Mycobacteria, metals, and the macrophage

Immunological Reviews

Volumn 264, Issue 1, 2015, Pages 249-263

  Neyrolles, Olivier ^a,b   Wolschendorf, Frank ^c   Mitra, Avishek ^d   Niederweis, Michael ^d  

^a CNRS   (France)

^b INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Copper; Innate immunity; Iron; Manganese; Nutritional immunity; Phagosome; Poisoning; Zinc

Indexed keywords

COBALT; COPPER; COPPER COMPLEX; HEME; IRON; LACTOFERRIN; MANGANESE; METAL; NICKEL; SIDEROPHORE; TRACE ELEMENT; TRANSFERRIN; TRANSITION ELEMENT; ZINC; TUBERCULOSTATIC AGENT;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CYTOPLASM; DNA DAMAGE; ELECTRON TRANSPORT; ESCHERICHIA COLI; FENTON REACTION; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INNATE IMMUNITY; INNER MEMBRANE; IRON OVERLOAD; IRON TRANSPORT; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; NEISSERIA GONORRHOEAE; NONHUMAN; OPERON; OUTER MEMBRANE; OXIDATION; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; TUBERCULOSIS; ANIMAL; DRUG EFFECTS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; VIRULENCE;

ANIMALS; ANTITUBERCULAR AGENTS; COPPER; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; IRON; MACROPHAGES; METALS; MYCOBACTERIUM TUBERCULOSIS; PHAGOSOMES; TUBERCULOSIS; VIRULENCE; ZINC;

EID: 84923165717     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/imr.12265     Document Type: Article

References (210)

1. van der Wel N, et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007;129:1287-1298.
2. Manzanillo PS, Shiloh MU, Portnoy DA, Cox JS. Mycobacterium tuberculosis activates the DNA-dependent cytosolic surveillance pathway within macrophages. Cell Host Microbe 2012;11:469-480.
3. Welin A, Lerm M. Inside or outside the phagosome? The controversy of the intracellular localization of Mycobacterium tuberculosis Tuberculosis 2012;92:113-120.
4. Vergne I, Chua J, Singh SB, Deretic V. Cell biology of Mycobacterium tuberculosis phagosome. Annu Rev Cell Dev Biol 2004;20:367-394.
5. Rohde K, Yates RM, Purdy GE, Russell DG. Mycobacterium tuberculosis and the environment within the phagosome. Immunol Rev 2007;219:37-54.
6. Rhee KY, et al. Central carbon metabolism in Mycobacterium tuberculosis: an unexpected frontier. Trends Microbiol 2011;19:307-314.
7. Eisenreich W, Dandekar T, Heesemann J, Goebel W. Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 2010;8:401-412.
8. Ehrt S, Rhee K. Mycobacterium tuberculosis metabolism and host interaction: mysteries and paradoxes. Curr Top Microbiol Immunol 2013;374:163-188.
9. Gouzy A, et al. Mycobacterium tuberculosis nitrogen assimilation and host colonization require aspartate. Nat Chem Biol 2013;9:674-676.
10. Gouzy A, et al. Mycobacterium tuberculosis exploits asparagine to assimilate nitrogen and resist acid stress during infection. PLoS Pathog 2014;10:e1003928.
11. Ehrt S, Schnappinger D. Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell Microbiol 2009;11:1170-1178.
12. Cellier MF. Nramp: from sequence to structure and mechanism of divalent metal import. Curr Top Membr 2012;69:249-293.
13. Cellier MF. Nutritional immunity: homology modeling of Nramp metal import. Adv Exp Med Biol 2012;946:335-351.
14. Li X, et al. SLC11A1 (NRAMP1) polymorphisms and tuberculosis susceptibility: updated systematic review and meta-analysis. PLoS ONE 2011;6:e15831.
15. Snow GA. Mycobactins: iron-chelating growth factors from mycobacteria. Bacteriol Rev. 1970;34:99-125.
16. Luo M, Fadeev EA, Groves JT. Mycobactin-mediated iron acquisition within macrophages. Nat Chem Biol 2005;1:149-153.
17. Jones CM, Niederweis M. Mycobacterium tuberculosis can utilize heme as an iron source. J Bacteriol 2011;193:1767-1770.
18. Tullius MV, et al. Discovery and characterization of a unique mycobacterial heme acquisition system. Proc Natl Acad Sci USA 2011;108:5051-5056.
