. (1992) Interaction of nutrition and infection: Effect of copper deficiency on resistance to Trypanosoma lewisi. J. Natl. Med. Assoc. 84, 697-706
12. Subashchandrabose, S., Hazen, T. H., Brumbaugh, A. R., Himpsl, S. D., Smith, S. N., Ernst, R. D., Rasko, D. A., and Mobley, H. L. (2014) Hostspecific induction of Escherichia coli fitness genes during human urinary tract infection. Proc. Natl. Acad. Sci. U.S.A. 111, 18327-18332
13. 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. U.S.A. 108, 1621-1626
14. White, C., Lee, J., Kambe, T., Fritsche, K., and Petris, M. J. (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949-33956
15. 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
16. Fischer Walker, C., and Black, R. E. (2004) Zinc and the risk for infectious disease. Annu. Rev. Nutr. 24, 255-275
17. Black, R. E. (2003) Zinc deficiency, infectious disease and mortality in the developing world. J. Nutr. 133, 1485S-1489S
18. Coles, C. L., Sherchand, J. B., Khatry, S. K., Katz, J., Leclerq, S. C., Mullany, L. C., and Tielsch, J. M. (2008) Zinc modifies the association between nasopharyngeal Streptococcus pneumoniae carriage and risk of acute lower respiratory infection among young children in rural Nepal. J. Nutr. 138, 2462-2467
19. Wirth, J. J., Fraker, P. J., and Kierszenbaum, F. (1984) Changes in the levels of marker expression by mononuclear phagocytes in zinc-deficient mice. J. Nutr. 114, 1826-1833
20. Ercan, M. T., and Bor, N. M. (1991) Phagocytosis by macrophages in zinc-deficient rats. Int. J. Rad. Appl. Instrum. B. 18, 765-768
21. Weston, W. L., Huff, J. C., Humbert, J. R., Hambidge, K. M., Neldner, K. H., and Walravens, P. A. (1977) Zinc correction of defective chemotaxis in acrodermatitis enteropathica. Arch. Dermatol. 113, 422-425
22. Briggs, W. A., Pedersen, M. M., Mahajan, S. K., Sillix, D. H., Prasad, A. S., and McDonald, F. D. (1982) Lymphocyte and granulocyte function in zinc-treated and zinc-deficient hemodialysis patients. Kidney Int. 21, 827-832
23. Kreindler, T. G., Weston, W. L., Hambidge, K. M., and Dustin, R. (1977) Effect of zinc deficiency on neutrophil and monocyte function in rats. J. Invest. Dermatol. 68, 240-241
24. Wirth, J. J., Fraker, P. J., and Kierszenbaum, F. (1989) Zinc requirement for macrophage function: Effect of zinc-deficiency on uptake and killing of a protozoan parasite. Immunology 68, 114-119
25. James, S. J., Swendseid, M., and Makinodan, T. (1987) Macrophage-mediated depression of t-cell proliferation in Zinc-deficient mice. J. Nutr. 117, 1982-1988
26. Karl, L., Chvapil, M., and Zukoski, C. F. (1973) Effect of zinc on viability and phagocytic capacity of peritoneal macrophages. Proc. Soc. Exp. Biol. Med. 142, 1123-1127
27. Chvapil, M., Stankova, L., Bernhard, D. S., Weldy, P. L., Carlson, E. C., and Campbell, J. B. (1977) Effect of zinc on peritoneal macrophages in vitro. Infect. Immun. 16, 367-373
28. Hodgkinson, V., and Petris, M. J. (2012) Copper homeostasis at the hostpathogen interface. J. Biol. Chem. 287, 13549-13555
29. Festa, R. A., and Thiele, D. J. (2012) Copper at the front line of the hostpathogen battle. PLoS Pathog. 8, e1002887
30. German, N., Doyscher, D., and Rensing, C. (2013) Bacterial killing in macrophages and amoeba: Do they all use a brass dagger? Future Microbiol. 8, 1257-1264
31. Rae, T. D., Schmidt, P. J., Pufahl, R. A., Culotta, V. C., and O'Halloran, T. V. (1999) Undetectable intracellular free copper: The requirement of a copper chaperone for superoxide dismutase. Science 284, 805-808
32. Vazquez-Torres, A., Jones-Carson, J., Mastroeni, P., Ischiropoulos, H., and Fang, F. C. (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effects on microbial killing by activated peritoneal macrophages in vitro. J. Exp. Med. 192, 227-236
33. Djoko, K. Y., Franiek, J. A., Edwards, J. L., Falsetta, M. L., Kidd, S. P., Potter, A. J., Chen, N. H., Apicella, M. A., Jennings, M. P., and McEwan, A. G. (2012) Phenotypic characterization of a copA mutant of Neisseria gonorrhoeae identifies a link between copper and nitrosative stress. Infect. Immun. 80, 1065-1071
