Redox Sensing by Fe2+ in Bacterial Fur Family Metalloregulators
Publication: Antioxidants & Redox Signaling
Volume 29, Issue Number 18
Abstract
Significance: Iron is required for growth and is often redox active under cytosolic conditions. As a result of its facile redox chemistry, iron homeostasis is intricately involved with oxidative stress. Bacterial adaptation to iron limitation and oxidative stress often involves ferric uptake regulator (Fur) proteins: a diverse set of divalent cation-dependent, DNA-binding proteins that vary widely in both metal selectivity and sensitivity to metal-catalyzed oxidation.
Recent Advances: Bacteria contain two Fur family metalloregulators that use ferrous iron (Fe2+) as their cofactor, Fur and PerR. Fur functions to regulate iron homeostasis in response to changes in intracellular levels of Fe2+. PerR also binds Fe2+, which enables metal-catalyzed protein oxidation as a mechanism for sensing hydrogen peroxide (H2O2).
Critical Issues: To effectively regulate iron homeostasis, Fur has an Fe2+ affinity tuned to monitor the labile iron pool of the cell and may be under selective pressure to minimize iron oxidation, which would otherwise lead to an inappropriate increase in iron uptake under oxidative stress conditions. Conversely, Fe2+ is bound more tightly to PerR but exhibits high H2O2 reactivity, which enables a rapid induction of peroxide stress genes.
Future Directions: The features that determine the disparate reactivity of these proteins with oxidants are still poorly understood. A controlled, comparative analysis of the affinities of Fur/PerR proteins for their metal cofactors and their rate of reactivity with H2O2, combined with structure/function analyses, will be needed to define the molecular mechanisms that have facilitated this divergence of function between these two paralogous regulators.
Get full access to this article
View all available purchase options and get full access to this article.
References
1.
Agriesti F, Roncarati D, Musiani F, Del Campo C, Iurlaro M, Sparla F, Ciurli S, Danielli A, and Scarlato V. FeON-FeOFF: the Helicobacter pylori Fur regulator commutates iron-responsive transcription by discriminative readout of opposed DNA grooves. Nucleic Acids Res 42: 3138–3151, 2014.
2.
Ahn BE and Baker TA. Oxidization without substrate unfolding triggers proteolysis of the peroxide-sensor, PerR. Proc Natl Acad Sci U S A 113: E23–E31, 2016.
3.
Ahn BE, Cha J, Lee EJ, Han AR, Thompson CJ, and Roe JH. Nur, a nickel-responsive regulator of the Fur family, regulates superoxide dismutases and nickel transport in Streptomyces coelicolor. Mol Microbiol 59: 1848–1858, 2006.
4.
Althaus EW, Outten CE, Olson KE, Cao H, and O'Halloran TV. The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38: 6559–6569, 1999.
5.
Anbar AD. Elements and evolution. Science 322: 1481–1483, 2008.
6.
Andrews SC, Robinson AK, and Rodriguez-Quinones F. Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215–237, 2003.
7.
Anjem A, Varghese S, and Imlay JA. Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72: 844–858, 2009.
8.
Antelmann H and Helmann JD. Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14: 1049–1063, 2011.
9.
Aslund F, Zheng M, Beckwith J, and Storz G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci U S A 96: 6161–6165, 1999.
10.
Bagg A and Neilands JB. 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, 1987.
11.
Bagg A and Neilands JB. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev 51: 509–518, 1987.
12.
Baichoo N and Helmann JD. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184: 5826–5832, 2002.
13.
Baichoo N, Wang T, Ye R, and Helmann JD. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol Microbiol 45: 1613–1629, 2002.
14.
Barford D. The role of cysteine residues as redox-sensitive regulatory switches. Curr Opin Struct Biol 14: 679–686, 2004.
15.
Bsat N and Helmann JD. Interaction of Bacillus subtilis Fur (ferric uptake repressor) with the dhb operator in vitro and in vivo. J Bacteriol 181: 4299–4307, 1999.
16.
Bsat N, Herbig A, Casillas-Martinez L, Setlow P, and Helmann JD. Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29: 189–198, 1998.
17.
Butcher J, Sarvan S, Brunzelle JS, Couture JF, and Stintzi A. Structure and regulon of Campylobacter jejuni ferric uptake regulator Fur define apo-Fur regulation. Proc Natl Acad Sci U S A 109: 10047–10052, 2012.
