Nutritional immunity: Transition metals at the pathogen-host interface

Nature Reviews Microbiology

Volumn 10, Issue 8, 2012, Pages 525-537

  Hood, M Indriati ^a   Skaar, Eric P ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; CADMIUM; CALGRANULIN; CALGRANULIN A; CALGRANULIN B; COPPER; FERRIC UPTAKE REGULATOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HAPTOGLOBIN; HEME; HEME OXYGENASE; HEME OXYGENASE 1; HEMOGLOBIN; IRON; MANGANESE; MERCURY; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PROTEIN CHUZ; PROTEIN CTR1; PROTEIN FEOA; PROTEIN FEOB; PROTEIN FEOC; PROTEIN TONB; PROTEIN ZNUD; PROTEIN ZUR; PSORIASIN; SILVER; TRANSITION ELEMENT; UNCLASSIFIED DRUG; UNINDEXED DRUG; ZINC;

ASPERGILLUS; BACILLUS ANTHRACIS; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; BRADYRHIZOBIUM JAPONICUM; BRUCELLA ABORTUS; CAMPYLOBACTER JEJUNI; CANDIDA; CHELATION; ECOLOGICAL NICHE; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; HELICOBACTER PYLORI; HOMEOSTASIS; HOST PATHOGEN INTERACTION; IMMUNITY; INNATE IMMUNITY; MORAXELLA CATARRHALIS; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA MENINGITIDIS; NONHUMAN; NUTRIENT; NUTRITION; PHOTORHABDUS LUMINESCENS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; REVIEW; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS SUIS; STREPTOMYCES COELICOLOR; YERSINIA PESTIS;

BACTERIA; FOOD; HOST-PATHOGEN INTERACTIONS; HUMANS; METALS; TRANSITION ELEMENTS;

BACTERIA (MICROORGANISMS);

EID: 84863899006     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2836     Document Type: Review

References (150)

1. Andreini, C., Bertini, I., Cavallaro, G., Holliday, G. L. & Thornton, J. M. Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem. 13, 1205-1218 (2008).
2. Andreini, C., Bertini, I. & Rosato, A. Metalloproteomes: a bioinformatic approach. Acc. Chem. Res. 42, 1471-1479 (2009).
3. Andreini, C., Banci, L., Bertini, I. & Rosato, A. Zinc through the three domains of life. J. Proteome Res. 5, 3173-3178 (2006).
4. Weinberg, E. D. Nutritional immunity. Host's attempt to withold iron from microbial invaders. JAMA 231, 39-41 (1975).
5. Weinberg, E. D. Iron availability and infection. Biochim. Biophys. Acta 1790, 600-605 (2009).
6. Cassat, J. E. & Skaar, E. P. Metal ion acquisition in Staphylococcus aureus: overcoming nutritional immunity. Semin. Immunopathol. 34, 215-235 (2011).
7. Haley, K. P. & Skaar, E. P. A battle for iron: host sequestration and Staphylococcus aureus acquisition. Microbes Infect. 14, 217-227 (2011).
8. Nobles, C. L. & Maresso, A. W. The theft of host heme by Gram-positive pathogenic bacteria. Metallomics 3, 788-796 (2011).
9. Ong, S. T., Shan Ho, J. Z., Ho, B. & Ding, J. L. Iron-withholding strategy in innate immunity. Immunobiology 211, 295-314 (2006).
10. Braun, V. & Hantke, K. Recent insights into iron import by bacteria. Curr. Opin. Chem. Biol. 15, 328-334 (2011).
11. Jabado, N. et al. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH dependent manganese transporter at the phagosomal membrane. J. Exp. Med. 192, 1237-1248 (2000).
12. Forbes, J. R. & Gros, P. Iron, managanese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 102, 1884-1892 (2003).
13. Schaible, U. E., Collins, H. L., Priem, F. & Kaufmann, S. H. E. Correction of the iron overload defect in β 2 microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J. Exp. Med. 196, 1507-1513 (2002).