34. Gold, B., Deng, H., Bryk, R., Vargas, D., Eliezer, D., Roberts, J., Jiang, X., and Nathan, C. (2008) Identification of a copper-binding metallothionein in pathogenic Mycobacteria. Nat. Chem. Biol. 4, 609-616
35. Valko, M., Morris, H., and Cronin, M. T. D. (2005) Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208
36. Williams, D. L. H. (1999) The chemistry of S-nitrosothiols. Acc. Chem. Res. 32, 869-876
37. Tottey, S., Patterson, C. J., Banci, L., Bertini, I., Felli, I. C., Pavelkova, A., Dainty, S. J., Pernil, R., Waldron, K. J., Foster, A. W., and Robinson, N. J. (2012) Cyanobacterial metallochaperone inhibits deleterious side reactions of copper. Proc. Natl. Acad. Sci. U.S.A. 109, 95-100
38. Macomber, L., and Imlay, J. A. (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 8344-8349
39. Chillappagari, S., Seubert, A., Trip, H., Kuipers, O. P., Marahiel, M. A., and Miethke, M. (2010) Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J. Bacteriol. 192, 2512-2524
40. Djoko, K. Y., and McEwan, A. G. (2013) Antimicrobial action of copper is amplified via inhibition of heme biosynthesis. ACS Chem. Biol. 8, 2217-2223
41. Fung, D. K. C., Lau, W. Y., Chan, W. T., and Yan, A. (2013) Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis. J. Bacteriol. 195, 4556-4568
42. Andreini, C., Banci, L., Bertini, I., and Rosato, A. (2006) Counting the zinc-proteins encoded in the human genome. J. Proteome Res. 5, 196-201
43. Maret, W. (2013) Zinc biochemistry: From a single zinc enzyme to a key element of life. Adv. Nutr. 4, 82-91
44. Maret, W. (2011) Metals on the move: Zinc ions in cellular regulation and in the coordination dynamics of zinc proteins. Biometals 24, 411-418
45. McDevitt, C. A., Ogunniyi, A. D., Valkov, E., Lawrence, M. C., Kobe, B., McEwan, A. G., and Paton, J. C. (2011) A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7, e1002357
46. Eijkelkamp, B. A., Morey, J. R., Ween, M. P., Ong, C. L., McEwan, A. G., Paton, J. C., and McDevitt, C. A. (2014) Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae. PLoS One 9, e89427
47. Maret, W. (2013) Inhibitory zinc sites in enzymes. Biometals 26, 197-204
48. Scheie, A. A., and Pearce, E. I. F. (1994) The effect of mineral-derived zinc ions on in vitro glucose metabolism of Streptococcus mutans NCTC 10449. Caries Res. 28, 329-334
49. Dineley, K. E., Votyakova, T. V., and Reynolds, I. J. (2003) Zinc inhibition of cellular energy production: Implications for mitochondria and neurodegeneration. J. Neurochem. 85, 563-570
50. Ong, C. L., Walker, M. J., and McEwan, A. G. (2015) Zinc disrupts central carbon metabolism and capsule biosynthesis in Streptococcus pyogenes. Sci. Rep. 5, 10799
51. Outten, F. W., Huffman, D. L., Hale, J. A., and 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
52. Liu, T., Ramesh, A., Ma, Z., Ward, S. K., Zhang, L., George, G. N., Talaat, A. M., Sacchettini, J. C., and Giedroc, D. P. (2007) CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat. Chem. Biol. 3, 60-68
53. Festa, R. A., Jones, M. B., Butler-Wu, S., Sinsimer, D., Gerads, R., Bishai, W. R., Peterson, S. N., and Darwin, K. H. (2011)Anovel copper-responsive regulon in Mycobacterium tuberculosis. Mol. Microbiol. 79, 133-148
54. 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
55. Shafeeq, S., Yesilkaya, H., Kloosterman, T. G., Narayanan, G., Wandel, M., Andrew, P. W., Kuipers, O. P., and Morrissey, J. A. (2011) The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Mol. Microbiol. 81, 1255-1270
56. 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
57. Achard, M. E., Tree, J. J., Holden, J. A., Simpfendorfer, K. R., Wijburg, O. L., Strugnell, R. A., Schembri, M. A., Sweet, M. J., Jennings, M. P., and McEwan, A. G. (2010) The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect. Immun. 78, 2312-2319
58. Tree, J. J., Kidd, S. P., Jennings, M. P., and McEwan, A. G. (2005) Copper sensitivity of cueO mutants of Escherichia coli K-12 and the biochemical suppression of this phenotype. Biochem. Biophys. Res. Commun. 328, 1205-1210
59. Schwan, W. R., Warrener, P., Keunz, E., Stover, C. K., and Folger, K. R. (2005) Mutations in the cueA gene encoding a copper homeostasis P-type ATPase reduce the pathogenicity of Pseudomonas aeruginosa in mice. Int. J. Med. Microbiol. 295, 237-242