18.
Caux-Thang C, Parent A, Sethu R, Maiga A, Blondin G, Latour JM, and Duarte V. Single asparagine to arginine mutation allows PerR to switch from PerR box to fur box. ACS Chem Biol 10: 682–686, 2015.
19.
Chai S, Welch TJ, and Crosa JH. Characterization of the interaction between Fur and the iron transport promoter of the virulence plasmid in Vibrio anguillarum. J Biol Chem 273: 33841–33847, 1998.
20.
Chandrangsu P and Helmann JD. Intracellular Zn(II) intoxication leads to dysregulation of the PerR regulon resulting in heme toxicity in Bacillus subtilis. PLoS Genet 12: e1006515, 2016.
21.
Chen L and Helmann JD. Bacillus subtilis MrgA is a Dps(PexB) homologue: evidence for metalloregulation of an oxidative-stress gene. Mol Microbiol 18: 295–300, 1995.
22.
Chen L, Keramati L, and Helmann JD. Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc Natl Acad Sci U S A 92: 8190–8194, 1995.
23.
Chiancone E and Ceci P. The multifaceted capacity of Dps proteins to combat bacterial stress conditions: detoxification of iron and hydrogen peroxide and DNA binding. Biochim Biophys Acta 1800: 798–805, 2010.
24.
Cosgrove K, Coutts G, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, and Foster SJ. Catalase (KatA) and alkyl hydroperoxide reductase (AhpC) have compensatory roles in peroxide stress resistance and are required for survival, persistence, and nasal colonization in Staphylococcus aureus. J Bacteriol 189: 1025–1035, 2007.
25.
Coy M, Doyle C, Besser J, and Neilands JB. Site-directed mutagenesis of the ferric uptake regulation gene of Escherichia coli. Biometals 7: 292–298, 1994.
26.
Coy M and Neilands JB. Structural dynamics and functional domains of the Fur protein. Biochemistry 30: 8201–8210, 1991.
27.
D'Autreaux B, Horner O, Oddou JL, Jeandey C, Gambarelli S, Berthomieu C, Latour JM, and Michaud-Soret I. Spectroscopic description of the two nitrosyl-iron complexes responsible for fur inhibition by nitric oxide. J Am Chem Soc 126: 6005–6016, 2004.
28.
D'Autreaux B, Touati D, Bersch B, Latour JM, and Michaud-Soret I. Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. Proc Natl Acad Sci U S A 99: 16619–16624, 2002.
29.
de Lorenzo V, Giovannini F, Herrero M, and Neilands JB. Metal ion regulation of gene expression. Fur repressor-operator interaction at the promoter region of the aerobactin system of pColV-K30. J Mol Biol 203: 875–884, 1988.
30.
de Lorenzo V, Wee S, Herrero M, and Neilands JB. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (Fur) repressor. J Bacteriol 169: 2624–2630, 1987.
31.
Delany I, Spohn G, Rappuoli R, and Scarlato V. The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol Microbiol 42: 1297–1309, 2001.
32.
Deng Z, Wang Q, Liu Z, Zhang M, Machado AC, Chiu TP, Feng C, Zhang Q, Yu L, Qi L, Zheng J, Wang X, Huo X, Qi X, Li X, Wu W, Rohs R, Li Y, and Chen Z. Mechanistic insights into metal ion activation and operator recognition by the ferric uptake regulator. Nat Commun 6: 7642, 2015.
33.
Dian C, Vitale S, Leonard GA, Bahlawane C, Fauquant C, Leduc D, Muller C, de Reuse H, Michaud-Soret I, and Terradot L. The structure of the Helicobacter pylori ferric uptake regulator Fur reveals three functional metal binding sites. Mol Microbiol 79: 1260–1275, 2011.
34.
Duarte V and Latour JM. PerR vs OhrR: selective peroxide sensing in Bacillus subtilis. Mol Biosyst 6: 316–323, 2010.
35.
Escolar L, Perez-Martin J, and de Lorenzo V. Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223–6229, 1999.
36.
Fang FC. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2: 820–832, 2004.
37.