14. Posey, J. E. & Gherardini, F. C. Lack of a role for iron in the Lyme disease pathogen. Science 288, 1651-1653 (2000).
15. Schalk, I. J. Metal trafficking via siderophores in Gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J. Inorg. Biochem. 102, 1159-1169 (2008).
16. Flo, T. H. et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432, 917-921 (2004).
17. Abergel, R. J. et al. Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc. Natl Acad. Sci. USA 103, 18499-18503 (2006).
18. Hantke, K., Nicholson, G., Rabsch, W. & Winkelmann, G. Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc. Natl Acad. Sci. USA 100, 3677-3682 (2003).
19. Cornelis, P. Iron uptake and metabolism in pseudomonads. Appl. Microbiol. Biotechnol. 86, 1637-1645 (2010).
20. Ratcliff-Griffin, M., Wilks, A. & Stojiljkovic, I. in Iron Transport in Bacteria: Molecular Genetics, Biochemistry, Microbial Pathogenesis and Ecology (eds Crosa, J. H., Mey, A. R. & Payne, S. M.) 86-94 (American Society for Microbiology Press, 2004).
21. Honsa, E. S. & Maresso, A. W. Mechanisms of iron import in anthrax. Biometals 24, 533-545 (2011).
22. Fabian, M., Solomaha, E., Olson, J. S. & Maresso, A. W. Heme transfer to the bacterial cell envelope occurs via a secreted hemophore in the Gram-positive pathogen Bacillus anthracis. J. Biol. Chem. 284, 32138-32146 (2009).
23. Cescau, S. et al. Heme acquisition by hemophores. Biometals 20, 603-613 (2007).
24. Wilks, A. Heme oxygenase: evolution, structure, and mechanism. Antioxid. Redox Signal. 4, 603-614 (2002).
25. Puri, S. & O'Brian, M. R. The hmuQ and hmuD genes from Bradyrhizobium japonicum encode heme-degrading enzymes. J. Bacteriol. 188, 6476-6482 (2006).
26. Chim, N., Iniguez, A., Nguyen, T. Q. & Goulding, C. W. Unusual diheme conformation of the heme-degrading protein from Mycobacterium tuberculosis. J. Mol. Biol. 395, 595-608 (2010).
27. Haley, K. P., Janson, E. M., Heilbronner, S., Foster, T. J. & Skaar, E. P. Staphylococcus lugdunensis IsdG liberates iron from host heme. J. Bacteriol. 193, 4749-4757 (2011).
28. Reniere, M. L. et al. The IsdG-family of haem oxygenases degrades haem to a novel chromophore. Mol. Microbiol. 75, 1529-1538 (2010).
29. Zhang, R. et al. Crystallization and preliminary crystallographic studies of Campylobacter jejuni ChuZ, a member of a novel haem oxygenase family. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67, 1228-1230 (2011).
30. Zhang, R. et al. Crystal structure of Campylobacter jejuni ChuZ: a split-barrel family heme oxygenase with a novel heme-binding mode. Biochem. Biophys. Res. Commun. 415, 82-87 (2011).
31. Cornelissen, C. Transferrin-iron uptake by Gram-negative bacteria. Front. Biosci. 8, D836-D847 (2003).
32. Aranda, J. et al. Contribution of the FeoB transporter to Streptococcus suis virulence. Int. Microbiol. 12, 137-143 (2009).
33. Cartron, M. L., Maddocks, S., Gillingham, P., Craven, C. J. & Andrews, S. C. Feo-transport of ferrous iron into bacteria. Biometals 19, 143-157 (2006).
34. Panciera, R., Marlow, D. & Stintzi, A. Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect. Immun. 74, 5433-5444 (2006).
35. Pandey, A. & Sonti, R. V. Role of the FeoB protein and siderophore in promoting virulence of Xanthomonas oryzae pv. oryzae on rice. J. Bacteriol. 192, 3187-3203 (2010).
36. Lemanceau, P., Expert, D., Gaymard, F., Bakker, P. A. H. M. & Briat, J. F. Chapter 12 Role of iron in plant-microbe interactions. Adv. Bot. Res. 51, 491-549 (2009).
