Ferritin mutants of Escherichia coli are iron deficient and growth impaired, and fur mutants are iron deficient

Journal of Bacteriology

Volumn 181, Issue 5, 1999, Pages 1415-1428

  Abdul Tehrani, Hossein ^a   Hudson, Aaron J ^a   Chang, Yung Sheng ^b   Timms, Andrew R ^a,c   Hawkins, Chris ^a   Williams, John M ^a   Harrison, Pauline M ^a   Guest, John R ^a   Andrews, Simon C ^b  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF READING   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FERRITIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; ESCHERICHIA COLI; GROWTH INHIBITION; IRON METABOLISM; NONHUMAN; PRIORITY JOURNAL;

ESCHERICHIA COLI;

EID: 0033025239     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.5.1415-1428.1999     Document Type: Article

References (62)

1. Andrews, S. C. 1998. Iron storage in bacteria. Adv. Microb. Physiol. 40:281-351.
2. Andrews, S. C., P. M. Harrison, and J. R. Guest. 1989. Cloning, sequencing, and mapping of the bacterioferritin gene (bfr) of Encherichia cali K-12. J. liacteriol. 171:3940-3947.
3. Andrews, S. C., N. E. Le Brun, V. Barynin, A. J. Thomson, G. R. Moore, J. R. Guest, and P. M. Harrison. 1995. Site-directed replacement of the coaxial heme ligands of bacterioferritin generates heme-free variants. J. Biol. Chem. 270:23268-23274.
4. Andrews, S. C., J. M. A. Smith, C. Hawkins, J. M. Williams, P. M. Harrison, and J. R. Guest. 1993. Overproduction, purification and characterisation of the bacterioferritin of Escherichia coli and a C-terminally extended variant. Eur. J. Biochem. 213:329-338.
5. Bagg, A., and J. B. Neilands. 1987. Ferric uptake regulation protein acts as a repressor. employing iron(II) as co-factor to bind the operator of an iron transport operon in Escherichia coli. Biochemistry 26:5471-5477.
6. Balla, G., H. S. Jacob, J. Balla, M. Rosenberg, K. Nath, F. Apple, J. W. Eaton and G. M. Vercellotti. 1992. Ferritin - a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem. 267:18148-18153.
7. Bauminger, E. R., S. G. Cohen, D. P. E. Dickson, A. Levy, S. Ofer, and J. Yariv. 1980. Mössbauer spectroscopy of Escherichia coli and its iron-storage protein. Biochim. Biophys. Acta 163:237-242.
8. Berlyn, M. B., K. B. Low, and K. E. Rudd. 1996. Linkage map of Escherichia coli K-12, edition 9, p. 1715-1902. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasarik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. G. Umbarger (ed.), Escherichia coli and Salmanella: cellular and molecular biology. 2nd ed. ASM Press, Washington, D.C.
9. Bishop, R. 1997. Iron metabolism in Escherichia coli. M. Phil. thesis. University of Sheffield, Sheffield, United Kingdom.
10. Blattner, F. R., G. Plunkett, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado Vides, J. D. Glasner, C. K. Rode, G. F. Mayhe, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao, 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
11. Bolann, B. J., and R. J. Ulvik. 1990. On the limited ability of superoxide to release iron from ferritin. Eur. J. Biochem. 193:899-904.
12. Carrano, C. J., R. Bohnke, and B. Matzanke. 1996. The ferritin from mycelia of Absidia spinosa is a bacterioferritin. FEBS Lett. 390:261-264.
13. Chambers, S. P., S. E. Prior, D. A. Barstow, and N. P. Minton. 1988. The MTL nic cloning vectors. I. Improved pUC polylinker regions to facilitate the use of sonicated DNA for nucleotide sequencing. Gene 68:139-149.
14. Cozzi, A., P. Santambrogio, S. Levi, and P. Arosio. 1990. Irondetoxification activity of ferritin. Effects of H and L human apoferritins on lipid peroxiadtion in vitro. FEBS Lett. 227:119-122.
15. 1, from Escherichia coli. J. Biol. Chem. 239:1024-1031.