Faulkner MJ and Helmann JD. Peroxide stress elicits adaptive changes in bacterial metal ion homeostasis. Antioxid Redox Signal 15: 175–189, 2011.
38.
Faulkner MJ, Ma Z, Fuangthong M, and Helmann JD. Derepression of the Bacillus subtilis PerR peroxide stress response leads to iron deficiency. J Bacteriol 194: 1226–1235, 2012.
39.
Ferrer M, Golyshina OV, Beloqui A, Golyshin PN, and Timmis KN. The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated. Nature 445: 91–94, 2007.
40.
Fillat MF. The FUR (ferric uptake regulator) superfamily: diversity and versatility of key transcriptional regulators. Arch Biochem Biophys 546: 41–52, 2014.
41.
Frechon D and Le Cam E. Fur (ferric uptake regulation) protein interaction with target DNA: comparison of gel retardation, footprinting and electron microscopy analyses. Biochem Biophys Res Commun 201: 346–355, 1994.
42.
Fuangthong M and Helmann JD. Recognition of DNA by three ferric uptake regulator (Fur) homologs in Bacillus subtilis. J Bacteriol 185: 6348–6357, 2003.
43.
Fuangthong M, Herbig AF, Bsat N, and Helmann JD. Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J Bacteriol 184: 3276–3286, 2002.
44.
Gaballa A, Antelmann H, Aguilar C, Khakh SK, Song KB, Smaldone GT, and Helmann JD. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105: 11927–11932, 2008.
45.
Gaballa A and Helmann JD. Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180: 5815–5821, 1998.
46.
Gaballa A, MacLellan S, and Helmann JD. Transcription activation by the siderophore sensor Btr is mediated by ligand-dependent stimulation of promoter clearance. Nucleic Acids Res 40: 3585–3595, 2012.
47.
Gilston BA, Wang S, Marcus MD, Canalizo-Hernandez MA, Swindell EP, Xue Y, Mondragon A, and O'Halloran TV. Structural and mechanistic basis of zinc regulation across the E. coli Zur regulon. PLoS Biol 12: e1001987, 2014.
48.
Guan G, Pinochet-Barros A, Gaballa A, Patel SJ, Arguello JM, and Helmann JD. PfeT, a P1B4-type ATPase, effluxes ferrous iron and protects Bacillus subtilis against iron intoxication. Mol Microbiol 98: 787–803, 2015.
49.
Guerra AJ and Giedroc DP. Metal site occupancy and allosteric switching in bacterial metal sensor proteins. Arch Biochem Biophys 519: 210–222, 2012.
50.
Handley RA, Mulholland F, Reuter M, Ramachandran VK, Musk H, Clissold L, Le Brun NE, and van Vliet AH. PerR controls oxidative stress defence and aerotolerance but not motility-associated phenotypes of Campylobacter jejuni. Microbiology 161: 1524–1536, 2015.
51.
Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet 182: 288–292, 1981.
52.
Hantke K. Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: fur not only affects iron metabolism. Mol Gen Genet 210: 135–139, 1987.
53.
Hantke K. Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172–177, 2001.
54.
Helmann JD. Specificity of metal sensing: iron and manganese homeostasis in Bacillus subtilis. J Biol Chem 289: 28112–28120, 2014.
55.
Helmann JD, Wu MF, Gaballa A, Kobel PA, Morshedi MM, Fawcett P, and Paddon C. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J Bacteriol 185: 243–253, 2003.
56.
Herbig AF and Helmann JD. Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA. Mol Microbiol 41: 849–859, 2001.
57.
Hillmann F, Fischer RJ, Saint-Prix F, Girbal L, and Bahl H. PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum. Mol Microbiol 68: 848–860, 2008.
58.
Horsburgh MJ, Clements MO, Crossley H, Ingham E, and Foster SJ. PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect Immun 69: 3744–3754, 2001.
59.
Huang X, Shin JH, Pinochet-Barros A, Su TT, and Helmann JD. Bacillus subtilis MntR coordinates the transcriptional regulation of manganese uptake and efflux systems. Mol Microbiol 103: 253–268, 2017.
60.
Ikeda JS, Janakiraman A, Kehres DG, Maguire ME, and Slauch JM. Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J Bacteriol 187: 912–922, 2005.
61.