37. Expert, D. Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu. Rev. Phytopathol. 37, 307-334 (1999).
38. Geiser, D. L. & Winzerling, J. J. Insect transferrins: multifunctional proteins. Biochim. Biophys. Acta 1820, 437-451 (2012).
39. Watson, R. J., Millichap, P., Joyce, S. A., Reynolds, S. & Clarke, D. J. The role of iron uptake in pathogenicity and symbiosis in Photorhabdus luminescens TT01. BMC Microbiol. 10, 177 (2010).
40. Kehl-Fie, T. E. & Skaar, E. P. Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 14, 218-224 (2010).
41. Nies, D. H. & Grass, G. Transition metal homeostasis. In Escherichia coli and Salmonella: Cellular and Molecular Biology (eds Böck, A. et al.) chapter 5.4.4.3 EcoSal [online] http://www.ecosal.org/(American Society for Microbiology Press, 2002).
42. Tseng, H. J. Srikhanta, Y., McEwan, A. G. & Jennings, M. P. Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol. Microbiol. 40, 1175-1186 (2001).
43. Anjem, A., Varghese, S. & Imlay, J. A. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol. Microbiol. 72, 844-858 (2009).
44. Martin, J. E. & Imlay, J. A. The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Mol. Microbiol. 80, 319-334 (2011).
45. Sobota, J. M. & Imlay, J. A. Iron enzyme ribulose-5 phosphate 3 epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc. Natl Acad. Sci. USA 108, 5402-5407 (2011).
46. Kehl-Fie, T. E. et al. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10, 158-164 (2011).
47. Hantke, K. Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8, 196-202 (2005).
48. Gläser, R. et al. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nature Immunol. 6, 57-64 (2005).
49. Moroz, O. V. et al. Structure of the human S100A12-copper complex: implications for host-parasite defence. Acta Crystallograph. Section D Biol. Crystallogr. 59, 859-867 (2003).
50. Moroz, O. V. et al. Both Ca2+ and Zn2+ are essential for S100A12 protein oligomerization and function. BMC Biochem. 10, 11 (2009).
51. Corbin, B. D. et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965 (2008).
52. McCormick, A. et al. NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect. 12, 928-936 (2010).
53. Urban, C. F. et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5, e1000639 (2009).
54. Liu, J. Z. et al. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11, 227-239 (2012).
55. Bianchi, M., Niemiec, M. J., Siler, U., Urban, C. F. & Reichenbach, J. Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin- dependent. J. Allergy Clin. Immunol. 127, 1243-1252.e7 (2011).
56. Hsu, K. et al. Anti-infective protective properties of S100 calgranulins. AntiInflamm. Antiallergy Agents Med. Chem. 8, 290-305 (2009).
57. Kehres, D. G., Janakiraman, A., Slauch, J. M. & Maguire, M. E. SitABCD is the alkaline Mn2+ transporter of Salmonella enterica serovar typhimurium. J. Bacteriol. 184, 3159-3166 (2002).
58. Ammendola, S. et al. High-affinity Zn2+ uptake system ZnuABC is required for bacterial zinc homeostasis in intracellular environments and contributes to the virulence of Salmonella enterica. Infect. Immun. 75, 5867-5876 (2007).
59. Campoy, S. et al. Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar typhimurium virulence. Infect. Immun. 70, 4721-4725 (2002).
60. Davis, L. M., Kakuda, T. & DiRita, V. J. A Campylobacter jejuni znuA orthologue is essential for growth in low-zinc environments and chick colonization. J. Bacteriol. 191, 1631-1640 (2009).
61. Bearden, S. W. & Perry, R. D. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32, 403-414 (1999).
62. Champion, O. L. et al. Yersinia pseudotuberculosis mntH functions in intracellular manganese accumulation, which is essential for virulence and survival in cells expressing functional Nramp1. Microbiology 157, 1115-1122 (2011).
63. Perry, R. D. et al. Manganese transporters Yfe and MntH are Fur regulated and important for the virulence of Yersinia pestis. Microbiology 158, 804-815 (2012).
