Transcriptional Response of Escherichia coli to TPEN - Journal of

Transcriptional Response of Escherichia coli to TPEN - Journal of

JOURNAL OF BACTERIOLOGY, Sept. 2006, p. 6709–6713 0021-9193/06/$08.00⫹0 doi:10.1128/JB.00680-06 Copyright © 2006, American Society for Microbiology. A...

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JOURNAL OF BACTERIOLOGY, Sept. 2006, p. 6709–6713 0021-9193/06/$08.00⫹0 doi:10.1128/JB.00680-06 Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Vol. 188, No. 18

Transcriptional Response of Escherichia coli to TPEN Tara K. Sigdel, J. Allen Easton, and Michael W. Crowder* Department of Chemistry and Biochemistry, 160 Hughes Hall, Miami University, Oxford, Ohio 45056 Received 12 May 2006/Accepted 4 July 2006

DNA microarrays were used to probe the transcriptional response of Escherichia coli to N, N, Nⴕ, Nⴕ-tetrakis(2pyridylmethyl)ethylenediamine (TPEN). Fifty-five transcripts were significantly up-regulated, including all of the genes that are regulated by Zur and many that are regulated by Fur. In the same TPEN-treated cells, 46 transcripts were significantly down-regulated. mented cultures are transcriptionally regulated by Fur, the iron uptake regulator (Table 1), and several are involved in Fe transport. The genes (entB, entA, entD, entE, and fes) which encode proteins involved with enterobactin synthesis and uptake (26, 29, 54) and the fec genes (fecR and fecI), which encode proteins involved in Fe import (23), were significantly up-regulated. Several other genes (fhuA, exbB, exbD, fhuD, fhuC, and fhuF) associated with ferrichrome transport in E. coli were also up-regulated (19, 56, 62). Forty-six transcripts were significantly down-regulated in E. coli cells stressed with TPEN (Table 2). Two operons in E. coli, flgBCDEFGHIJKL and flgAMN, possess genes that encode proteins involved in flagellar biosynthesis (8). Some of these motility-related genes, namely, flgB, fliM, and motB, were previously reported as being up-regulated in E. coli cells stressed with excess Zn(II) (51). In addition, the expression of flagellar biosynthetic proteins in E. coli is affected by the concentration of copper, possibly exerting its effect via the OmpR or H-NS transcriptional regulators (42). All of the genes in the cus and cue systems, which confer copper tolerance to E. coli (68), were also down-regulated, although cusA and copA were filtered out of the data shown in Table 2. Previous studies have demonstrated that the expression levels of the cus and cue genes are dependent on aerobic/anaerobic conditions as well as on the levels of copper in the periplasm/cytoplasm (68). The expression levels of cytoplasmic ferritin (3) were also significantly down-regulated in TPEN-treated cells. To validate the microarray data, two representative genes were selected for real-time PCR and assayed for the level of mRNA by a two-step, real-time PCR technique. The genes yodA and pdxH, which were up-regulated (21-fold) and exhibited no change (1.1-fold), respectively, were analyzed with realtime PCR. Real-time PCR results were as follows: yodA upregulated, 17 ⫾ 1; pdxH up-regulated, 1.1 ⫾ 0.1. In order to probe whether the changes observed in cells grown in the presence of TPEN were due to the chelator, RT-PCR was used to probe for the expression levels of yodA in E. coli cells grown in minimal medium containing 5 ␮M TPEN and 30 ␮M Zn(II). There was no change in transcript levels of yodA when E. coli was cultured in this medium. Despite the fact that TPEN is often referred to as a Zn(II)specific chelator (17, 33, 38, 48, 59, 64, 71, 79, 80, 83, 88), the analyses of our microarray data suggest that the levels of other metal ions may have been affected by the presence of TPEN.

