The ins and outs of bacterial iron metabolism

Molecular Microbiology

Volumn 93, Issue 4, 2014, Pages 609-616

  Frawley, Elaine R ^a   Fang, Ferric C ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; HFE PROTEIN; IRON; IRON CITRATE EFFLUX TRANSPORTER PROTEIN; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SIDEROPHORE; STM3944 PROTEIN; TRANSITION ELEMENT; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; ELECTRON TRANSPORT; FENTON REACTION; HOST PATHOGEN INTERACTION; HUMAN; INTRACELLULAR BACTERIUM; IRON BALANCE; IRON CHELATION; IRON KINETICS; IRON METABOLISM; IRON OVERLOAD; IRON TRANSPORT; MYCOBACTERIUM TUBERCULOSIS; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; ANIMAL; HOMEOSTASIS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS;

BACTERIA (MICROORGANISMS); SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

ANIMALS; HOMEOSTASIS; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 84927786829     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12709     Document Type: Review

References (103)

1. Almiron, M., Link, A.J., Furlong, D., and Kolter, R. (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6: 2646-2654.
2. Altuvia, S., Almiron, M., Huisman, G., Kolter, R., and Storz, G. (1994) The dps promoter is activated by OxyR during growth and by IHF and sigma S in stationary phase. Mol Microbiol 13: 265-272.
3. Andreini, C., Bertini, I., Cavallaro, G., Holliday, G.L., and Thornton, J.M. (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13: 1205-1218.
4. Anjem, A., and Imlay, J.A. (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287: 15544-15556.
5. Atkinson, P.G., and Barton, C.H. (1999) High level expression of Nramp1G169 in RAW264.7 cell transfectants: analysis of intracellular iron transport. Immunology 96: 656-662.
6. Bagg, A., and Neilands, J.B. (1987) Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26: 5471-5477.
7. Baranova, N., and Nikaido, H. (2002) The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184: 4168-4176.
8. Barton, C.H., Biggs, T.E., Baker, S.T., Bowen, H., and Atkinson, P.G. (1999) Nramp1: a link between intracellular iron transport and innate resistance to intracellular pathogens. J Leukoc Biol 66: 757-762.
9. Baumgart, M., Mustafi, N., Krug, A., and Bott, M. (2011) Deletion of the aconitase gene in Corynebacterium glutamicum causes strong selection pressure for secondary mutations inactivating citrate synthase. J Bacteriol 193: 6864-6873.
10. Beck, G., Ellis, T.W., Habicht, G.S., Schluter, S.F., and Marchalonis, J.J. (2002) Evolution of the acute phase response: iron release by echinoderm (Asterias forbesi) coelomocytes, and cloning of an echinoderm ferritin molecule. Dev Comp Immunol 26: 11-26.
11. Beinert, H., Holm, R.H., and Munck, E. (1997) Iron-sulfur clusters: nature's modular, multipurpose structures. Science 277: 653-659.
12. Blackwell, J.M., and Searle, S. (1999) Genetic regulation of macrophage activation: understanding the function of Nramp1 (=Ity/Lsh/Bcg). Immunol Lett 65: 73-80.
13. Bleuel, C., Grosse, C., Taudte, N., Scherer, J., Wesenberg, D., Krauss, G.J., etal. (2005) TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J Bacteriol 187: 6701-6707.
14. Boyer, E., Bergevin, I., Malo, D., Gros, P., and Cellier, M.F. (2002) Acquisition of Mn(II) in addition to Fe(II) is required for full virulence of Salmonella enterica serovar Typhimurium. Infect Immun 70: 6032-6042.
15. Bullen, J.J., Spalding, P.B., Ward, C.G., and Gutteridge, J.M. (1991) Hemochromatosis, iron and septicemia caused by Vibrio vulnificus. Arch Intern Med 151: 1606-1609.
16. Cartron, M.L., Maddocks, S., Gillingham, P., Craven, C.J., and Andrews, S.C. (2006) Feo - transport of ferrous iron into bacteria. Biometals 19: 143-157.
17. Cassat, J.E., and Skaar, E.P. (2013) Iron in infection and immunity. Cell Host Microbe 13: 509-519.
18. Cellier, M.F., Courville, P., and Campion, C. (2007) Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9: 1662-1670.
19. Cerasi, M., Ammendola, S., and Battistoni, A. (2013) Competition for zinc binding in the host-pathogen interaction. Front Cell Infect Microbiol 3: 108.