19. Wolschendorf F, et al. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 2011;108:1621-1626.
20. Botella H, et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 2011;10:248-259.
21. Gold B, et al. Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat Chem Biol 2008;4:609-616.
22. Rowland JL, Niederweis M. Resistance mechanisms of Mycobacterium tuberculosis against phagosomal copper overload. Tuberculosis 2012;92:202-210.
23. Rowland JL, Niederweis M. A multicopper oxidase is required for copper resistance in Mycobacterium tuberculosis. J Bacteriol 2013;195:3724-3733.
24. Crichton RR, Pierre JL. Old iron, young copper: from Mars to Venus. Biometals 2001;14:99-112.
25. Outten FW, Theil EC. Iron-based redox switches in biology. Antioxid Redox Signal 2009;11:1029-1046.
26. Posey JE, Gherardini FC. Lack of a role for iron in the Lyme disease pathogen. Science 2000;288:1651-1653.
27. Finch CA, Huebers H. Perspectives in iron metabolism. N Engl J Med 1982;306:1520-1528.
28. Andrews SC, Robinson AK, Rodriguez-Quinones F. Bacterial iron homeostasis. FEMS Microbiol Rev 2003;27:215-237.
29. Anzaldi LL, Skaar EP. Overcoming the heme paradox: heme toxicity and tolerance in bacterial pathogens. Infect Immun 2010;78:4977-4989.
30. Morgenthau A, Pogoutse A, Adamiak P, Moraes TF, Schryvers AB. Bacterial receptors for host transferrin and lactoferrin: molecular mechanisms and role in host-microbe interactions. Future Microbiol 2013;8:1575-1585.
31. Ratledge C, Dover LG. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 2000;54:881-941.
32. Hentze MW, Muckenthaler MU, Galy B, Camaschella C. Two to tango: regulation of Mammalian iron metabolism. Cell 2010;142:24-38.
33. Drakesmith H, Prentice AM. Hepcidin and the iron-infection axis. Science 2012;338:768-772.
34. Mello Filho AC, Hoffmann ME, Meneghini R. Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron. Biochem J 1984;218:273-275.
35. Giorgio M, Trinei M, Migliaccio E, Pelicci PG. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 2007;8:722-728.
36. Saha R, Saha N, Donofrio RS, Bestervelt LL. Microbial siderophores: a mini review. J Basic Microbiol 2013;53:303-317.
37. Koster W. ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res Microbiol 2001;152:291-301.
38. Hammer ND, Skaar EP. Molecular mechanisms of Staphylococcus aureus iron acquisition. Annu Rev Microbiol 2011;65:129-147.
39. Beasley FC, et al. Characterization of staphyloferrin A biosynthetic and transport mutants in Staphylococcus aureus. Mol Microbiol 2009;72:947-963.
40. Dale SE, Doherty-Kirby A, Lajoie G, Heinrichs DE. Role of siderophore biosynthesis in virulence of Staphylococcus aureus: identification and characterization of genes involved in production of a siderophore. Infect Immun 2004;72:29-37.
41. Dale SE, Sebulsky MT, Heinrichs DE. Involvement of SirABC in iron-siderophore import in Staphylococcus aureus. J Bacteriol 2004;186:8356-8362.
42. Skaar EP. The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 2010;6:e1000949.
43. Krewulak KD, Vogel HJ. TonB or not TonB: is that the question? Biochem Cell Biol 2011;89:87-97.
44. Noinaj N, Guillier M, Barnard TJ, Buchanan SK. TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol 2010;64:43-60.
45. Postle K, Larsen RA. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 2007;20:453-465.
46. Mademidis A, Killmann H, Kraas W, Flechsler I, Jung G, Braun V. ATP-dependent ferric hydroxamate transport system in Escherichia coli: periplasmic FhuD interacts with a periplasmic and with a transmembrane/cytoplasmic region of the integral membrane protein FhuB, as revealed by competitive peptide mapping. Mol Microbiol 1997;26:1109-1123.
47. Rohrbach MR, Braun V, Koster W. Ferrichrome transport in Escherichia coli K-12: altered substrate specificity of mutated periplasmic FhuD and interaction of FhuD with the integral membrane protein FhuB. J Bacteriol 1995;177:7186-7193.
48. Oda M, Takahashi M, Matsuno T, Uoo K, Nagahama M, Sakurai J. Hemolysis induced by Bacillus cereus sphingomyelinase. Biochim Biophys Acta 2010;1798:1073-1080.
49. Huseby M, et al. Structure and biological activities of beta toxin from Staphylococcus aureus. J Bacteriol 2007;189:8719-8726.