* Corresponding author. Mailing address: Department of Chemistry and Biochemistry, 160 Hughes Hall, Miami University, Oxford, OH 45056. Phone: (513) 529-7274. Fax: (513) 529-5715. E-mail: crowdemw @muohio.edu. 6709

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The transcriptional response of Escherichia coli to elevated levels of metal ions such as Zn(II), Cd(II), Co(II), Ni(II), and Fe(II) has been probed in an effort to understand the mechanisms by which the homeostatic levels of these metal ions are maintained (10, 15, 51, 95, 96). In contrast, very few studies have probed the global response of E. coli to low levels of metal ions, presumably due to the difficulty of sufficiently depleting the growth medium of metal ions. In this study, cDNA microarrays were used to probe the transcriptional response of E. coli to stress by N, N, N⬘, N⬘-tetrakis(2-pyridylmethyl)ethylenediamine (TPEN). TPEN (58, 81), a cell-permeative, divalent metal chelator, is often called “Zn(II) specific” (17, 33, 38, 48, 59, 64, 71, 79, 80, 83, 88). Our data show significant changes in the transcription of several genes in cells stressed with TPEN. To identify genes that are differentially expressed in response to TPEN, E. coli BL21(DE3) cells were grown in minimal medium (76) until the cultures reached mid-log phase. TPEN was introduced, and the cells were cultured for 5 h; this time was chosen so that the results would correspond to previous transcriptional response studies with excess Zn(II) (51). The cultures containing 5 ␮M TPEN were analyzed with DNA microarrays (E. coli K12 V2 array slides from MWGBIOTECH), and the results were compared to those from E. coli cells grown in minimal medium containing no TPEN. A minimum of six slides was used for each experiment (three slides with one combination of Cy3 and Cy5 dyes and three slides with swapped dyes). Fifty-five transcripts were significantly up-regulated (twofold) (Table 1). Four genes (ykgM, znuA, znuC, and yodA) that are regulated by Zur, the Zn(II) uptake regulator (30), exhibited significant increases in expression. The remaining Zur-regulated transcript, znuB, was also up-regulated; however, this transcript did not meet our filtering criteria: (i) P values of ⱕ0.5, (ii) ⱖ2-fold changes in expression, and (iii) consistent data in all six slides. The expression of zntA, which is regulated by ZntR and encodes the high-affinity Zn(II) exporter in E. coli (7, 14, 78), was unchanged in E. coli cultures stressed with TPEN (see the complete set of DNA array data). Twenty-nine of the up-regulated genes from TPEN-supple-

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NOTES

J. BACTERIOL. TABLE 1. Genes up-regulated in E. coli cells stressed with TPEN IDa

Gene

Increase (fold)

P value

Zur regulated

B0296 B1973 B1857 B1858

ykgM yodA znuA znuC

23 21 7.6 2.2

5.5E-04 2.8E-03 1.5E-03 1.1E-02

Ribosomal protein; L31 paralog Cd(II) induced; putative Zn(II) transporter Periplasmic component of Zn(II)-specific ZnuABC transporter ATPase of ZnuABC

70 21, 75 73 73

Fur regulated

B2673 B2674 B0595 B0596 B0583 B3006 B3005 B0594 B1683 B1682

nrdH nrdI entB entA entD exbB exbD entE sufB sufC

12 12 9.7 8.7 7.2 5.8 5.3 5.1 5.1 5.1

1.9E-04 8.8E-03 2.4E-05 6.1E-03 1.0E-04 4.9E-04 1.3E-03 1.6E-02 3.6E-03 4.2E-03

39 39 26 91 26 34 34 26 69 69

B0151 B4292 B4293 B0585 B1102 B0150 B4367 B1679 B1252 B1681 B1680 B2676 B3908 B4290 B2155 B0153 B0592 B1132 B0586

fhuC fecR fecI fes fhuE fhuA fhuF sufE tonB ynhC sufS nrdF sodA fecB cirA fhuB fepB ycfC entF

5.1 4.9 4.8 4.5 4.4 4.3 2.10 2.01 3.9 3.9 3.7 3.1 3.0 3.0 2.9 2.9 2.7 2.6 2.4

1.1E-03 2.4E-03 4.5E-03 1.9E-02 3.4E-03 1.9E-03 4.7E-03 1.4E-03 5.2E-04 3.5E-03 6.7E-03 8.7E-04 2.0E-02 4.4E-02 3.3E-03 5.0E-02 2.2E-02 2.1E-02 2.5E-02