Ilari A, Ceci P, Ferrari D, Rossi GL, and Chiancone E. Iron incorporation into Escherichia coli Dps gives rise to a ferritin-like microcrystalline core. J Biol Chem 277: 37619–37623, 2002.
62.
Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol 57: 395–418, 2003.
63.
Imlay JA. The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443–454, 2013.
64.
Imlay JA. The mismetallation of enzymes during oxidative stress. J Biol Chem 289: 28121–28128, 2014.
65.
Jacquamet L, Dole F, Jeandey C, Oddou JL, Perret E, Le Pape L, Aberdam D, Hazemann JL, Michaud-Soret I, and Latour JM. First spectroscopic characterization of FeII-Fur, the physiological active form of the Fur protein. J Am Chem Soc 122: 394–395, 2000.
66.
Jacquamet L, Traore DA, Ferrer JL, Proux O, Testemale D, Hazemann JL, Nazarenko E, El Ghazouani A, Caux-Thang C, Duarte V, and Latour JM. Structural characterization of the active form of PerR: insights into the metal-induced activation of PerR and Fur proteins for DNA binding. Mol Microbiol 73: 20–31, 2009.
67.
Ji CJ, Kim JH, Won YB, Lee YE, Choi TW, Ju SY, Youn H, Helmann JD, and Lee JW. Staphylococcus aureus PerR is a hypersensitive hydrogen peroxide sensor using iron-mediated histidine oxidation. J Biol Chem 290: 20374–20386, 2015.
68.
Kim JH, Ji CJ, Ju SY, Yang YM, Ryu SH, Kwon Y, Won YB, Lee YE, Youn H, and Lee JW. Bacillus licheniformis contains two more PerR-like proteins in addition to PerR, Fur, and Zur Orthologues. PLoS One 11: e0155539, 2016.
69.
Kim JH, Won YB, Ji CJ, Yang YM, Ryu SH, Ju SY, Kwon Y, Lee YE, and Lee JW. The difference in in vivo sensitivity between Bacillus licheniformis PerR and Bacillus subtilis PerR is due to the different cellular environments. Biochem Biophys Res Commun 484: 125–131, 2017.
70.
Kim JH, Yang YM, Ji CJ, Ryu SH, Won YB, Ju SY, Kwon Y, Lee YE, Youn H, and Lee JW. The inability of Bacillus licheniformis perR mutant to grow is mainly due to the lack of PerR-mediated fur repression. J Microbiol 55: 457–463, 2017.
71.
Le Cam E, Frechon D, Barray M, Fourcade A, and Delain E. Observation of binding and polymerization of Fur repressor onto operator-containing DNA with electron and atomic force microscopes. Proc Natl Acad Sci U S A 91: 11816–11820, 1994.
72.
Lee JW and Helmann JD. Biochemical characterization of the structural Zn2+ site in the Bacillus subtilis peroxide sensor PerR. J Biol Chem 281: 23567–23578, 2006.
73.
Lee JW and Helmann JD. The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440: 363–367, 2006.
74.
Lee JW and Helmann JD. Functional specialization within the Fur family of metalloregulators. Biometals 20: 485–499, 2007.
75.
Lee JW, Soonsanga S, and Helmann JD. A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc Natl Acad Sci U S A 104: 8743–8748, 2007.
76.
Lewin AC, Doughty PA, Flegg L, Moore GR, and Spiro S. The ferric uptake regulator of Pseudomonas aeruginosa has no essential cysteine residues and does not contain a structural zinc ion. Microbiology 148: 2449–2456, 2002.
77.
Liu Y, Bauer SC, and Imlay JA. The YaaA protein of the Escherichia coli OxyR regulon lessens hydrogen peroxide toxicity by diminishing the amount of intracellular unincorporated iron. J Bacteriol 193: 2186–2196, 2011.
78.
Ma Z, Faulkner MJ, and Helmann JD. Origins of specificity and cross-talk in metal ion sensing by Bacillus subtilis Fur. Mol Microbiol 86: 1144–1155, 2012.
79.
Ma Z, Lee JW, and Helmann JD. Identification of altered function alleles that affect Bacillus subtilis PerR metal ion selectivity. Nucleic Acids Res 39: 5036–5044, 2011.
80.