50. Matsuda S, Kodama T, Okada N, Okayama K, Honda T, Iida T. Association of Vibrio parahaemolyticus thermostable direct hemolysin with lipid rafts is essential for cytotoxicity but not hemolytic activity. Infect Immun 2010;78:603-610.
51. Pishchany G, et al. IsdB-dependent hemoglobin binding is required for acquisition of heme by Staphylococcus aureus. J Infect Dis 2014;209:1764-1772.
52. Mazmanian SK, et al. Passage of heme-iron across the envelope of Staphylococcus aureus. Science 2003;299:906-909.
53. Runyen-Janecky LJ. Role and regulation of heme iron acquisition in gram-negative pathogens. Front Cell Infect Microbiol 2013;3:55.
54. Ghigo JM, Letoffe S, Wandersman C. A new type of hemophore-dependent heme acquisition system of Serratia marcescens reconstituted in Escherichia coli. J Bacteriol 1997;179:3572-3579.
55. Krieg S, et al. Heme uptake across the outer membrane as revealed by crystal structures of the receptor-hemophore complex. Proc Natl Acad Sci USA 2009;106:1045-1050.
56. Gkouvatsos K, Papanikolaou G, Pantopoulos K. Regulation of iron transport and the role of transferrin. Biochim Biophys Acta 2012;1820:188-202.
57. Garcia-Montoya IA, Cendon TS, Arevalo-Gallegos S, Rascon-Cruz Q. Lactoferrin a multiple bioactive protein: an overview. Biochim Biophys Acta 2012;1820:226-236.
58. Wally J, Buchanan SK. A structural comparison of human serum transferrin and human lactoferrin. Biometals 2007;20:249-262.
59. Gray-Owen SD, Schryvers AB. Bacterial transferrin and lactoferrin receptors. Trends Microbiol 1996;4:185-191.
60. Noinaj N, Buchanan SK, Cornelissen CN. The transferrin-iron import system from pathogenic Neisseria species. Mol Microbiol 2012;86:246-257.
61. Cornelissen CN, Hollander A. TonB-dependent transporters expressed by Neisseria gonorrhoeae. Front Microbiol 2011;2:117.
62. Noinaj N, et al. Structural basis for iron piracy by pathogenic Neisseria. Nature 2012;483:53-58.
63. Perkins-Balding D, Ratliff-Griffin M, Stojiljkovic I. Iron transport systems in Neisseria meningitidis. Microbiol Mol Biol Rev 2004;68:154-171.
64. Ratledge C. Iron, mycobacteria and tuberculosis. Tuberculosis 2004;84:110-130.
65. Gobin J, Horwitz MA. Exochelins of Mycobacterium tuberculosis remove iron from human iron-binding proteins and donate iron to mycobactins in the M. tuberculosis cell wall. J Exp Med 1996;183:1527-1532.
66. Evans RW, Kong X, Hider RC. Iron mobilization from transferrin by therapeutic iron chelating agents. Biochim Biophys Acta 2012;1820:282-290.
67. Boradia VM, et al. Mycobacterium tuberculosis acquires iron by cell-surface sequestration and internalization of human holo-transferrin. Nat Commun 2014;5:4730.
68. Clemens DL, Horwitz MA. The Mycobacterium tuberculosis phagosome interacts with early endosomes and is accessible to exogenously administered transferrin. J Exp Med 1996;184:1349-1355.
69. Olakanmi O, Schlesinger LS, Ahmed A, Britigan BE. Intraphagosomal Mycobacterium tuberculosis acquires iron from both extracellular transferrin and intracellular iron pools. Impact of interferon-gamma and hemochromatosis. J Biol Chem 2002;277:49727-49734.
70. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. Cryo-electron tomography and vitreous sections reveal the outer membrane of mycobacteria. Int J Med Microbiol 2007;297:138-139.
71. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 2008;105:3963-3967.
72. Sani M, et al. Direct visualization by cryo-EM of the mycobacterial capsular layer: a labile structure containing ESX-1-secreted proteins. PLoS Pathog 2010;6:e1000794.
73. Niederweis M, Danilchanka O, Huff J, Hoffmann C, Engelhardt H. Mycobacterial outer membranes: in search of proteins. Trends Microbiol 2010;18:109-116.
74. Rodriguez GM. Control of iron metabolism in Mycobacterium tuberculosis. Trends Microbiol 2006;14:320-327.
75. Chavadi SS, et al. Mutational and phylogenetic analyses of the mycobacterial mbt gene cluster. J Bacteriol 2011;193:5905-5913.