Glutaredoxin-like protein Stimulates NrdH 2,3-Dihydro-2,3-dihydroxybenzoate synthetase 2,3-Dihydro-2,3-dihydroxybenzoate dehydrogenase Enterochelin synthetase, component D Uptake of enterochelin; TonB-dependent uptake of b colicins Enterochelin synthetase, component d 2,3-Dihydroxybenzoate-AMP ligase Component of SufBCD cysteine desulfurase activator complex ATP-binding component of SufBCD cysteine desulfurase activator complex ATP-binding component of hydroxymate-dependent iron transport Regulator for fec operon, periplasmic Probable RNA polymerase sigma factor Enterochelin esterase Outer membrane receptor for ferric iron uptake Outer membrane protein receptor for ferrichrome, colicin m Ferrioxamine B reductase Cysteine desulfurase TonB Component of SufBCD cysteine desulfurase activator complex L-Selenocysteine lyase Subunit of ribonucleoside-diphosphate reductase II Mn superoxide dismutase Periplasmic component of iron dicitrate ABC transporter Outer membrane receptor for colicin I receptor Component of Fe(III) hydroxamate ABC transporter Fe(III) enterobactin ABC transporter Membrane protein in operon with purB Apo-serine activating enzyme

16 22 4 13 11 24 62 55 45 69 72 46 36 31 12 16 84 28 26

SoxRS regulated

B1611 B2962 B2963 B2237 B3924

fumC yggX mltC inaA fpr

3.8 3.2 2.6 2.2 2.1

2.6E-02 6.4E-03 4.6E-05 3.1E-03 4.8E-02

Class II fumarase Protects Fe-S clusters from oxidation Component of lytic murein transglycosylase C pH-inducible protein involved in stress response Flavodoxin NADP⫹ reductase

89 67 6 93 9

Other stress related

B0126 B1053 B0313 B1629 B4062 B1307

yadF yceE betI rsxC soxS pspD

3.7 2.5 2.4 2.1 2.1 2.0

6.9E-03 1.3E-03 5.9E-03 2.9E-02 7.3E-03 3.4E-02

Carbonic anhydrase Drug resistance protein Transcription repressor of bet genes Component of SoxR reducing complex Superoxide response regulon Phage shock protein

60 65 49 47 52 61

Anabolic processes

B1264 B3161 B1265 B2678 B0311 B4245 B2028 B1261 B3409 B1981 B0931

trpE mtr trpL proW betA pyrB ugd trpB feoB shiA pncB

5.3 2.9 2.7 2.6 2.6 2.6 2.4 2.3 2.3 2.3 2.0

3.7E-02 7.6E-04 3.1E-02 2.4E-02 3.1E-03 2.1E-02 3.1E-03 5.0E-02 1.7E-02 4.7E-02 7.3E-03

Anthranilate synthase component I Trp transport protein Trp operon leader peptide Pro and Gly betaine transporter Choline dehydrogenase Aspartate transcarbamoylase UDP-glucose-6-dehydrogenase Trp synthase ␤ Fe(II) transport protein Shikimate transporter Nicotinate phosphoribosyltransferase

20 32 43 5 77 41 85 44 40 92 94

Grouping

Reference

ID, identifier.

TPEN has been reported to bind Cd(II) (Kd ⫽ 4.7 ⫻ 10⫺17), Co(II) (Kd ⫽ 2.6 ⫻ 10⫺17), Ni(II) (Kd ⫽ 2.8 ⫻ 10⫺22), and Cu(II) (Kd ⫽ 2.9 ⫻ 10⫺21) more tightly than it binds Zn(II) (2). In addition, TPEN forms stable complexes with Fe(II) (Kd ⫽

2.5 ⫻ 10⫺15) (2). Since TPEN forms much tighter complexes with Cu(II), it is likely that the down-regulation of the copper homeostasis/export transcripts, cueO, copA, cusA, cusB, cusC, and cusF, is due to low levels of intracellular copper. Twenty-

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a

Description

VOL. 188, 2006

NOTES

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TABLE 2. Genes down-regulated in E. coli cells stressed with TPEN Decrease (fold)