Martin JE, Waters LS, Storz G, and Imlay JA. The Escherichia coli small protein MntS and exporter MntP optimize the intracellular concentration of manganese. PLoS Genet 11: e1004977, 2015.
81.
Masse E and Gottesman S. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99: 4620–4625, 2002.
82.
Masse E, Salvail H, Desnoyers G, and Arguin M. Small RNAs controlling iron metabolism. Curr Opin Microbiol 10: 140–145, 2007.
83.
Masse E, Vanderpool CK, and Gottesman S. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187: 6962–6971, 2005.
84.
Massey V. Activation of molecular oxygen by flavins and flavoproteins. J Biol Chem 269: 22459–22462, 1994.
85.
May JJ, Wendrich TM, and Marahiel MA. The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J Biol Chem 276: 7209–7217, 2001.
86.
McGuire AM, Cuthbert BJ, Ma Z, Grauer-Gray KD, Brunjes Brophy M, Spear KA, Soonsanga S, Kliegman JI, Griner SL, Helmann JD, and Glasfeld A. Roles of the A and C sites in the manganese-specific activation of MntR. Biochemistry 52: 701–713, 2013.
87.
Merchant SS and Helmann JD. Elemental economy: microbial strategies for optimizing growth in the face of nutrient limitation. Adv Microb Physiol 60: 91–210, 2012.
88.
Miethke M, Monteferrante CG, Marahiel MA, and van Dijl JM. The Bacillus subtilis EfeUOB transporter is essential for high-affinity acquisition of ferrous and ferric iron. Biochim Biophys Acta 1833: 2267–2278, 2013.
89.
Mills SA and Marletta MA. Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli. Biochemistry 44: 13553–13559, 2005.
90.
Moore CM, Gaballa A, Hui M, Ye RW, and Helmann JD. Genetic and physiological responses of Bacillus subtilis to metal ion stress. Mol Microbiol 57: 27–40, 2005.
91.
Moore CM and Helmann JD. Metal ion homeostasis in Bacillus subtilis. Curr Opin Microbiol 8: 188–195, 2005.
92.
Moore CM, Nakano MM, Wang T, Ye RW, and Helmann JD. Response of Bacillus subtilis to nitric oxide and the nitrosating agent sodium nitroprusside. J Bacteriol 186: 4655–4664, 2004.
93.
Mostertz J, Scharf C, Hecker M, and Homuth G. Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology 150: 497–512, 2004.
94.
Ollinger J, Song KB, Antelmann H, Hecker M, and Helmann JD. Role of the Fur regulon in iron transport in Bacillus subtilis. J Bacteriol 188: 3664–3673, 2006.
95.
Parent A, Caux-Thang C, Signor L, Clemancey M, Sethu R, Blondin G, Maldivi P, Duarte V, and Latour JM. Single glutamate to aspartate mutation makes ferric uptake regulator (Fur) as sensitive to H2O2 as peroxide resistance regulator (PerR). Angew Chem Int Ed Engl 52: 10339–10343, 2013.
96.
Que Q and Helmann JD. Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins. Mol Microbiol 35: 1454–1468, 2000.
97.
Schoffman H, Lis H, Shaked Y, and Keren N. Iron-Nutrient Interactions within Phytoplankton. Front Plant Sci 7: 1223, 2016.
98.
Schoneich C. Mechanisms of metal-catalyzed oxidation of histidine to 2-oxo-histidine in peptides and proteins. J Pharm Biomed Anal 21: 1093–1097, 2000.
99.
Seaver LC and Imlay JA. Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183: 7173–7181, 2001.
100.
Sethu R, Goure E, Signor L, Caux-Thang C, Clemancey M, Duarte V, and Latour JM. Reaction of PerR with molecular oxygen may assist H2O2 sensing in anaerobes. ACS Chem Biol 11: 1438–1444, 2016.
101.
Shin JH and Helmann JD. Molecular logic of the Zur-regulated zinc deprivation response in Bacillus subtilis. Nat Commun 7: 12612, 2016.
102.
Shin JH, Jung HJ, An YJ, Cho YB, Cha SS, and Roe JH. Graded expression of zinc-responsive genes through two regulatory zinc-binding sites in Zur. Proc Natl Acad Sci U S A 108: 5045–5050, 2011.
103.