16. Denoel, P. A., R. M. Crawford, M. S. Zygmunt, A. Tibor, V. E. Weynants, F. Godfroid, D. L. Hoover, and J.-J. Letesson. 1997. Survival of a bacterioferritin deletion mutant of Brucella melitensis 16M in human monocyte-derived macrophages. Infect. Immun. 65:4337-4340.
17. 14C-labelled amino acids. J. Bacteriol. 95: 851-857.
18. Earhart, C. F. 1996. Uptake and metabolism of iron and molybdenum, p. 1075-1090. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasarik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed. ASM Press, Washington, D.C.
19. Ferreira, F., and N. A. Straus. 1994. Iron deprivation in cyanobacteria. J. Appl. Phycol. 6:199-210.
20. Foster, J. W., and H. K. Hall. 1992. Effect of Salmonella typhimurium ferric uptake regulator (fur) mutations on iron-and pH-regulated protein synthesis. J. Bacteriol. 174:4317-4323.
21. Frolow, F., A. J. Kalb, and J. Yariv. 1994. Structure of a unique twofold symetric baem-binding site. Nat. Stuct. Biol. 7:453-460.
22. Gannon, D. E., J. Varani, S. H. Phan, J. H. Ward, J. Kaplan, G. O. Till, R. H. Simon, U. S. Ryan, and P. A. Ward. 1987. Source of iron in neutrophilmediated killing of endothelial cells. Lab. Investig. 57:37-44.
23. Garg, R. P., C. J. Vargo, X. Y. Cui, and D. M. Kurtz, Jr. 1996. A [2Fe-2S] protein encoded by an open reading frame upstream of the Escherichia coli bacterioferritin gene. Biochemistry 35:6297-6301.
24. Grogan, J. M. 1997. Regulation and function of the genes encoding bacterioferritin (Bfr) and Bfr-associatcd ferredoxin (Bfd) of E. coli. Ph.D. thesis. University of Sheffield. Sheffield, United Kingdom.
25. Gruer, M. J., and J. R. Guest. 1994. Two genetically-distinct and differentially regulated aconitases (acnA and acnB) in Escherichia coli. Microbiology 140:2531-2541.
26. Halliwell, B., and J. M. C. Gutteridge. 1986. Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch. Biochem. Biophys. 246:501-514.
27. Hamilton, C. M., M. Aldea, B. K. Washburn, P. Babitzke, and S. R. Kushner. 1989. New method for generating deletions and gene replacements in Escherichia coli. J. Bacteriol. 171:4617-4622.
28. Hantke, K. 1981. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol. Gen. Genet. 182:288-292.
29. Harrison, P. M., and P. Arosio. 1996. The ferritins: molecular properties, iron storage function and cellular regulation. Biochim. Biophys. Act a 1275: 161-203.
30. Harrison, P. M., P. D. Hempstead, P. J. Artymiuk, and S. C. Andrews. 1998. Structure-function relationships in the ferritins. Metal Ions Biol. Syst. 35: 435-477.
31. Hartmann, A., and V. Braun. 1981. Iron uptake and iron limited growth of Escherichia coli K-12. Arch. Microbiol. 130:353-356.
32. Hempstead, P. D., A. J. Hudson, P. J. Artymiuk, S. C. Andrews, M. J. Banfield, J. R. Guest, and P. M. Harrison. 1994. First direct observation of the iron-binding sites in ferritin. FEBS Lett. 350:258-262.
33. Hudson, A. J., S. C. Andrews, C. Hawkins, J. M. Williams, M. Izuhara, F. C. Meldrura, S. Mann, P. M. Harrison, and J. R. Guest. 1993. Overexpression, purification and characterization of the Escherichia coli ferritin. Eur. J. Biochem. 218:985-995.
34. Izuhara, M., K. Takamune, and R. Takata. 1991. Cloning and sequencing of an Escherichia coli K12 gene which encodes a polypeptide having similarity to the human ferritin H subunit. Mol. Gen. Genet. 225:510-513.
35. Keyer, K., and J. A. Imlay. 1996. Superoxide accelerates DNA-damage by elevating free-iron levels. Proc. Natl. Acad. Sci. USA 193:13635-13640.
36. Kunkel, T. A. 1985. Rapid and effcient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA 82:488-492.
37. Marmur, J. 1964. A procedure for the isolation of deoxyribonucleic acid from microorganisms. Methods Enzymol. 6:726-739.
38. Mello Fihlo, A. C., M. E. Hoffman, and R. Meneghini. 1984. Cell killing and DNA damage by hydrogen peroxide are mediated by intracellular iron Bioehem. J. 218:273-275.