76. Wells RM, et al. Discovery of a siderophore export system essential for virulence of Mycobacterium tuberculosis. PLoS Pathog 2013;9:e1003120.
77. Rodriguez GM, Smith I. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol 2006;188:424-430.
78. Ryndak MB, Wang S, Smith I, Rodriguez GM. The Mycobacterium tuberculosis high-affinity iron importer, IrtA, contains an FAD-binding domain. J Bacteriol 2010;192:861-869.
79. Jones CM, et al. Self-poisoning of Mycobacterium tuberculosis by interrupting siderophore recycling. Proc Natl Acad Sci USA 2014;111:1945-1950.
80. Siegrist MS, et al. Mycobacterial Esx-3 requires multiple components for iron acquisition. MBio 2014;5:e01073-01014.
81. Serafini A, Pisu D, Palu G, Rodriguez GM, Manganelli R. The ESX-3 secretion system is necessary for iron and zinc homeostasis in Mycobacterium tuberculosis. PLoS ONE 2013;8:e78351.
82. Siegrist MS, et al. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci USA 2009;106:18792-18797.
83. Serafini A, Boldrin F, Palu G, Manganelli R. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J Bacteriol 2009;191:6340-6344.
84. Prados-Rosales R, Weinrick BC, Pique DG, Jacobs WR Jr, Casadevall A, Rodriguez GM. Role for Mycobacterium tuberculosis membrane vesicles in iron acquisition. J Bacteriol 2014;196:1250-1256.
85. Owens CP, Du J, Dawson JH, Goulding CW. Characterization of heme ligation properties of Rv0203, a secreted heme binding protein involved in Mycobacterium tuberculosis heme uptake. Biochemistry 2012;51:1518-1531.
86. Owens CP, et al. The Mycobacterium tuberculosis secreted protein Rv0203 transfers heme to membrane proteins MmpL3 and MmpL11. J Biol Chem 2013;288:21714-21728.
87. Tahlan K, et al. SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis. Antimicrob Agents Chemother 2012;56:1797-1809.
88. Grzegorzewicz AE, et al. Inhibition of mycolic acid transport across the Mycobacterium tuberculosis plasma membrane. Nat Chem Biol 2012;8:334-341.
89. Cox JS, Chen B, McNeil M, Jacobs WR Jr. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 1999;402:79-83.
90. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 1999;34:257-267.
91. Converse SE, Mougous JD, Leavell MD, Leary JA, Bertozzi CR, Cox JS. MmpL8 is required for sulfolipid-1 biosynthesis and Mycobacterium tuberculosis virulence. Proc Natl Acad Sci USA 2003;100:6121-6126.
92. Milano A, et al. Azole resistance in Mycobacterium tuberculosis is mediated by the MmpS5-MmpL5 efflux system. Tuberculosis 2009;89:84-90.
93. Nambu S, Matsui T, Goulding CW, Takahashi S, Ikeda-Saito M. A new way to degrade heme: the Mycobacterium tuberculosis enzyme MhuD catalyzes heme degradation without generating CO. J Biol Chem 2013;288:10101-10109.
94. Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I. IdeR, an essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 2002;70:3371-3381.
95. Dussurget O, Rodriguez M, Smith I. An ideR mutant of Mycobacterium smegmatis has derepressed siderophore production and an altered oxidative-stress response. Mol Microbiol 1996;22:535-544.
96. Gold B, Rodriguez GM, Marras SA, Pentecost M, Smith I. The Mycobacterium tuberculosis IdeR is a dual functional regulator that controls transcription of genes involved in iron acquisition, iron storage and survival in macrophages. Mol Microbiol 2001;42:851-865.
97. Rodriguez GM, Smith I. Mechanisms of iron regulation in mycobacteria: role in physiology and virulence. Mol Microbiol 2003;47:1485-1494.
98. Pandey R, Rodriguez GM. IdeR is required for iron homeostasis and virulence in Mycobacterium tuberculosis. Mol Microbiol 2014;91:98-109.
99. Trousseau A. True and false chlorosis. Lectures on Clinical Medicine 1872;5:95-117.
100. Javaheri-Kermani M, Farazmandfar T, Ajami A, Yazdani Y. Impact of hepcidin antimicrobial peptide on iron overload in tuberculosis patients. Scand J Infect Dis 2014;46:693-696.
101. Isanaka S, et al. Iron status predicts treatment failure and mortality in tuberculosis patients: a prospective cohort study from Dar es Salaam, Tanzania. PLoS ONE 2012;7:e37350.