64. Anderson, E. S. et al. The manganese transporter MntH is a critical virulence determinant for Brucella abortus 2308 in experimentally infected mice. Infect. Immun. 77, 3466-3474 (2009).
65. Rosadini, C. V., Gawronski, J. D., Raimunda, D., Argüello, J. M. & Akerley, B. J. A novel zinc binding system, ZevAB, is critical for survival of nontypeable Haemophilus influenzae in a murine lung infection model. Infect. Immun. 79, 3366-3376 (2011).
66. Corbett, D. et al. Two zinc uptake systems contribute to the full virulence of Listeria monocytogenes during growth in vitro and in vivo. Infect. Immun. 80, 14-21 (2012).
67. Bayle, L. et al. Zinc uptake by Streptococcus pneumoniae depends on both AdcA and AdcAII and is essential for normal bacterial morphology and virulence. Mol. Microbiol. 82, 904-916 (2011).
68. Hohle, T. H., Franck, W. L., Stacey, G. & O'Brian, M. R. Bacterial outer membrane channel for divalent metal ion acquisition. Proc. Natl Acad. Sci. USA 108, 15390-15395 (2011).
69. Stork, M. et al. An outer membrane receptor of Neisseria meningitidis involved in zinc acquisition with vaccine potential. PLoS Pathog. 6, e1000969 (2010).
70. Kumar, P., Sannigrahi, S. & Tzeng, Y. L. The Neisseria meningitidis ZnuD zinc receptor contributes to interactions with epithelial cells and supports heme utilization when expressed in Escherichia coli. Infect. Immun. 80, 657-667 (2012).
71. Li, J. M., Russell, C. S. & Cosloy, S. D. The structure of the Escherichia coli hemB gene. Gene 75, 177-184 (1989).
72. Kallifidas, D. et al. The zinc-responsive regulator Zur controls expression of the coelibactin gene cluster in Streptomyces coelicolor. J. Bacteriol. 192, 608-611 (2010).
73. Brandel, J. et al. Pyochelin, a siderophore of Pseudomonas aeruginosa: physicochemical characterization of the iron(iii), copper(ii) and zinc(ii) complexes. Dalton Trans. 41, 2820-2834 (2012).
74. Klein, J. S. & Lewinson, O. Bacterial ATP-driven transporters of transition metals: physiological roles, mechanisms of action, and roles in bacterial virulence. Metallomics 3, 1098-1108 (2011).
75. Andresen, E. et al. S100A7/psoriasin expression in the human lung: unchanged in patients with COPD, but upregulated upon positive S. aureus detection. BMC Pulm. Med. 11, 10 (2011).
76. Nielubowicz, G. R., Smith, S. N. & Mobley, H. L. T. Zinc uptake contributes to motility and provides a competitive advantage to Proteus mirabilis during experimental urinary tract infection. Infect. Immun. 78, 2823-2833 (2010).
77. Dashper, S. G. et al. A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J. Biol. Chem. 280, 28095-28102 (2005).
78. Botella, H., Stadthagen, G., Lugo-Villarino, G., de Chastellier, C. & Neyrolles, O. Metallobiology of host-pathogen interactions: an intoxicating new insight. Trends Microbiol. 20, 106-112 (2012).
79. Botella, H. et al. Mycobacterial P1 type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259 (2011).
80. Hou, Z. J., Narindrasorasak, S., Bhushan, B., Sarkar, B. & Mitra, B. Functional analysis of chimeric proteins of the Wilson Cu(I)-ATPase (ATP7B) and ZntA, a Pb(II)/Zn(II)/Cd(II)-ATPase from Escherichia coli. J. Biol. Chem. 276, 40858-40863 (2001).
81. Veyrier, F. J., Boneca, I. G., Cellier, M. F. & Taha, M. K. A novel metal transporter mediating manganese export (MntX) regulates the Mn to Fe intracellular ratio and Neisseria meningitidis virulence. PLoS Pathog. 7, e1002261 (2011).