P value

flgC flgD flgG flgI flgH flgF flgJ flgB flgA flgK flgM

7.9 7.5 4.9 4.3 4.0 3.9 3.9 3.8 3.4 3.1 2.3

3.1E-05 3.6E-04 1.2E-05 3.3E-04 8.7E-03 5.4E-05 2.8E-03 3.8E-04 4.7E-02 2.6E-02 3.6E-03

Cell-proximal portion of basal-body rod Initiator of hook assembly Cell-distal portion of basal-body rod p ring of flagellar basal body Outer membrane ring protein Cell-proximal portion of basal-body rod Flagellar protein Cell proximal portion of basal-body rod Assembly of basal-body p ring Hook filament junction protein Anti-flia factor

8 8 8 8 8 8 8 8 8 8 8

B2094 B2095 B2092 B2091 B2167 B2093 B2169 B2168 B2096 B4034 B3417 B1198 B1817

gatA gatZ gatC gatD fruA gatB fruB fruK gatY malE malP ycgC manX

6.4 5.3 4.9 4.7 4.0 3.7 3.5 3.2 2.6 2.4 2.3 2.3 2.1

5.9E-03 5.6E-03 2.7E-02 2.4E-03 2.2E-03 1.3E-02 3.1E-03 2.8E-02 1.7E-02 8.1E-03 5.0E-03 6.5E-03 1.5E-03

Enzyme IIa of PTS Putative tagatose 6-phosphate kinase Enzyme IIc of PTS Galactitol-1-phosphate dehydrogenase Fructose specific transporter Enzyme IIb of PTS Fructose specific IIa component Fructose 1-phosphate kinase Tagatose-bisphosphate aldolase Maltose binding protein Maltodextrin phosphorylase Dihydroxyacetone kinase M Mannose transporter

66 66 66 66 66 66 66 66 66 66 66 66 66

Fe and Cu metabolism

B1905 B0123 B0573 B0572 B0574

ftnA yacK ylcC ylcB ylcD

5.3 2.5 2.5 2.4 2.2

3.8E-04 2.7E-03 2.7E-03 2.0E-02 1.4E-02

Cytoplasmic ferritin CueO, Cu(I) oxidase CusF, copper efflux CusC, copper efflux CusB, copper efflux

82 27 27 27 27

Stress

B1656 B1379 B3687

sodB hslJ ibpA

3.7 2.3 2.1

2.0E-03 7.4E-03 4.7E-03

Fe superoxide dismutase Heat shock protein Heat shock protein

36 53 50

Metabolic proteins

B3936 B2142 B2286 B0972 B4116 B0411 B1380 B3209 B0651 B1245 B0872 B1241

rpmE yohK nuoC hyaA adiY tsx ldhA yhbL ybeK oppC hcr adhE

3.4 2.5 2.5 2.5 2.4 2.3 2.3 2.3 2.3 2.2 2.2 2.0

2.2E-02 3.0E-02 1.3E-02 4.8E-02 2.8E-02 2.8E-2 1.1E-02 1.8E-02 1.9E-2 7.2E-3 4.0E-02 2.1E-03

63 43 25 37 86 57 18 35 74 87 90 18

B1246 B2284

oppD nuoF

2.0 2.0

3.8E-02 7.0E-03

L31 ribosomal protein Serotonin transporter Component of NADH dehydrogenase Hydrogenase small subunit Transcription activator of Arg decarboxylase Nucleoside channel Lactate dehydrogenase Isoprenoid biosynthesis protein Ribonucleoside hydrolase ABC transporter for peptides NADH oxidoreductase Acetaldehyde dehydrogenase and Fe-dependent alcohol dehydrogenase ABC transporter for peptides NADH dehydrogenase

IDb

Flagellar biosynthesis

B1074 B1075 B1078 B1080 B1079 B1077 B1081 B1073 B1072 B1082 B1071

Sugar metabolism

a b

Gene

Descriptiona

Reference

87 25

PTS, phosphotransferase system. ID, identifier.