102. Olakanmi O, Schlesinger LS, Britigan BE. Hereditary hemochromatosis results in decreased iron acquisition and growth by Mycobacterium tuberculosis within human macrophages. J Leukoc Biol 2007;81:195-204.
103. Schaible UE, Collins HL, Priem F, Kaufmann SH. Correction of the iron overload defect in beta-2-microglobulin knockout mice by lactoferrin abolishes their increased susceptibility to tuberculosis. J Exp Med 2002;196:1507-1513.
104. Forbes JR, Gros P. Divalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 2001;9:397-403.
105. Soe-Lin S, et al. Nramp1 promotes efficient macrophage recycling of iron following erythrophagocytosis in vivo. Proc Natl Acad Sci USA 2009;106:5960-5965.
106. Jones CM, Niederweis M. Organ pathology in the absence of bacteria? J Infect Dis 2014;209:971.
107. de Voss JJ, Rutter K, Schroeder BG, Su H, Zhu Y, Barry CE 3rd. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc Natl Acad Sci USA 2000;97:1252-1257.
108. Reddy PV, et al. Disruption of mycobactin biosynthesis leads to attenuation of Mycobacterium tuberculosis for growth and virulence. J Infect Dis 2013;208:1255-1265.
109. Lisher JP, Giedroc DP. Manganese acquisition and homeostasis at the host-pathogen interface. Front Cell Infect Microbiol 2013;3:91.
110. Corbin BD, et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 2008;319:962-965.
111. Kehl-Fie TE, Skaar EP. Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 2010;14:218-224.
112. Kehl-Fie TE, et al. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 2011;10:158-164.
113. Kehl-Fie TE, et al. MntABC and MntH contribute to systemic Staphylococcus aureus infection by competing with calprotectin for nutrient manganese. Infect Immun 2013;81:3395-3405.
114. Gopal R, et al. S100A8/A9 proteins mediate neutrophilic inflammation and lung pathology during tuberculosis. Am J Respir Crit Care Med 2013;188:1137-1146.
115. Waldron KJ, Rutherford JC, Ford D, Robinson NJ. Metalloproteins and metal sensing. Nature 2009;460:823-830.
116. Zambelli B, Musiani F, Savini M, Tucker P, Ciurli S. Biochemical studies on Mycobacterium tuberculosis UreG and comparative modeling reveal structural and functional conservation among the bacterial UreG family. Biochemistry 2007;46:3171-3182.
117. Campbell DR, et al. Mycobacterial cells have dual nickel-cobalt sensors: sequence relationships and metal sites of metal-responsive repressors are not congruent. J Biol Chem 2007;282:32298-32310.
118. Gopinath K, Moosa A, Mizrahi V, Warner DF. Vitamin B(12) metabolism in Mycobacterium tuberculosis. Future Microbiol 2013;8:1405-1418.
119. Festa RA, Thiele DJ. Copper: an essential metal in biology. Curr Biol 2011;21:R877-R883.
120. Ekici S, et al. Intracytoplasmic copper homeostasis controls cytochrome c oxidase production. MBio 2014;5:e01055-01013.
121. Gennis R, Ferguson-Miller S. Structure of cytochrome c oxidase, energy generator of aerobic life. Science 1995;269:1063-1064.
122. Nies DH, Herzberg M. A fresh view of the cell biology of copper in enterobacteria. Mol Microbiol 2013;87:447-454.
123. Halliwell B, Gutteridge JM. Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 1984;219:1-14.
124. Macomber L, Rensing C, Imlay JA. Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 2007;189:1616-1626.
125. Macomber L, Imlay JA. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc Natl Acad Sci USA 2009;106:8344-8349.
126. Fung DK, Lau WY, Chan WT, Yan A. Copper efflux is induced during anaerobic amino acid limitation in Escherichia coli to protect iron-sulfur cluster enzymes and biogenesis. J Bacteriol 2013;195:4556-4568.
127. Chillappagari S, Seubert A, Trip H, Kuipers OP, Marahiel MA, Miethke M. Copper stress affects iron homeostasis by destabilizing iron-sulfur cluster formation in Bacillus subtilis. J Bacteriol 2010;192:2512-2524.
128. Ward SK, Hoye EA, Talaat AM. The global responses of Mycobacterium tuberculosis to physiological levels of copper. J Bacteriol 2008;190:2939-2946.
129. Hassett R, Kosman DJ. Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J Biol Chem 1995;270:128-134.
130. Ogra Y, Aoyama M, Suzuki KT. Protective role of metallothionein against copper depletion. Arch Biochem Biophys 2006;451:112-118.