60. Johnson, M. D. L., Kehl-Fie, T. E., Klein, R., Kelly, J., Burnham, C., Mann, B., and Rosch, J. W. (2015) Role of copper efflux in pneumococcal pathogenesis and resistance to macrophage-mediated immune clearance. Infect. Immun. 83, 1684-1694
61. Corbett, D., Schuler, S., Glenn, S., Andrew, P. W., Cavet, J. S., and Roberts, I. S. (2011) The combined actions of the copper-responsive repressor CsoR and copper-metallochaperone CopZ modulate CopA-mediated copper efflux in the intracellular pathogen Listeria monocytogenes. Mol. Microbiol. 81, 457-472
62. Francis, M. S., and Thomas, C. J. (1997) Mutants in the CtpA copper transporting P-type ATPase reduce virulence of Listeria monocytogenes. Microb. Pathog. 22, 67-78
63. Marrero, K., Sánchez, A., González, L. J., Ledón, T., Rodríguez-Ulloa, A., Castellanos-Serra, L., Pérez, C., and Fando, R. (2012) Periplasmic proteins encoded by VCA0261-0260 and VC2216 genes together with copA and cueR products are required for copper tolerance but not for virulence in Vibrio cholerae. Microbiology 158, 2005-2016
64. Ward, S. K., Abomoelak, B., Hoye, E. A., Steinberg, H., and Talaat, A. M. (2010) CtpV: A putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol. Microbiol. 77, 1096-1110
65. 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
66. Tree, J. J., Ulett, G. C., Ong, C. L., Trott, D. J., McEwan, A. G., and Schembri, M. A. (2008) Trade-off between iron uptake and protection against oxidative stress: Deletion of cueO promotes uropathogenic Escherichia coli virulence in a mouse model of urinary tract infection. J. Bacteriol. 190, 6909-6912
67. Tree, J. J., Ulett, G. C., Hobman, J. L., Constantinidou, C., Brown, N. L., Kershaw, C., Schembri, M. A., Jennings, M. P., and McEwan, A. G. (2007) The multicopper oxidase (CueO) and cell aggregation in Escherichia coli. Environ. Microbiol. 9, 2110-2116
68. Brocklehurst, K. R., Hobman, J. L., Lawley, B., Blank, L., Marshall, S. J., Brown, N. L., and Morby, A. P. (1999) ZntR is a Zn(II)-responsive MerRlike transcriptional regulator of zntA in Escherichia coli. Mol. Microbiol. 31, 893-902
69. Rensing, C., Mitra, B., and Rosen, B. P. (1997) The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. U.S.A. 94, 14326-14331
70. Kloosterman, T. G., Van Der Kooi-Pol, M. M., Bijlsma, J. J. E., and Kuipers, O. P. (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
71. Ong, C.-l. Y., Gillen, C. M., Barnett, T. C., Walker, M. J., and McEwan, A. G. (2014) An antimicrobial role for zinc in innate immune defense against Group A Streptococcus. J. Infect. Dis. 209, 1500-1508
72. Carlomagno, M. A., Coghlan, L. G., and McMurray, D. N. (1986) Chronic zinc deficiency and listeriosis in rats: Acquired cellular resistance and response to vaccination. Med. Microbiol. Immunol. 175, 271-280
73. McMurray, D. N., Bartow, R. A., Mintzer, C. L., and Hernandez-Frontera, E. (1990) Micronutrient status and immune function in tuberculosis. Ann. N.Y. Acad. Sci. 587, 59-69
74. Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., Wang, C., Tailleux, L., Tilleul, S., Charrière, G. M., Waddell, S. J., Foti, M., Lugo-Villarino, G., Gao, Q., Maridonneau-Parini, I., Butcher, P. D., Castagnoli, P. R., Gicquel, B., De Chastellier, C., and Neyrolles, O. (2011) Mycobacterial P-1-Type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259
75. Stähler, F. N., Odenbreit, S., Haas, R., Wilrich, J., Van Vliet, A. H., Kusters, J. G., Kist, M., and Bereswill, S. (2006) The novel Helicobacter pylori CznABC metal efflux pump is required for cadmium, zinc, and nickel resistance, urease modulation, and gastric colonization. Infect. Immun. 74, 3845-3852
76. Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C. E., 3rd, Höner Zu Bentrup, K., Russell, D. G., and Bermudez, L. E. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 174, 1491-1500
77. Lichten, L. A., and Cousins, R. J. (2009) Mammalian zinc transporters: Nutritional and physiologic regulation. Annu. Rev. Nutr. 29, 153-176