20. Chao, Y., and Fu, D. (2004) Kinetic study of the antiport mechanism of an Escherichia coli zinc transporter, ZitB. J Biol Chem 279: 12043-12050.
21. Charlesworth, A., Georgieva, T., Gospodov, I., Law, J.H., Dunkov, B.C., Ralcheva, N., etal. (1997) Isolation and properties of Drosophila melanogaster ferritin - molecular cloning of a cDNA that encodes one subunit, and localization of the gene on the third chromosome. Eur J Biochem 247: 470-475.
22. Chen, O.S., Hemenway, S., and Kaplan, J. (2002) Genetic analysis of iron citrate toxicity in yeast: implications for mammalian iron homeostasis. Proc Natl Acad Sci USA 99: 16922-16927.
23. Crouch, M.L., Castor, M., Karlinsey, J.E., Kalhorn, T., and Fang, F.C. (2008) Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol Microbiol 67: 971-983.
24. D'Autreaux, B., Tucker, N.P., Dixon, R., and Spiro, S. (2005) A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437: 769-772.
25. Delmar, J.A., Su, C.C., and Yu, E.W. (2013) Structural mechanisms of heavy-metal extrusion by the Cus efflux system. Biometals 26: 593-607.
26. Diaz-Ochoa, V.E., Jellbauer, S., Klaus, S., and Raffatellu, M. (2014) Transition metal ions at the crossroads of mucosal immunity and microbial pathogenesis. Front Cell Infect Microbiol 4: 2.
27. Ernst, J.F., Bennett, R.L., and Rothfield, L.I. (1978) Constitutive expression of the iron- enterochelin and ferrichrome uptake systems in a mutant strain of Salmonella typhimurium. J Bacteriol 135: 928-934.
28. Farooq, M.A., Pracheil, T.M., Dong, Z., Xiao, F., and Liu, Z. (2013) Mitochondrial DNA instability in cells lacking aconitase correlates with iron citrate toxicity. Oxid Med Cell Longev 2013: 493536.
29. Felmy, B., Songhet, P., Slack, E.M., Muller, A.J., Kremer, M., Van Maele, L., etal. (2013) NADPH oxidase deficient mice develop colitis and bacteremia upon infection with normally avirulent, TTSS-1- and TTSS-2-deficient Salmonella Typhimurium. PLoS ONE 8: e77204.
30. Fink, R.C., Evans, M.R., Porwollik, S., Vazquez-Torres, A., Jones-Carson, J., Troxell, B., etal. (2007) FNR is a global regulator of virulence and anaerobic metabolism in Salmonella enterica serovar Typhimurium (ATCC 14028s). J Bacteriol 189: 2262-2273.
31. Fischbach, M.A., Lin, H., Liu, D.R., and Walsh, C.T. (2005) In vitro characterization of IroB, a pathogen-associated C-glycosyltransferase. Proc Natl Acad Sci USA 102: 571-576.
32. Fleming, R.E., Holden, C.C., Tomatsu, S., Waheed, A., Brunt, E.M., Britton, R.S., etal. (2001) Mouse strain differences determine severity of iron accumulation in Hfe knockout model of hereditary hemochromatosis. Proc Natl Acad Sci USA 98: 2707-2711.
33. Flo, T.H., Smith, K.D., Sato, S., Rodriguez, D.J., Holmes, M.A., Strong, R.K., etal. (2004) Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432: 917-921.
34. Frawley, E.R., Crouch, M.L., Bingham-Ramos, L.K., Robbins, H.F., Wang, W., Wright, G.D., and Fang, F.C. (2013) Iron and citrate export by a major facilitator superfamily pump regulates metabolism and stress resistance in Salmonella Typhimurium. Proc Natl Acad Sci USA 110: 12054-12059.
35. Fritsche, G., Nairz, M., Libby, S.J., Fang, F.C., and Weiss, G. (2012) Slc11a1 (Nramp1) impairs growth of Salmonella enterica serovar Typhimurium in macrophages via stimulation of lipocalin-2 expression. J Leukoc Biol 92: 353-359.
36. Furrer, J.L., Sanders, D.N., Hook-Barnard, I.G., and McIntosh, M.A. (2002) Export of the siderophore enterobactin in Escherichia coli: involvement of a 43kDa membrane exporter. Mol Microbiol 44: 1225-1234.