131. Wang Y, Hodgkinson V, Zhu S, Weisman GA, Petris MJ. Advances in the understanding of mammalian copper transporters. Advances in nutrition 2011;2:129-137.
132. Maryon EB, Molloy SA, Kaplan JH. Cellular glutathione plays a key role in copper uptake mediated by human copper transporter 1. Am J Physiol Cell Physiol 2013;304:C768-C779.
133. Hatori Y, Clasen S, Hasan NM, Barry AN, Lutsenko S. Functional partnership of the copper export machinery and glutathione balance in human cells. J Biol Chem 2012;287:26678-26687.
134. Glerum DM, Shtanko A, Tzagoloff A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 1996;271:14504-14509.
135. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 1999;284:805-808.
136. Banci L, Bertini I, Ciofi-Baffoni S. Copper trafficking in biology: an NMR approach. HFSP J 2009;3:165-175.
137. Pufahl RA, et al. Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 1997;278:853-856.
138. Petris MJ, Mercer JFB. The Menkes protein (ATP7A; MNK) cycles via the plasma membrane both in basal and elevated extracellular copper using a C-terminal di-leucine endocytic signal. Hum Mol Genet 1999;8:2107-2115.
139. White C, Lee J, Kambe T, Fritsche K, Petris MJ. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J Biol Chem 2009;284:33949-33956.
140. Williams DM. Copper deficiency in humans. Semin Hematol 1983;20:118-128.
141. Babu U, Failla ML. Copper status and function of neutrophils are reversibly depressed in marginally and severely copper-deficient rats. J Nutr 1990;120:1700-1709.
142. Babu U, Failla ML. Respiratory burst and candidacidal activity of peritoneal macrophages are impaired in copper-deficient rats. J Nutr 1990;120:1692-1699.
143. Cordano A, Placko RP, Graham GG. Hypocupremia and neutropenia in copper deficiency. Blood 1966;28:280-283.
144. Achard ME, et al. Copper redistribution in murine macrophages in response to Salmonella infection. Biochem J 2012;444:51-57.
145. Samanovic MI, Ding C, Thiele DJ, Darwin KH. Copper in microbial pathogenesis: meddling with the metal. Cell Host Microbe 2012;11:106-115.
146. Hodgkinson V, Petris MJ. Copper homeostasis at the host-pathogen interface. J Biol Chem 2012;287:13549-13555.
147. Via LE, et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 2008;76:2333-2340.
148. Zimnicka AM, et al. Upregulated copper transporters in hypoxia-induced pulmonary hypertension. PLoS ONE 2014;9:e90544.
149. White C, et al. Copper transport into the secretory pathway is regulated by oxygen in macrophages. J Cell Sci 2009;122:1315-1321.
150. Sullivan JT, Young EF, McCann JR, Braunstein M. The Mycobacterium tuberculosis SecA2 system subverts phagosome maturation to promote growth in macrophages. Infect Immun 2012;80:996-1006.
151. 2+ signaling and phagosome maturation in human macrophages via specific inhibition of sphingosine kinase. J Immunol 2003;170:2811-2815.
152. Via LE, Deretic D, Ulmer RJ, Hibler NS, Huber LA, Deretic V. Arrest of mycobacterial phagosome maturation is caused by a block in vesicle fusion between stages controlled by rab5 and rab7. J Biol Chem 1997;272:13326-13331.
153. Kolonko M, Geffken AC, Blumer T, Hagens K, Schaible UE, Hagedorn M. WASH-driven actin polymerization is required for efficient mycobacterial phagosome maturation arrest. Cell Microbiol 2014;16:232-246.
154. Ward SK, Abomoelak B, Hoye EA, Steinberg H, Talaat AM. CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol Microbiol 2010;77:1096-1110.
155. Matsoso LG, et al. Function of the cytochrome bc1-aa3 branch of the respiratory network in mycobacteria and network adaptation occurring in response to its disruption. J Bacteriol 2005;187:6300-6308.
156. Megehee JA, Hosler JP, Lundrigan MD. Evidence for a cytochrome bcc-aa3 interaction in the respiratory chain of Mycobacterium smegmatis. Microbiology 2006;152:823-829.
157. Sassetti CM, Rubin EJ. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 2003;100:12989-12994.
158. Small JL, Park SW, Kana BD, Ioerger TR, Sacchettini JC, Ehrt S. Perturbation of cytochrome c maturation reveals adaptability of the respiratory chain in Mycobacterium tuberculosis. MBio 2013;4:e00475-00413.
159. Boshoff HI, Barry CE 3rd. Tuberculosis - metabolism and respiration in the absence of growth. Nat Rev Microbiol 2005;3:70-80.
