Submicromolar hydrogen peroxide disrupts the ability of fur protein to control free-iron levels in Escherichia coli

Molecular Microbiology

Volumn 64, Issue 3, 2007, Pages 822-830

  Varghese, Shery ^a   Wu, Amy ^a   Park, Sunny ^a   Imlay, Karin R C ^a   Imlay, James A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHELATING AGENT; HYDROGEN PEROXIDE; IRON;

ARTICLE; BACTERIAL STRAIN; BACTERIOSTASIS; BINDING SITE; CELL STRESS; ENVIRONMENT; ESCHERICHIA COLI; EVOLUTION; FENTON REACTION; IRON TRANSPORT; MUTAGENESIS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REGULON; UPREGULATION;

BACTERIAL PROTEINS; BLOTTING, NORTHERN; DNA-BINDING PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN PEROXIDE; HYDROXYL RADICAL; IRON; MUTAGENESIS; MUTATION; PEROXIDASES; REGULON; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ESCHERICHIA COLI; LURIA;

EID: 34247472147     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05701.x     Document Type: Article

References (41)

1. Almiron, M., Link, A.J., Furlong, D. Kolter, R. (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6 : 2646 2654.
2. Aslund, F., Zheng, M., Beckwith, J. Storz, G. (1999) Regulation of the OxyR transcriptional factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96 : 6161 6165.
3. Bagg, A. Neilands, J.B. (1985) Mapping of a mutation affecting regulation of iron uptake systems in Escherichia coli K-12. J Bacteriol 161 : 450 453.
4. Beauchamp, C. Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44 : 276 287.
5. Braun, V. (2003) Iron uptake by Escherichia coli. Front Biosci 1 : s1409 s1421.
6. Brown, N.M., Kennedy, M.C., Antholine, W.E., Eisenstein, R.S. Walden, W.E. (2002) Detection of a "3Fe-4S" cluster intermediate of cytosolic aconitase in yeast expressing iron regulatory protein 1. Insights into the mechanism of Fe-S cluster cycling. J Biol Chem 277 : 7246 7254.
7. Cairo, G., Recalcati, S., Pietrangelo, A. Minotti, G. (2002) The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage. Free Radic Biol Med 32 : 1237 1243.
8. Carlioz, A. Touati, D. (1986) Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5 : 623 630.
9. Compan, I. Touati, D. (1993) Interaction of six global transcription regulators in expression of manganese superoxide dismutase in Escherichia coli K-12. J Bacteriol 175 : 1687 1696.
10. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
11. Ding, H. Demple, B. (1997) In vivo kinetics of a redox-regulated transcriptional switch. Proc Natl Acad Sci USA 94 : 8445 8449.
12. Djaman, O., Outten, F.W. Imlay, J.A. (2004) Repair of oxidized iron-sulfur clusters in Escherichia coli. J Biol Chem 279 : 44590 44599.
13. Escolar, L., Perez-Martin, J. de Lorenzo, V. (1999) Opening the iron box; transcriptional metalloregulation by the Fur protein. J Bacteriol 181 : 6223 6229.
14. Gaudu, P., Moon, N. Weiss, B. (1997) Regulation of the soxRS oxidative stress regulon. Reversible oxidation of the Fe-S center of SoxR in vivo. J Biol Chem 272 : 5082 5086.
15. Geissmann, T.A. Touati, D. (2004) Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 23 : 396 405.
16. Grogan, D.W. Cronan, J.E. (1984) Genetic characterization of the Escherichia coli cyclopropane fatty acid (cfa) locus and neighboring loci. Mol Gen Genet 196 : 367 372.
17. Halliwell, B. Gutteridge, J.M.C. (1990) Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 186 : 1 85.
18. Hassan, H.M. Fridovich, I. (1977) Regulation of the synthesis of superoxide dismutase in Escherichia coli. Induction by methyl viologen. J Biol Chem 252 : 7667 7672.
19. Hassan, H.M. Sun, H.C.H. (1992) Regulatory roles of Fnr, Fur, and Arc in expression of manganese-containing superoxide dismutase in Escherichia coli. Proc Natl Acad Sci USA 89 : 3217 3221.
20. Imlay, J.A. (2003) Pathways of oxidative damage. Ann Rev Microbiol 57 : 395 418.
21. Imlay, J.A. Fridovich, I. (1991) Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266 : 6957 6965.
22. Imlay, J.A., Chin, S.M. Linn, S. (1988) Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 240 : 640 642.
23. Jang, S. Imlay, J.A. (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron-sulfur enzymes. J Biol Chem 282 : 929 937.
24. Lee, J.W. Helmann, J.D. (2006) The PerR transcription factor senses H2O2 by metal-catalyzed histidine oxidation. Nature 440 : 363 367.
25. McCord, J.M. Fridovich, I. (1969) Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244 : 6049 6055.
26. Manchado, M., Michan, C. Pueyo, C. (2000) Hydrogen peroxide activates the SoxRS regulon in vivo. J Bacteriol 182 : 6842 6844.
27. Masse, E. 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.
28. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
29. Park, S., You, X. 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.
30. Privalle, C.T. Fridovich, I. (1988) Inductions of superoxide dismutases in Escherichia coli under anaerobic conditions. Accumulation of an inactive form of the manganese enzyme. J Biol Chem 263 : 4274 4279.
31. Rush, J.D., Maskos, Z. Koppenol, W.H. (1990) Distinction between hydroxyl radical and ferryl species. Methods Enzymol 186 : 148.
32. Seaver, L.C. Imlay, J.A. (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183 : 7182 7189.
33. Seaver, L.C. Imlay, J.A. (2004) Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem 279 : 48742 48750.
34. Tsaneva, I.R. Weiss, B. (1990) soxR, a locus governing a superoxide response regulon in Escherichia coli K-12. J Bact 172 : 4197 4205.
35. Walling, C. (1975) Fenton's reagent revisited. Accounts Chem Res 8 : 125 131.
36. Wiener, M.C. (2005) TonB-dependent outer membrane transport: going for Baroque? Curr Opin Struct Biol 15 : 294 400.
37. Woodmansee, A.L. Imlay, J.A. (2002) Quantitation of intracellular free iron by electron paramagnetic resonance spectroscopy. Methods Enzymol 349 : 3 9.
38. Zhao, G., Ceci, P., Ilari, A., Giangiacomo, L., Laue, T.M., Chiancone, E. 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.
39. Zheng, M., Doan, B., Schneider, T.D. Storz, G. (1999) OxyR and SoxRS regulation of. Fur J Bacteriol 181 : 4639 4643.
40. Zheng, M., Wang, X., Doan, B., Lewis, K.A., Schneider, T.D. Storz, G. (2001a) Computation-directed identification of OxyR DNA binding sites in Escherichia coli. J Bacteriol 183 : 4571 4579.
41. Zheng, M., Wang, X., Templeton, L.J., Smulski, D.R., LaRossa, R.A. Storz, G. (2001b) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183 : 4562 4570.