82. Rosch, J. W., Gao, G., Ridout, G., Wang, Y. D. & Tuomanen, E. I. Role of the manganese efflux system mntE for signalling and pathogenesis in Streptococcus pneumoniae. Mol. Microbiol. 72, 12-25 (2009).
83. Jacobsen, F. E., Kazmierczak, K. M., Lisher, J. P., Winkler, M. E. & Giedroc, D. P. Interplay between manganese and zinc homeostasis in the human pathogen Streptococcus pneumoniae. Metallomics 3, 38-41 (2011).
84. McDevitt, C. A. et al. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog. 7, e1002357 (2011).
85. Dintilhac, A., Alloing, G., Granadel, C. & Claverys, J. P. Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol. Microbiol. 25, 727-739 (1997).
86. Lawrence, M. C. et al. The crystal structure of pneumococcal surface antigen PsaA reveals a metal-binding site and a novel structure for a putative ABC type binding protein. Structure 6, 1553-1561 (1998).
87. Ogunniyi, A. D. et al. Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae. J. Bacteriol. 192, 4489-4497 (2010).
88. Samanovic, M. I., Ding, C., Thiele, D. J. & Darwin, K. H. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 11, 106-115 (2012).
89. Wolschendorf, F. et al. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 108, 1621-1626 (2011).
90. White, C., Lee, J., Kambe, T., Fritsche, K. & Petris, M. J. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949-33956 (2009).
91. Kim, B. E., Nevitt, T. & Thiele, D. J. Mechanisms for copper acquisition, distribution and regulation. Nature Chem. Biol. 4, 176-185 (2008).
92. Kim, H. W. et al. Human macrophage ATP7A is localized in the trans-Golgi apparatus, controls intracellular copper levels, and mediates macrophage responses to dermal wounds. Inflammation 35, 167-175 (2011).
93. Macomber, L., Rensing, C. & Imlay, J. A. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J. Bacteriol. 189, 1616-1626 (2007).
94. Djoko, K. Y. et al. Phenotypic characterization of a copA mutant of Neisseria gonorrhoeae identifies a link between copper and nitrosative stress. Infect. Immun. 80, 1065-1071 (2012).
95. Edwards, J. L. Neisseria gonorrhoeae survival during primary human cervical epithelial cell infection requires nitric oxide and is augmented by progesterone. Infect. Immun. 78, 1202-1213 (2010).
96. Xu, F. F. & Imlay, J. A. Silver(I), mercury(II), cadmium(II), and zinc(II) target exposed enzymic iron-sulfur clusters when they toxify Escherichia coli. Appl. Environ. Microbiol. 78, 3614-3621 (2012).
97. Achard, M. E. S. et al. The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect. Immun. 78, 2312-2319 (2010).
98. Macomber, L. & Imlay, J. A. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl Acad. Sci. USA 106, 8344-8349 (2009).
99. Knapp, C. W., Fowle, D. A., Kulczycki, E., Roberts, J. A. & Graham, D. W. Methane monooxygenase gene expression mediated by methanobactin in the presence of mineral copper sources. Proc. Natl Acad. Sci. USA 104, 12040-12045 (2007).
100. Hakemian, A. S. & Rosenzweig, A. C. The biochemistry of methane oxidation. Annu. Rev. Biochem. 76, 223-241 (2007).
101. Kenney, G. E. & Rosenzweig, A. C. Chemistry and biology of the copper chelator methanobactin. ACS Chem. Biol. 7, 260-268 (2011).
102. Kim, H. J. Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305, 1612-1615 (2004).
103. Balasubramanian, R. & Rosenzweig, A. C. Copper methanobactin: a molecule whose time has come. Curr. Opin. Chem. Biol. 12, 245-249 (2008).
104. Hakemian, A. S. et al. The copper chelator methanobactin from Methylosinus trichosporium OB3b binds copper(I). J. Am. Chem. Soc. 127, 17142-17143 (2005).
105. El Ghazouani, A. et al. Copper-binding properties and structures of methanobactins from Methylosinus trichosporium OB3b. Inorg. Chem. 50, 1378-1391 (2011).