78. Subramanian Vignesh, K., Landero Figueroa, J. A., Porollo, A., Caruso, J. A., and Deepe, G. S., Jr. (2013) Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39, 697-710
79. Haase, H., Ober-Blöbaum, J. L., Engelhardt, G., Hebel, S., Heit, A., Heine, H., and Rink, L. (2008) Zinc signals are essential for lipopolysaccharideinduced signal transduction in monocytes. J. Immunol. 181, 6491-6502
80. Liu, M. J., Bao, S., Gálvez-Peralta, M., Pyle, C. J., Rudawsky, A. C., Pavlovicz, R. E., Killilea, D. W., Li, C., Nebert, D. W., Wewers, M. D., and Knoell, D. L. (2013) ZIP8 regulates host defense through zinc-mediated inhibition of NF -B. Cell Rep. 3, 386-400
81. Fukada, T., Yamasaki, S., Nishida, K., Murakami, M., and Hirano, T. (2011) Zinc homeostasis and signaling in health and diseases. J. Biol. Inorg. Chem. 16, 1123-1134
82. Haase, H., and Rink, L. (2009) Functional significance of zinc-related signaling pathways in immune cells. Annu. Rev. Nutr. 29, 133-152
83. Anderson, C. J., Schwarz, S. W., Connett, J. M., Cutler, P. D., Guo, L. W., Germain, C. J., Philpott, G. W., Zinn, K. R., Greiner, D. P., Meares, C. F., and Welch, M. J. (1995) Preparation, Biodistribution and dosimetry of copper-64-labeled anti-colorectal carcinoma monoclonal antibody fragments 1a3-F(Ab -)2. J. Nucl. Med. 36, 850-858
84. McQuade, P., Martin, K. E., Castle, T. C., Went, M. J., Blower, P. J., Welch, M. J., and Lewis, J. S. (2005) Investigation into 64Cu-labeled Bis(selenosemicarbazone) and Bis(thiosemicarbazone) complexes as hypoxia imaging agents. Nucl. Med. Biol. 32, 147-156
85. Linder, M. C., and Hazegh-Azam, M. (1996) Copper biochemistry and molecular biology. Am. J. Clin. Nutr. 63, 797S-811S
86. Wheeler, E. M., and Roberts, P. F. (1976) Menkes's steely hair syndrome. Arch. Dis. Child. 51, 269-274
87. Tümer, Z., and Møller, L. B. (2010) Menkes disease. Eur. J. Hum. Genet. 18, 511-518
88. Talaat, A. M., Lyons, R., Howard, S. T., and Johnston, S. A. (2004) The temporal expression profile of Mycobacterium tuberculosis infection in mice. Proc. Natl. Acad. Sci. U.S.A. 101, 4602-4607
89. Liuzzi, J. P., Lichten, L. A., Rivera, S., Blanchard, R. K., Aydemir, T. B., Knutson, M. D., Ganz, T., and Cousins, R. J. (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc. Natl. Acad. Sci. U.S.A. 102, 6843-6848
90. Cousins, R. J., and Leinart, A. S. (1988) Tissue-specific regulation of zinc metabolism and metallothionein genes by interleukin 1. FASEB J. 2, 2884-2890
91. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., Anderson, K. L., Dattilo, B. M., Dunman, P. M., Gerads, R., Caprioli, R. M., Nacken, W., Chazin, W. J., and Skaar, E. P. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965
92. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., and Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535
93. Brophy, M. B., Hayden, J. A., and Nolan, E. M. (2012) Calcium ion gradients modulate the zinc affinity and antibacterial activity of human calprotectin. J. Am. Chem. Soc. 134, 18089-18100
94. Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., Brinkmann, V., Jungblut, P. R., and Zychlinsky, A. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5, e1000639
95. Conforti, A., Franco, L., Milanino, R., Totorizzo, A., and Velo, G. P. (1983) Copper metabolism during acute inflammation: Studies on liver and serum copper concentrations in normal and inflamed rats. Br. J. Pharmacol. 79, 45-52
96. Conforti, A., Franco, L., Milanino, R., and Velo, G. P. (1982) Copper and ceruloplasmin (Cp) concentrations during the acute inflammatory process in the rat. Agents. Actions. 12, 303-307
97. Abboud, S., and Haile, D. J. (2000) A novel mammalian iron-regulated protein involved in intracellular iron metabolism. J. Biol. Chem. 275, 19906-19912
98. De Domenico, I., Ward, D. M., di Patti, M. C. B., Jeong, S. Y., David, S., Musci, G., and Kaplan, J. (2007) Ferroxidase activity is required for the stability of cell surface ferroportin in cells expressing GPI-ceruloplasmin. EMBO J. 26, 2823-2831
99. Lutsenko, S., Barnes, N. L., Bartee, M. Y., and Dmitriev, O. Y. (2007) Function and regulation of human copper-transporting ATPases. Physiol. Rev. 87, 1011-1046