nine Fur-regulated transcripts were up-regulated. Despite the fact that Fe(II) binds 1 order of magnitude less tightly to TPEN than Zn(II) (2), it is possible that TPEN lowered the intracellular concentrations of Fe(II), resulting in the transcription of Fur-regulated iron uptake proteins. The reduction in intracellular concentrations of Fe(II) could be due to direct chelation by TPEN or by oxidation of intracellular Fe(II) to Fe(III). The fact that several other SoxRS-regulated transcripts were up-regulated in cultures stressed with TPEN (Table 1) suggests oxidative stress in these cells (97). It is also

possible that the reduction of intracellular Zn(II) caused by the presence of TPEN resulted in an improperly folded Fur, which requires one Zn(II) for proper structure/function (1). Taken together, these results strongly suggest that the intracellular levels of several metal ions in E. coli can be affected by TPEN, which indicates that caution should be exercised when TPEN is used in experiments to control intracellular concentrations of Zn(II) in cells. Microarray data accession number. The microarray data have been loaded into the Gene Expression Omnibus (GEO)

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Grouping

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NOTES

with the accession number GSE5356 (www.ncbi.nlm.nih.gov /geo). We thank Paul Christopher Wood and Maria Lia Molas from the Center for Bioinformatics and Functional Genomics (CBFG) for helping with the microarray scanner and real-time PCR experiments. We are also grateful to Herbert Auer, Director of the Affymetrix Core, Columbus Children’s Research Institute, for training and assistance in the analysis of cDNA microarray data. We acknowledge Miami University (Committee on Faculty Research and OARS) and the National Institutes of Health (GM079411) for funding this work.