37. Ganz, T. (2013) Systemic iron homeostasis. Physiol Rev 93: 1721-1741.
38. Gort, A.S., and Imlay, J.A. (1998) Balance between endogenous superoxide stress and antioxidant defenses. J Bacteriol 180: 1402-1410.
39. Green, J., Trageser, M., Six, S., Unden, G., and Guest, J.R. (1991) Characterization of the FNR protein of Escherichia coli, an iron-binding transcriptional regulator. Proc Biol Sci 244: 137-144.
40. Gruer, M.J., Bradbury, A.J., and Guest, J.R. (1997) Construction and properties of aconitase mutants of Escherichia coli. Microbiology 143: 1837-1846.
41. Guilhen, C., Taha, M.K., and Veyrier, F.J. (2013) Role of transition metal exporters in virulence: the example of Neisseria meningitidis. Front Cell Infect Microbiol 3: 102.
42. Hantke, K. (1981) Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182: 288-292.
43. Hantke, K., Nicholson, G., Rabsch, W., and Winkelmann, G. (2003) 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.
44. Hidalgo, E., and Demple, B. (1994) An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J 13: 138-146.
45. Hoch, E., Lin, W., Chai, J., Hershfinkel, M., Fu, D., and Sekler, I. (2012) Histidine pairing at the metal transport site of mammalian ZnT transporters controls Zn2+ over Cd2+ selectivity. Proc Natl Acad Sci USA 109: 7202-7207.
46. Hood, M.I., and Skaar, E.P. (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10: 525-537.
47. Jang, S., and Imlay, J.A. (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem 282: 929-937.
48. Karlinsey, J.E., Bang, I.S., Becker, L.A., Frawley, E.R., Porwollik, S., Robbins, H.F., etal. (2012) The NsrR regulon in nitrosative stress resistance of Salmonella enterica serovar Typhimurium. Mol Microbiol 85: 1179-1193.
49. Keyer, K., and Imlay, J.A. (1996) Superoxide accelerates DNA damage by elevating free- iron levels. Proc Natl Acad Sci USA 93: 13635-13640.
50. Levy, J.E., Montross, L.K., Cohen, D.E., Fleming, M.D., and Andrews, N.C. (1999) The C282Y mutation causing hereditary hemochromatosis does not produce a null allele. Blood 94: 9-11.
51. Levy, J.E., Montross, L.K., and Andrews, N.C. (2000) Genes that modify the hemochromatosis phenotype in mice. J Clin Invest 105: 1209-1216.
52. Liesegang, H., Lemke, K., Siddiqui, R.A., and Schlegel, H.G. (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175: 767-778.
53. Long, F., Su, C.C., Lei, H.T., Bolla, J.R., Do, S.V., and Yu, E.W. (2012) Structure and mechanism of the tripartite CusCBA heavy-metal efflux complex. Philos Trans R Soc Lond B Biol Sci 367: 1047-1058.
54. Mahren, S., Schnell, H., and Braun, V. (2005) Occurrence and regulation of the ferric citrate transport system in Escherichia coli B, Klebsiella pneumoniae, Enterobacter aerogenes, and Photorhabdus luminescens. Arch Microbiol 184: 175-186.
55. Masse, E., and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99: 4620-4625.
56. Moalem, S., Weinberg, E.D., and Percy, M.E. (2004) Hemochromatosis and the enigma of misplaced iron: implications for infectious disease and survival. Biometals 17: 135-139.
57. Nairz, M., Fritsche, G., Crouch, M.L., Barton, H.C., Fang, F.C., and Weiss, G. (2009a) Slc11a1 limits intracellular growth of Salmonella enterica sv. Typhimurium by promoting macrophage immune effector functions and impairing bacterial iron acquisition. Cell Microbiol 11: 1365-1381.
58. Nairz, M., Theurl, I., Schroll, A., Theurl, M., Fritsche, G., Lindner, E., etal. (2009b) Absence of functional Hfe protects mice from invasive Salmonella enterica serovar Typhimurium infection via induction of lipocalin-2. Blood 114: 3642-3651.
59. Neilands, J.B. (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270: 26723-26726.
60. Nishino, K., Honda, T., and Yamaguchi, A. (2005) Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol 187: 1763-1772.
61. Olakanmi, O., Schlesinger, L.S., and Britigan, B.E. (2007) Hereditary hemochromatosis results in decreased iron acquisition and growth by Mycobacterium tuberculosis within human macrophages. J Leukoc Biol 81: 195-204.