160. Beswick PH, Hall GH, Hook AJ, Little K, McBrien DC, Lott KA. Copper toxicity: evidence for the conversion of cupric to cuprous copper in vivo under anaerobic conditions. Chem Biol Interact 1976;14:347-356.
161. Brennan PJ, Nikaido H. The envelope of mycobacteria. Annu Rev Biochem 1995;64:29-63.
162. Speer A, Rowland JL, Haeili M, Niederweis M, Wolschendorf F. Porins increase copper susceptibility of Mycobacterium tuberculosis. J Bacteriol 2013;195:5133-5140.
163. Novoa-Aponte L, et al. In silico identification and characterization of the ion transport specificity for P-type ATPases in the Mycobacterium tuberculosis complex. BMC Struct Biol 2012;12:25.
164. Siroy A, et al. Rv1698 of Mycobacterium tuberculosis represents a new class of channel-forming outer membrane proteins. J Biol Chem 2008;283:17827-17837.
165. Tsolaki AG, et al. Functional and evolutionary genomics of Mycobacterium tuberculosis: insights from genomic deletions in 100 strains. Proc Natl Acad Sci USA 2004;101:4865-4870.
166. Liu T, et al. CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat Chem Biol 2007;3:60-68.
167. Festa RA, et al. A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol Microbiol 2011;79:133-148.
168. Shi X, et al. The copper-responsive RicR regulon contributes to Mycobacterium tuberculosis virulence. MBio 2014;5:e00876-13.
169. Hasman H, Bjerrum MJ, Christiansen LE, Bruun Hansen HC, Aarestrup FM. The effect of pH and storage on copper speciation and bacterial growth in complex growth media. J Microbiol Methods 2009;78:20-24.
170. Burke CM, McVeigh I. Toxicity of copper to Escherichia coli in relation to incubation temperature and method of sterilization of media. Can J Microbiol 1967;13:1299-1309.
171. Kershaw CJ, Brown NL, Constantinidou C, Patel MD, Hobman JL. The expression profile of Escherichia coli K-12 in response to minimal, optimal and excess copper concentrations. Microbiology 2005;151:1187-1198.
172. Tree JJ, Kidd SP, Jennings MP, McEwan AG. Copper sensitivity of cueO mutants of Escherichia coli K-12 and the biochemical suppression of this phenotype. Biochem Biophys Res Commun 2005;328:1205-1210.
173. Speer A, et al. Copper-boosting compounds: a novel concept for antimycobacterial drug discovery. Antimicrob Agents Chemother 2013;57:1089-1091.
174. Wagner D, et al. 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 2005;174:1491-1500.
175. Rybicka JM, Balce DR, Chaudhuri S, Allan ER, Yates RM. Phagosomal proteolysis in dendritic cells is modulated by NADPH oxidase in a pH-independent manner. EMBO J 2012;31:932-944.
176. Rybicka JM, Balce DR, Khan MF, Krohn RM, Yates RM. NADPH oxidase activity controls phagosomal proteolysis in macrophages through modulation of the lumenal redox environment of phagosomes. Proc Natl Acad Sci USA 2010;107:10496-10501.
177. Stafford SL, et al. Metal ions in macrophage antimicrobial pathways: emerging roles for zinc and copper. Biosci Rep 2013;33:e00049.
178. McDevitt CA, et al. A molecular mechanism for bacterial susceptibility to zinc. PLoS Pathog 2011;7:e1002357.
179. Eijkelkamp BA, et al. Extracellular zinc competitively inhibits manganese uptake and compromises oxidative stress management in Streptococcus pneumoniae. PLoS ONE 2014;9:e89427.
180. Botella H, Stadthagen G, Lugo-Villarino G, de Chastellier C, Neyrolles O. Metallobiology of host-pathogen interactions: an intoxicating new insight. Trends Microbiol 2012;20:106-112.
181. Lichten LA, Cousins RJ. Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 2009;29:153-176.
182. Ballestin R, et al. Ethanol reduces zincosome formation in cultured astrocytes. Alcohol Alcohol 2011;46:17-25.
183. Beyersmann D, Haase H. Functions of zinc in signaling, proliferation and differentiation of mammalian cells. Biometals 2001;14:331-341.
184. Nies DH. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 2003;27:313-339.
185. Kulathila R, Indic M, van den Berg B. Crystal structure of Escherichia coli CusC, the outer membrane component of a heavy metal efflux pump. PLoS ONE 2011;6:e15610.