106. Balasubramanian, R., Kenney, G. E. & Rosenzweig, A. C. Dual pathways for copper uptake by methanotrophic bacteria. J. Biol. Chem. 286, 37313-37319 (2011).
107. Shafeeq, S. et al. The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Mol. Microbiol. 81, 1255-1270 (2011).
108. Sharan, R., Chhibber, S. & Reed, R. H. A murine model to study the antibacterial effect of copper on infectivity of Salmonella enterica serovar Typhimurium. Int. J. Environ. Res. Public Health 8, 21-36 (2011).
109. Ward, S. K., Abomoelak, B., Hoye, E. A., Steinberg, H. & Talaat, A. M. CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol. Microbiol. 77, 1096-1110 (2010).
110. Liu, T. et al. CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nature Chem. Biol. 3, 60-68 (2006).
111. Festa, R. A. et al. A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol. Microbiol. 79, 133-148 (2010).
112. Kim, J. S. et al. The sctR of Salmonella enterica serova Typhimurium encoding a homologue of MerR protein is involved in the copper-responsive regulation of cuiD. FEMS Microbiol. Lett. 210, 99-103 (2002).
113. Osman, D. et al. Copper homeostasis in Salmonella is atypical and copper-CueP is a major periplasmic metal complex. J. Biol. Chem. 285, 25259-25268 (2010).
114. Outten, F. W., Huffman, D. L., Hale, J. A. & O'Halloran, T. V. The independent cue and cus systems confer copper tolerance during aerobic and anaerobic growth in Escherichia coli. J. Biol. Chem. 276, 30670-30677 (2001).
115. Lu, Z. H., Dameron, C. T. & Solioz, M. The Enterococcus hirae paradigm of copper homeostasis: copper chaperone turnover, interactions, and transactions. Biometals 16, 137-143 (2003).
116. Hsu, Y. H. et al. Association of NRAMP 1 gene polymorphism with susceptibility to tuberculosis in Taiwanese aboriginals. J. Formos. Med. Assoc. 105, 363-369 (2006).
117. Huang, J. H. et al. Analyses of the NRAMP1 and IFN γR1 genes in women with Mycobacterium avium-intracellulare pulmonary disease. Am. J. Respir. Crit. Care Med. 157, 377-381 (1998).
118. Tanaka, G. et al. Pulmonary Mycobacterium avium complex infection: association with NRAMP1 polymorphisms. Eur. Respir. J. 30, 90-96 (2007).
119. Isidor, B. et al. Hyperzincemia and hypercalprotectinemia: unsuccessful treatment with tacrolimus. Acta Paediatr. 98, 410-412 (2009).
120. Saito, Y. et al. Hyperzincemia with systemic inflammation: a heritable disorder of calprotectin metabolism with rheumatic manifestations? J. Pediatr. 140, 267-269 (2002).
121. Lee, A. C. W. & Li, C. H. Age as a factor in severe bacterial infection in transfusion-dependent patients with thalassemia major. Clin. Infect. Dis. 38, 1194-1195; author reply 1195 (2004).
122. Wang, S. C. et al. Severe bacterial infection in transfusion-dependent patients with thalassemia major. Clin. Infect. Dis. 37, 984-988 (2003).
123. Gerhard, G. S. et al. Vibrio vulnificus septicemia in a patient with the hemochromatosis HFE C282Y mutation. Arch. Pathol. Lab. Med. 125, 1107-1109 (2001).
124. Höpfner, M. et al. Yersinia enterocolitica infection with multiple liver abscesses uncovering a primary hemochromatosis. Scand. J. Gastroenterol. 36, 220-224 (2001).
125. Weinberg, E. D. Survival advantage of the hemochromatosis C282Y mutation. Perspect. Biol. Med. 51, 98-102 (2008).
126. Pishchany, G. et al. Specificity for human hemoglobin enhances Staphylococcus aureus infection. Cell Host Microbe 8, 544-550 (2010).