62. Ong, D.S., Wang, L., Zhu, Y., Ho, B., and Ding, J.L. (2005) The response of ferritin to LPS and acute phase of Pseudomonas infection. J Endotoxin Res 11: 267-280.
63. Padilla-Benavides, T., George Thompson, A.M., McEvoy, M.M., and Arguello, J.M. (2014) Mechanism of ATPase-mediated Cu+ export and delivery to periplasmic chaperones: the interaction of Escherichia coli CopA and CusF. J Biol Chem. pii: jbc.M114.577668, epub ahead of print. doi:10.1074/jbc.M114.577668
64. Park, S., You, X., and Imlay, J.A. (2005) Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc Natl Acad Sci USA 102: 9317-9322.
65. Parkkila, S., Parkkila, A.K., Waheed, A., Britton, R.S., Zhou, X.Y., Fleming, R.E., etal. (2000) Cell surface expression of HFE protein in epithelial cells, macrophages, and monocytes. Haematologica 85: 340-345.
66. Patel, S.J., Padilla-Benavides, T., Collins, J.M., and Arguello, J.M. (2014) Functional diversity of five homologous Cu+-ATPases present in Sinorhizobium meliloti. Microbiology 160: 1237-1251.
67. Pomposiello, P.J., and Demple, B. (2000) Identification of SoxS-regulated genes in Salmonella enterica serovar Typhimurium. J Bacteriol 182: 23-29.
68. Puschmann, M., and Ganzoni, A.M. (1977) Increased resistance of iron-deficient mice to Salmonella infection. Infect Immun 17: 663-664.
69. Quenee, L.E., Hermanas, T.M., Ciletti, N., Louvel, H., Miller, N.C., Elli, D., etal. (2012) Hereditary hemochromatosis restores the virulence of plague vaccine strains. J Infect Dis 206: 1050-1058.
70. Raffatellu, M., George, M.D., Akiyama, Y., Hornsby, M.J., Nuccio, S.P., Paixao, T.A., etal. (2009) Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 5: 476-486.
71. 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 USA 94: 14326-14331.
72. Sawatzki, G., Hoffmann, F.A., and Kubanek, B. (1983) Acute iron overload in mice: pathogenesis of Salmonella typhimurium infection. Infect Immun 39: 659-665.
73. Schaible, U.E., and Kaufmann, S.H. (2005) A nutritive view on the host-pathogen interplay. Trends Microbiol 13: 373-380.
74. Schwartz, C.J., Giel, J.L., Patschkowski, T., Luther, C., Ruzicka, F.J., Beinert, H., and Kiley, P.J. (2001) IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc Natl Acad Sci USA 98: 14895-14900.
75. Seaver, L.C., and Imlay, J.A. (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183: 7182-7189.
76. Shiloh, M.U., MacMicking, J.D., Nicholson, S., Brause, J.E., Potter, S., Marino, M., etal. (1999) Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 10: 29-38.
77. Simonsen, K.T., Moller-Jensen, J., Kristensen, A.R., Andersen, J.S., Riddle, D.L., and Kallipolitis, B.H. (2011) Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2: 120-130.
78. Sobota, J.M., and Imlay, J.A. (2011) 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.
79. Stahler, F.N., Odenbreit, S., Haas, R., Wilrich, J., Van Vliet, A.H., Kusters, J.G., etal. (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.
80. Theurl, I., Fritsche, G., Ludwiczek, S., Garimorth, K., Bellmann-Weiler, R., and Weiss, G. (2005) The macrophage: a cellular factory at the interphase between iron and immunity for the control of infections. Biometals 18: 359-367.
81. Touati, D., Jacques, M., Tardat, B., Bouchard, L., and Despied, S. (1995) Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol 177: 2305-2314.
82. Tucker, N.P., Hicks, M.G., Clarke, T.A., Crack, J.C., Chandra, G., Le Brun, N.E., etal. (2008) The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS ONE 3: e3623.
83. Varghese, S., Tang, Y., and Imlay, J.A. (2003) Contrasting sensitivities of Escherichia coli aconitases A and B to oxidation and iron depletion. J Bacteriol 185: 221-230.
84. Velayudhan, J., Castor, M., Richardson, A., Main-Hester, K.L., and Fang, F.C. (2007) The role of ferritins in the physiology of Salmonella enterica sv. Typhimurium: a unique role for ferritin B in iron-sulphur cluster repair and virulence. Mol Microbiol 63: 1495-1507.