22. Enz, S., H. Brand, C. Orellana, S. Mahren, and V. Braun. 2003. Sites of interaction between the FecA and FecR signal transduction proteins of ferric citrate transport in Escherichia coli K-12. J. Bacteriol. 185:3745–3752. 23. Enz, S., S. Mahren, C. Menzel, and V. Braun. 2003. Analysis of the ferric citrate transport gene promoter of Escherichia coli. J. Bacteriol. 185:2387– 2391. 24. Ferguson, A. D., E. Hofmann, J. W. Coulton, K. Diederichs, and W. Welte. 1998. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215–2220. 25. Friedrich, T. 1998. The NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli. Biochim. Biophys. Acta 1364:134–146. 26. Gehring, A. M., I. Mori, and C. T. Walsh. 1998. Reconstitution and characterization of the Escherichia coli enterobactin synthetase from EntB, EntE, and EntF. Biochemistry 37:2648–2659. 27. Grass, G., and C. Rensing. 2001. Genes involved in copper homeostasis in Escherichia coli. J. Bacteriol. 183:2145–2147. 28. Green, S. M., T. Malik, I. G. Giles, and W. T. Drabble. 1996. The purB gene of Escherichia coli K-12 is located in an operon. Microbiology 142:3219– 3230. 29. Hantash, F. M., M. Ammerlaan, and C. F. Earhart. 1997. Enterobactin synthase polypeptides of Escherichia coli are present in an osmotic-shocksensitive cytoplasmic locality. Microbiology 143:147–156. 30. Hantke, K. 2005. Bacterial zinc uptake and regulators. Curr. Opin. Microbiol. 8:196–202. 31. Harle, C., I. Kim, A. Angerer, and V. Braun. 1995. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 14:1430–1438. 32. Heatwole, V. M., and R. L. Somerville. 1991. The tryptophan-specific permease gene, mtr, is differentially regulated by the tryptophan and tyrosine repressors in Escherichia coli K-12. J. Bacteriol. 173:3601–3604. 33. Hegeman, C. E., M. L. Hayes, and M. R. Hanson. 2005. Substrate and cofactor requirements for RNA editing of chloroplast transcripts in Arabidopsis in vitro. Plant J. 42:124–132. 34. Held, K. G., and K. Postle. 2002. ExbB and ExbD do not function independently in TonB-dependent energy transduction. J. Bacteriol. 184:5170–5173. 35. Hemmi, H., S. Ohnuma, K. Nagaoka, and T. Nishino. 1998. Identification of genes affecting lycopene formation in Escherichia coli transformed with carotenoid biosynthetic genes: candidates for early genes in isoprenoid biosynthesis. J. Biochem. (Tokyo) 123:1088–1096. 36. Hopkin, K., M. Papazian, and H. Steinman. 1992. Functional differences between manganese and iron superoxide dismutases in Escherichia coli K-12. J. Biol. Chem. 267:24253–24258. 37. Hube, M., M. Blokesch, and A. Bock. 2002. Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybF. J. Bacteriol. 184:3879–3885. 38. Hyun, H. J., J. H. Sohn, D. W. Ha, Y. H. Ahn, J. Y. Koh, and Y. H. Yoon. 2001. Depletion of intracellular zinc and copper with TPEN results in apoptosis of cultured human retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 42:460–469. 39. Jordan, A., F. Aslund, E. Pontis, P. Reichard, and A. Holmgren. 1997. Characterization of Escherichia coli NrdH. A glutaredoxin-like protein with a thioredoxin-like activity profile. J. Biol. Chem. 272:18044–18050. 40. Kammler, M., C. Schon, and K. Hantke. 1993. Characterization of the ferrous iron uptake system of Escherichia coli. J. Bacteriol. 175:6212–6219. 41. Ke, H. M., R. B. Nonzatko, and W. N. Lipscomb. 1984. Structure of unligated aspartate carbamoyltransferase of Escherichia coli at 2.6 Å resolution. Proc. Natl. Acad. Sci. USA 81:4037–4040. 42. Kershaw, C. J., N. L. Brown, C. Constantinidou, M. D. Patel, and J. L. Hobman. 2005. The expression profile of Escherichia coli K-12 in response to minimal, optimal, and excess copper conditions. Microbiology 151:1187– 1198. 43. Keseler, I. M., J. Collado-Vides, S. Gama-Castro, J. Ingraham, S. Paley, I. T. Paulsen, M. Peralta-Gil, and P. D. Karp. 2005. EcoCyc: a comprehensive database resource for Escherichia coli. Nucleic Acids Res. 33:D334–D337. 44. Kirschner, K., A. N. Lane, and A. W. Strasser. 1991. Reciprocal communication between the lyase and synthase active sites of the tryptophan synthase bienzyme complex. Biochemistry 30:472–478. 45. Kodding, J., F. Killig, P. Polzer, S. P. Howard, K. Diederichs, and W. Welte. 2004. Crystal structure of a 92-residue C-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J. Biol. Chem. 280:3022–3028. 46. Kolberg, M., K. R. Strand, P. Graff, and K. K. Andersson. 2004. Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699:1–34. 47. Koo, M. S., J. H. Lee, S. Y. Rah, W. S. Yeo, J. W. Lee, K. L. Lee, Y. S. Koh, S. O. Kang, and J. H. Roe. 2003. A reducing system of the superoxide sensor SoxR in Escherichia coli. EMBO J. 22:2614–2622. 48. Kresse, W., I. Sekler, A. Hoffmann, O. Peters, C. Nolte, A. Moran, and H. Kettenmann. 2005. Zinc ions are endogenous modulators of neurotransmitter-stimulated capacitative Ca2⫹ entry in both cultured and in situ mouse astrocytes. Eur. J. Neurosci. 21:1626–1634. 49. Lamark, T., I. Kaasen, M. W. Eshoo, P. Falkenberg, J. McDougall, and A. R.