39. Messing, J. 1983. New M13 vectors for cloning. Methods Enzymol. 101:20-78.
40. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N.Y.
41. Minakami, H., J. W. Kitzler, and I. Fridovich. 1990. Effects of pH, glucose, and chelating agents on lethality of paraquat to Escherichia coli. J. Bacteriol. 172:691-695.
42. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
43. Niederhoffer, E. C., C. M. Naranjo, K. L. Bradley, and J. A. Fee. 1990. Control of Escherichia coli superoxide sidmuatase (sodA and sodB) genes by the ferric iron uptake regulation (fur) locus. J. Bacteriol. 172:1930-1938.
44. Park, S. J., and R. P. Gunsalus. 1995. Oxygen, iron, carbon, and superoxide control of the fumarase fumA and fumC genes of Escherichia coli - role of the arcA. fur, and soxR gene products. J. Bacteriol. 177:6255-6262.
45. Prentki, P. and H. M. Krisch. 1984. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303-313.
46. Pugsley, A. P., and P. Reeves. 1976. Characterization of group B colicin-resistant mutants of Escherichia coli K-12: colicin resistance and the role of enterochelin. J. Bacteriol. 127:218-228.
47. Quail, M. A., P. Jordan, J. M. Grogan, J. N. Butt, M. Lutz, A. J. Thomson, S. C. Andrews, and J. R. Guest. 1996. Spectroscopic and voltammetric characterisation of the bacterioferritin-associated ferredoxin of Escherichia coli. Biochem. Biophys. Res. Commun. 229:635-642.
48. Razquin, P., S. Schmitz, M. F. Fillat, M. L. Peleato, and H. Bohme. 1994. Transcriptional and translational analysis of ferredoxin and flavodoxin under iron and nitrogen stress in Anabaena sp strain PCC 7120. J. Bacteriol. 176: 7409-7411.
49. Repine, J. E., R. B. Fox, and E. M. Berger. 1981. Hydrogen peroxide kills Staphylococcus aureus by reacting with Staphylococcal iron to form hydroxyl radicals. J. Biol. Chem. 256:7094-7096.
50. Rouf, M. A. 1964. Spectrochemical analysis of inorganic elements in bacteria. J. Bacteriol. 88:1545-1549.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
52. Sanger, F., A. R. Coulson, B. G. Barrell, A. J. H. Smith, and B. A. Roc. 1980. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J. Mol. Biol. 143:161-178.
53. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984 Experiments with gene fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
54. 557.5 is a bacterioferritin. Nature 279:81-83.
55. Stojiljkovic, I., A. J. Bäumler, and K. Hantke. 1994. Fur regulon in gramnegative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay. J. Mol. Biol. 236:531-545.
56. Theil, E. C. 1987. Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu. Rev. Biochem. 56:289-315.
57. Touati, D., M. Jacques, B. Tardat, L. Bouchard, and S. Despied. 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.
58. Tseng, C.-P. 1997. Regulation of fumarase (fumB) gene expression in Escherichia coli in response to oxygen, iron and heme availability: role of the arcA, fur, and hemA gene products. FEMS Microbiol. Lett. 157:67-72.
59. Vogel, H. J., and D. M. Bonner. 1955. Acetylornithinase of Escherichia coli: partial purification and some properties. J. Biol. Chem. 218:97-106.
60. Wai, S. N., K. Nakayama, K. Umene, T. Moriya, and K. Amako. 1996. Construction of a ferritin-deficient mutant of Campylobacter jejuni - contribution of ferritin to iron storage and protection against oxidative stress. Mol. Microbiol. 20:1127-1134.
61. 1 involvement in the functioning of lac-permease in respiring Escherichia coli. J. Theor. Biol. 182: 459-462.
62. Zigler, J. S., H. M. Jernigan, D. Garland, and V. N. Reddy. 1985. The effects of oxygen radicals generated in the medium on lenses in organ culture-inhibition of damage by chelated iron. Arch. Biochem. Biophys. 241:163-172.