85. Velayudhan, J., Karlinsey, J.E., Frawley, E.R., Becker, L.A., Nartea, M., and Fang, F.C. (2014) Distinct Roles of the Salmonella enterica Serovar Typhimurium CyaY and YggX Proteins in the Biosynthesis and Repair of Iron-Sulfur Clusters. Infect Immun 82: 1390-1401.
86. Vidal, S., Gros, P., and Skamene, E. (1995a) Natural resistance to infection with intracellular parasites: molecular genetics identifies Nramp1 as the Bcg/Ity/Lsh locus. J Leukoc Biol 58: 382-390.
87. Vidal, S., Tremblay, M.L., Govoni, G., Gauthier, S., Sebastiani, G., Malo, D., etal. (1995b) The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J Exp Med 182: 655-666.
88. Viollier, P.H., Nguyen, K.T., Minas, W., Folcher, M., Dale, G.E., and Thompson, C.J. (2001) Roles of aconitase in growth, metabolism, and morphological differentiation of Streptomyces coelicolor. J Bacteriol 183: 3193-3203.
89. Wagegg, W., and Braun, V. (1981) Ferric citrate transport in Escherichia coli requires outer membrane receptor protein fecA. J Bacteriol 145: 156-163.
90. Waheed, A., Parkkila, S., Zhou, X.Y., Tomatsu, S., Tsuchihashi, Z., Feder, J.N., etal. (1997) Hereditary hemochromatosis: effects of C282Y and H63D mutations on association with beta2-microglobulin, intracellular processing, and cell surface expression of the HFE protein in COS-7 cells. Proc Natl Acad Sci USA 94: 12384-12389.
91. Waldron, K.J., Rutherford, J.C., Ford, D., and Robinson, N.J. (2009) Metalloproteins and metal sensing. Nature 460: 823-830.
92. Warszawska, J.M., Gawish, R., Sharif, O., Sigel, S., Doninger, B., Lakovits, K., etal. (2013) Lipocalin 2 deactivates macrophages and worsens pneumonia outcomes. J Clin Invest 123: 3363-3372.
93. Waters, L.S., Sandoval, M., and Storz, G. (2011) The Escherichia coli MntR miniregulon includes genes encoding a small protein and an efflux pump required for manganese homeostasis. J Bacteriol 193: 5887-5897.
94. Weinberg, E.D. (2000) Microbial pathogens with impaired ability to acquire host iron. Biometals 13: 85-89.
95. Weiss, G., and Schett, G. (2013) Anaemia in inflammatory rheumatic diseases. Nat Rev Rheumatol 9: 205-215.
96. Woodmansee, A.N., and Imlay, J.A. (2003) A mechanism by which nitric oxide accelerates the rate of oxidative DNA damage in Escherichia coli. Mol Microbiol 49: 11-22.
97. Worlock, A.J., and Smith, R.L. (2002) ZntB is a novel Zn2+ transporter in Salmonella enterica serovar Typhimurium. J Bacteriol 184: 4369-4373.
98. Wright, A.C., Simpson, L.M., and Oliver, J.D. (1981) Role of iron in the pathogenesis of Vibrio vulnificus infections. Infect Immun 34: 503-507.
99. Zaharik, M.L., Cullen, V.L., Fung, A.M., Libby, S.J., Kujat Choy, S.L., Coburn, B., etal. (2004) The Salmonella enterica serovar Typhimurium divalent cation transport systems MntH and SitABCD are essential for virulence in an Nramp1G169 murine typhoid model. Infect Immun 72: 5522-5525.
100. Zhao, G., Ceci, P., Ilari, A., Giangiacomo, L., Laue, T.M., Chiancone, E., and Chasteen, N.D. (2002) Iron and hydrogen peroxide detoxification properties of DNA-binding protein from starved cells. A ferritin-like DNA-binding protein of Escherichia coli. J Biol Chem 277: 27689-27696.
101. Zheng, M., Doan, B., Schneider, T.D., and Storz, G. (1999) OxyR and SoxRS regulation of fur. J Bacteriol 181: 4639-4643.
102. Zhou, D., Hardt, W.D., and Galan, J.E. (1999) Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun 67: 1974-1981.
103. Zhou, X.Y., Tomatsu, S., Fleming, R.E., Parkkila, S., Waheed, A., Jiang, J., etal. (1998) HFE gene knockout produces mouse model of hereditary hemochromatosis. Proc Natl Acad Sci USA 95: 2492-2497.