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REFERENCES 1. Althaus, E. W., C. E. Outten, K. E. Olson, H. Cao, and T. V. O’Halloran. 1999. The ferric uptake regulation (Fur) repressor is a zinc metalloprotein. Biochemistry 38:6559–6569. 2. Anderegg, G., E. Hubmann, N. G. Podder, and F. Wenk. 1977. Pyridinderivate als Komplexbildner. XI1. Die Thermodynamik der Metallkomplexbildung mit Bis-, Tris-, and Tetrakis[(2-pyridyl)methyl]-aminen. Helv. Chem. Acta 60:123–140. 3. Andrews, S. C. 1998. Iron storage in bacteria. Adv. Microb. Physiol. 40:281– 351. 4. Angerer, A., S. Enz, M. Ochs, and V. Braun. 1995. Transcriptional regulation of ferric citrate transport in Escherichia coli K-12. FecI belongs to a new subfamily of sigma 70-type factors that respond to extracytoplasmic stimuli. Mol. Microbiol. 18:163–174. 5. Barron, A., J. U. Jung, and M. Villarejo. 1987. Purification and characterization of a glycine betaine binding protein from Escherichia coli. J. Biol. Chem. 262:11841–11846. 6. Bateman, A., and M. Bycroft. 2000. The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J. Mol. Biol. 299:1113–1119. 7. Beard, S. J., R. Hashim, J. Membrillo-Hernandez, M. N. Hughes, and R. K. Poole. 1997. Zinc(II) tolerance in Escherichia coli K-12: evidence that the zntA gene (o732) encodes a cation transport ATPase. Mol. Microbiol. 25: 883–891. 8. Berg, H. C. 2003. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72:19–54. 9. Bianchi, V., P. Reichard, R. Eliasson, E. Pontis, M. Krook, H. Jornvall, and E. Haggard-Ljungquist. 1993. Escherichia coli ferredoxin NADP⫹ reductase: activation of E. coli anaerobic ribonucleotide reduction, cloning of the gene (fpr), and overexpression of the protein. J. Bacteriol. 175:1590–1595. 10. Binet, M. R., and R. K. Poole. 2000. Cd(II), Pb(II) and Zn(II) ions regulate expression of the metal-transporting P-type ATPase ZntA in Escherichia coli. FEBS Lett. 473:67–70. 11. Bitter, W., I. S. van Leeuwen, J. de Boer, H. W. Zomer, M. C. Koster, P. J. Weisbeek, and J. Tommaseen. 1994. Localization of functional domains in the Escherichia coli coprogen receptor FhuE and the Pseudomonas putida ferric-pseudobactin 358 receptor PupA. Mol. Gen. Genet. 245:694–703. 12. Braun, V., S. I. Patzer, and K. Hantke. 2002. Ton-dependent colicins and microcins: modular design and evolution. Biochimie 84:365–380. 13. Brickman, T., and M. McIntosh. 1992. Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J. Biol. Chem. 267: 12350–12355. 14. Brocklehurst, K. R., J. L. Hobman, B. Lawley, L. Blank, S. J. Marshall, N. L. Brown, and A. P. Morby. 1999. ZntR is a Zn(II)-responsive MerR-like transcriptional regulator of zntA in Escherichia coli. Mol. Microbiol. 31:893– 902. 15. Brocklehurst, K. R., and A. P. Morby. 2000. Metal-ion tolerance in Escherichia coli: analysis of transcriptional profiles by gene-array technology. Microbiology 146:2277–2282. 16. Burkhardt, R., and V. Braun. 1987. Nucleotide sequence of the fhuC and fhuD genes involved in iron(III) hydroxamate transport: domains in FhuC homologous to ATP-binding proteins. Mol. Gen. Genet. 209:49–55. 17. Chimienti, F., M. Seve, S. Richard, J. Mathieu, and A. Favier. 2001. Role of cellular zinc in programmed cell death: temporal relationship between zinc depletion, activation of caspases, and cleavage of Sp family transcription factors. Biochem. Pharmacol. 62:51–62. 18. Clark, D. P. 1989. The fermentation pathways of Escherichia coli. FEMS Microbiol. Rev. 5:223–234. 19. Coulton, J. W., P. Mason, and D. D. Allatt. 1987. fhuC and fhuD genes for iron(III)-ferrichrome transport into Escherichia coli K-12. J. Bacteriol. 169: 3844–3849. 20. Crawford, I. P. 1989. Evolution of a biosynthetic pathway: the tryptophan paradigm. Annu. Rev. Microbiol. 43:567–600. 21. David, G., K. Blondeau, M. Schiltz, S. Penel, and A. Lewit-Bentley. 2003. YodA from Escherichia coli is a metal-binding, lipocalin-like protein. J. Biol. Chem. 278:43728–43735.

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