127. Torres, V. J., Pishchany, G., Humayun, M., Schneewind, O. & Skaar, E. P. Staphylococcus aureus IsdB is a hemoglobin receptor required for heme iron utilization. J. Bacteriol. 188, 8421-8429 (2006).
128. Krishna Kumar, K. et al. Structural basis for hemoglobin capture by Staphylococcus aureus cell-surface protein, IsdH. J. Biol. Chem. 286, 38439-38447 (2011).
129. Zarantonelli, M. L. et al. Transgenic mice expressing human transferrin as a model for meningococcal infection. Infect. Immun. 75, 5609-5614 (2007).
130. Schryvers, A. B. & Morris, L. J. Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol. Microbiol. 2, 281-288 (1988).
131. Noinaj, N. et al. Structural basis for iron piracy by pathogenic Neisseria. Nature 483, 53-58 (2012).
132. Calmettes, C., Alcantara, J., Yu, R. H., Schryvers, A. B. & Moraes, T. F. The structural basis of transferrin sequestration by transferrin-binding protein B. Nature Struct. Mol. Biol. 19, 358-360 (2012).
133. Borkow, G. & Gabbay, J. Copper as a biocidal tool. Curr. Med. Chem. 12, 2163-2175 (2005).
134. Mikolay, A. et al. Survival of bacteria on metallic copper surfaces in a hospital trial. Appl. Microbiol. Biotechnol. 87, 1875-1879 (2010).
135. Casey, A. L. et al. Role of copper in reducing hospital environment contamination. J. Hosp. Infect. 74, 72-77 (2010).
136. Zhou, T., Ma, Y., Kong, X. & Hider, R. C. Design of iron chelators with therapeutic application. Dalton Trans. 41, 6371-6389 (2012).
137. Summer, K. H. et al. The biogenic methanobactin is an effective chelator for copper in a rat model for Wilson disease. J. Trace Elem. Med. Biol. 25, 36-41 (2011).
138. Thiennimitr, P. et al. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc. Natl Acad. Sci. USA 108, 17480-17485 (2011).
139. Winter, S. E. et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426-429 (2010).
140. Hoffman, L. R. et al. Nutrient availability as a mechanism for selection of antibiotic tolerant Pseudomonas aeruginosa within the CF airway. PLoS Pathog. 6, e1000712 (2010).
141. Ponton, F., Wilson, K., Cotter, S. C., Raubenheimer, D. & Simpson, S. J. Nutritional immunology: a multi-dimensional approach. PLoS Pathog. 7, e1002223 (2011).
142. Rohmer, L., Hocquet, D. & Miller, S. I. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol. 19, v341-348 (2011).
143. Eisenreich, W., Dandekar, T., Heesemann, J. & Goebel, W. Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nature Rev. Microbiol. 8, 401-412 (2010).
144. Price, C. T. D., Al Quadan, T., Santic, M., Rosenshine, I. & Abu Kwaik, Y. Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science 334, 1553-1557 (2011).
145. Segond, D. et al. NRAMP genes function in Arabidopsis thaliana resistance to Erwinia chrysanthemi infection. Plant J. 58, 195-207 (2009).
146. Dellagi, A. et al. Microbial siderophores exert a subtle role in Arabidopsis during infection by manipulating the immune response and the iron status. Plant Physiol. 150, 1687-1696 (2009).
147. Rokhbakhsh-Zamin, F. et al. Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetum glaucum. J. Microbiol. Biotechnol. 21, 556-566 (2011).
148. Lemanceau, P., Bauer, P., Kraemer, S. & Briat, J. F. Iron dynamics in the rhizosphere as a case study for analyzing interactions between soils, plants and microbes. Plant Soil 321, 513-535 (2009).
149. Cheung, J., Beasley, F. C., Liu, S., Lajoie, G. A. & Heinrichs, D. E. Molecular characterization of staphyloferrin B biosynthesis in Staphylococcus aureus. Mol. Microbiol. 74, 594-608 (2009).
150. Beasley, F. C. et al. Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol. Microbiol. 72, 947-963 (2009).