Smaldone GT, Antelmann H, Gaballa A, and Helmann JD. The FsrA sRNA and FbpB protein mediate the iron-dependent induction of the Bacillus subtilis lutABC iron-sulfur-containing oxidases. J Bacteriol 194: 2586–2593, 2012.
104.
Sobota JM, Gu M, and Imlay JA. Intracellular hydrogen peroxide and superoxide poison 3-deoxy-D-arabinoheptulosonate 7-phosphate synthase, the first committed enzyme in the aromatic biosynthetic pathway of Escherichia coli. J Bacteriol 196: 1980–1991, 2014.
105.
Sobota JM and Imlay JA. 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 U S A 108: 5402–5407, 2011.
106.
Soonsanga S, Lee JW, and Helmann JD. Oxidant-dependent switching between reversible and sacrificial oxidation pathways for Bacillus subtilis OhrR. Mol Microbiol 68: 978–986, 2008.
107.
Toledano MB, Delaunay A, Monceau L, and Tacnet F. Microbial H2O2 sensors as archetypical redox signaling modules. Trends Biochem Sci 29: 351–357, 2004.
108.
Traore DA, El Ghazouani A, Ilango S, Dupuy J, Jacquamet L, Ferrer JL, Caux-Thang C, Duarte V, and Latour JM. Crystal structure of the apo-PerR-Zn protein from Bacillus subtilis. Mol Microbiol 61: 1211–1219, 2006.
109.
Traore DA, El Ghazouani A, Jacquamet L, Borel F, Ferrer JL, Lascoux D, Ravanat JL, Jaquinod M, Blondin G, Caux-Thang C, Duarte V, and Latour JM. Structural and functional characterization of 2-oxo-histidine in oxidized PerR protein. Nat Chem Biol 5: 53–59, 2009.
110.
Varghese S, Wu A, Park S, Imlay KR, and Imlay JA. Submicromolar hydrogen peroxide disrupts the ability of Fur protein to control free-iron levels in Escherichia coli. Mol Microbiol 64: 822–830, 2007.
111.
Vitale S, Fauquant C, Lascoux D, Schauer K, Saint-Pierre C, and Michaud-Soret I. A ZnS(4) structural zinc site in the Helicobacter pylori ferric uptake regulator. Biochemistry 48: 5582–5591, 2009.
112.
Waldron KJ and Robinson NJ. How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7: 25–35, 2009.
113.
Waldron KJ, Rutherford JC, Ford D, and Robinson NJ. Metalloproteins and metal sensing. Nature 460: 823–830, 2009.
114.
Wildschut JD, Caffrey SM, Voordouw JK, and Voordouw G. Oxygen exposure increases resistance of Desulfovibrio vulgaris Hildenborough to killing by hydrogen peroxide. Antonie Van Leeuwenhoek 101: 303–311, 2012.
115.
Zheleznova EE, Crosa JH, and Brennan RG. Characterization of the DNA- and metal-binding properties of Vibrio anguillarum Fur reveals conservation of a structural Zn(2+) ion. J Bacteriol 182: 6264–6267, 2000.
116.
Zheng M, Aslund F, and Storz G. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718–1721, 1998.
117.
Zheng M, Doan B, Schneider TD, and Storz G. OxyR and SoxRS regulation of fur. J Bacteriol 181: 4639–4643, 1999.
118.
Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, and Storz G. DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562–4570, 2001.
119.
Zuber P. Management of oxidative stress in Bacillus. Annu Rev Microbiol 63: 575–597, 2009.
Information & Authors
Information
Published In
Antioxidants & Redox Signaling
Volume 29 • Issue Number 18 • December 20, 2018
Pages: 1858 - 1871
PubMed: 28938859
Copyright
Copyright 2018, Mary Ann Liebert, Inc., publishers.
History
Published in print: December 20, 2018
Published online: 1 November 2018
Published ahead of print: 31 October 2017
Published ahead of production: 22 September 2017
Accepted: 9 September 2017
Received: 6 September 2017
Authors
Metrics & Citations
Metrics
Citations
Export Citation
Export citation
Select the format you want to export the citations of this publication.
View Options
Get Access
Access content
To read the fulltext, please use one of the options below to sign in or purchase access.⚠ Society Access
If you are a member of a society that has access to this content please log in via your society website and then return to this publication.