186. Su CC, Long F, Zimmermann MT, Rajashankar KR, Jernigan RL, Yu EW. Crystal structure of the CusBA heavy-metal efflux complex of Escherichia coli. Nature 2011;470:558-562.
187. Long F, Su CC, Lei HT, Bolla JR, Do SV, Yu EW. Structure and mechanism of the tripartite CusCBA heavy-metal efflux complex. Philos Trans R Soc Lond B Biol Sci 2012;367:1047-1058.
188. Cole ST, et al. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 1998;393:537-544.
189. Veyrier FJ, Boneca IG, Cellier MF, Taha MK. A novel metal transporter mediating manganese export (MntX) regulates the Mn to Fe intracellular ratio and Neisseria meningitidis virulence. PLoS Pathog 2011;7:e1002261.
190. 2+ transporter in Salmonella enterica serovar Typhimurium. J Bacteriol 2002;184:4369-4373.
191. Neyrolles O, Mintz E, Catty P. Zinc and copper toxicity in host defense against pathogens: Mycobacterium tuberculosis as a model example of an emerging paradigm. Front Cell Infect Microbiol 2013;3:89.
192. Fu Y, et al. A new structural paradigm in copper resistance in Streptococcus pneumoniae. Nat Chem Biol 2013;9:177-183.
193. Arguello JM. Identification of ion-selectivity determinants in heavy-metal transport P1B-type ATPases. J Membr Biol 2003;195:93-108.
194. Raimunda D, Long JE, Sassetti CM, Arguello JM. Role in metal homeostasis of CtpD, a Co(2+) transporting P(1B4) -ATPase of Mycobacterium smegmatis. Mol Microbiol 2012;84:1139-1149.
195. Raimunda D, Long JE, Padilla-Benavides T, Sassetti CM, Arguello JM. Differential roles for the Co(2+)/Ni(2+) transporting ATPases, CtpD and CtpJ, in Mycobacterium tuberculosis virulence. Mol Microbiol 2014;91:185-197.
196. Cavet JS, Meng W, Pennella MA, Appelhoff RJ, Giedroc DP, Robinson NJ. A nickel-cobalt-sensing ArsR-SmtB family repressor. Contributions of cytosol and effector binding sites to metal selectivity. J Biol Chem 2002;277:38441-38448.
197. Ward SK, Abomoelak B, Hoye EA, Steinberg H, Talaat AM. CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol Microbiol 2010;77:1096-1110.
198. 2+-transporting ATPase is required for secreted protein metallation in mycobacteria. J Biol Chem 2013;288:11334-11347.
199. Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 2012;10:525-537.
200. Sorkin E, Roth W, Erlenmeyer H. [Copper dependent bacteriostatic action]. Experientia 1951;7:64-65.
201. Krivis AF, Rabb JM. Cuprous complexes formed with isonicotinic hydrazide. Science 1969;164:1064-1065.
202. Xiao Z, Donnelly PS, Zimmermann M, Wedd AG. Transfer of copper between bis(thiosemicarbazone) ligands and intracellular copper-binding proteins. insights into mechanisms of copper uptake and hypoxia selectivity. Inorg Chem 2008;47:4338-4347.
203. Dearling JL, Lewis JS, Mullen GE, Rae MT, Zweit J, Blower PJ. Design of hypoxia-targeting radiopharmaceuticals: selective uptake of copper-64 complexes in hypoxic cells in vitro. Eur J Nucl Med 1998;25:788-792.
204. Vavere AL, Lewis JS. Cu-ATSM: a radiopharmaceutical for the PET imaging of hypoxia. Dalton Trans 2007;43:4893-4902.
205. Hung LW, et al. The hypoxia imaging agent CuII(atsm) is neuroprotective and improves motor and cognitive functions in multiple animal models of Parkinson's disease. J Exp Med 2012;209:837-854.
206. Haeili M, et al. Copper complexation screen reveals compounds with potent antibiotic properties against methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2014;58:3727-3736.
207. Djoko KY, Paterson BM, Donnelly PS, McEwan AG. Antimicrobial effects of copper(ii) bis(thiosemicarbazonato) complexes provide new insight into their biochemical mode of action. Metallomics 2014;6:854-863.
208. Emsley J. The Elements. 3rd edn. Oxford: Clarendon Press, 1998.
209. Nathan C. Fresh approaches to anti-infective therapies. Sci Transl Med 2012;4:140sr142.
210. Wagner D, et al. Changes of the phagosomal elemental concentrations by Mycobacterium tuberculosis Mramp. Microbiology 2005;151:323-332.