Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators

Molecular Microbiology

Volumn 48, Issue 2, 2003, Pages 495-506

  Guedon, Emmanuel ^a   Helmann, John D ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIPHTHERIA TOXIN; IRON; MANGANESE; METAL ION; MUTANT PROTEIN; PROTEIN DTXR; PROTEIN MNTR; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; CONTROLLED STUDY; CORYNEBACTERIUM DIPHTHERIAE; GENE EXPRESSION REGULATION; GENE MUTATION; HOMEOSTASIS; IRON TRANSPORT; METAL BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY;

ACTINOBACTERIA (CLASS); BACILLUS SUBTILIS; CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; POSIBACTERIA; UNCULTURED ACTINOMYCETE;

EID: 0038349048     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03445.x     Document Type: Article

References (50)

1. Baichoo, N., Wang, T., Ye, R., and Helmann, J.D. (2002) Global analysis of the Bacillus subtilis fur regulon and the iron starvation stimulon. Mol Microbiol 45; 1613-1629.
2. Bell, S.D., Cairns, S.S., Robson, R.L., and Jackson, S.P. (1999) Transcriptional regulation of an archaeal operon in vivo and in vitro. Mol Cell 4: 971-982.
3. Braun, V. (2001) Iron uptake mechanisms and their regulation in pathogenic bacte ria. Int J Med Microbiol 291: 67-79.
4. Bsat, N., and Helmann, J.D. (1999) Interaction of Bacillus subtilis Fur (ferric uptake repressor) with the dhb operator in vitro and in vivo. J Bacteriol 181: 4299-4307.
5. Bsat, N., Herbig, A., Casillas-Martinez, L., Setlow, P., and Helmann, J.D. (1998) Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29: 189-198.
6. Cavet, J.S., Meng, W., Pennella, M.A., Appelhoff, R.J., Giedroc, D.P., and Robinson, N.J. (2002) A nickel-cobalt sensing ArsR-SmtB family repressor: contributions of cytosol and effector binding sites to metal selectivity. J Biol Chem 277: 38441-38448.
7. Chen, C.S., White, A., Love, J., Murphy, J.R., and Ringe, D. (2000) Methyl groups of thymine bases are important for nucleic acid recognition by DtxR. Biochemistry 39: 10397-10407.
8. Cutting, S.M., and Vander Horn, P.B. (1990) Genetic Analysis. In Molecular Biological Methods for Bacillus. Harwood, C.R., and Cutting, S.M. (eds). Chichester: John Wiley and Sons, pp. 27-74.
9. Ding, X., Zeng, H., Schiering, N., Ringe, D., and Murphy, J.R. (1996) Identification of the primary metal ion-activation sites of the diphtheria tox repressor by X-ray crystallography and site-directed mutational analysis. Nature Struct Biol 3: 382-387.
10. Dussurget, O., Timm, J., Gomez, M., Gold, B., Yu, S., Sabol, S.Z., et al. (1999) Transcriptional control of the iron-responsive fxbA gene by the mycobacterial regulator IdeR. J Bacteriol 181: 3402-3408.
11. Escolar, L., Perez-Martin, J., and de Lorenzo, V. (1999) Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181: 6223-6229.
12. Feese, M.D., Ingason, B.P., Goranson-Siekierke, J., Holmes, R.K., and Hol, W.G. (2001) Crystal structure of the iron-dependent regulator from Mycobacterium tuberculosis at 2.0-A resolution reveals the Src homology domain 3-like fold and metal binding function of the third domain. J Biol Chem 276: 5959-5966.
13. Gaballa, A., and Helmann, J.D. (1998) Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis. J Bacteriol 180: 5815-5821.
14. Genco, C.A., and Dixon, D.W. (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39: 1-11.
15. Groman, N., and Judge, K. (1979) Effect of metal ions on diphtheria toxin production. Infect Immun 26: 1065-1070.
16. Guérout-Fleury, A.-M., Frandsen, N., and Stragier, P. (1996) Plasmids for ectopic integration in Bacillus subtilis. Gene 180: 57-61.
17. Hantke, K. (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172-177.
18. Herbig, A., and Helmann, J.D. (2002) Metal ion uptake and oxidative stress. In Bacillus Subtilis and its Closest Relatives. Sonenshein, A.L., Hoch, J.A., and Losick, R. (eds). Washington, DC: American Society for Microbiology Press, pp. 405-414.
19. Hill, P.J., Cockayne, A., Landers, P., Morrissey, J.A., Sims, C.M., and Williams, P. (1998) SirR, a novel iron-dependent repressor in Staphylococcus epidermidis. Infect Immun 66: 4123-4129.
20. Horsburgh, M.J., Wharton, S.J., Cox, A.G., Ingham, E., Peacock, S., and Foster, S.J. (2002) MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol Microbiol 44: 1269-1286.
21. Horton, R.M., Hunt, H.D., Ho, S.N., Pullen, J.K., and Pease, L.R. (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61-68.
22. Jakubovics, N.S., Smith, A.W., and Jenkinson, H.F. (2000) Expression of the virulence-related Sca (Mn2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol Microbiol 38: 140-153.
23. 2+. J Bacteriol 184: 3151-3158.
24. Keyer, K., and Imlay, J.A. (1996) Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci USA 93; 13635-13640.
25. May, J.J., Wendrich, T.M., and Marahiel, M.A. (2001) 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.
26. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory, pp. 352-355.
27. O'Halloran, T.V. (1993) Transition metals in control of gene expression. Science 261: 715-725.
28. Pappenheimer, A.M., Jr (1936) Studies in diphtheria toxin production. I. The effect of iron and copper. Br J Exp Pathol 17: 335-341.
29. 2+-MntR of the mntH gene, encoding an NRAMP-like Mn (2+) transporter in Escherichia coli. J Bacteriol 183: 4806-4813.
30. Pohl, E., Holmes, R.K., and Hol, W.G. (1999) Crystal structure of a cobalt-activated diphtheria toxin repressor-DNA complex reveals a metal-binding SH3-like domain. J Mol Biol 292: 653-667.
31. Posey, J.E., and Gherardini, F.C. (2000) Lack of a role for iron in the Lyme disease pathogen. Science 288: 1651-1653.
32. Posey, J.E., Hardham, J.M., Norris, S.J., and Gherardini, F.C. (1999) Characterization of a manganese-dependent regulatory protein, TroR, from Treponema pallidum. Proc Natl Acad Sci USA 96: 10887-10892.
33. Qian, Y., Lee, J.H., and Holmes, R.K. (2002) Identification of a DtxR-regulated operon that is essential for siderophore-dependent iron uptake in Corynebacterium diphtheriae. J Bacteriol 184: 4846-4856.
34. Que, Q., and Helmann, J.D. (2000) 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.
35. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
36. Rodriguez, G.M., Voskuil, M.I., Gold, B., Schoolnik, G.K., and Smith, I. (2002) ideR, An essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70: 3371-3381.
37. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Press.
38. Schmitt, M.P. (1999) Identification of a two-component signal transduction system from Corynebacterium diphtheriae that activates gene expression in response to the presence of heine and hemoglobin. J Bacteriol 181: 5330-5340.
39. Schmitt, M.P., and Holmes, R.K. (1991) Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene dtxR. C. diphtheriae C7 strains. Infect Immun 59: 1899-1904.
40. Schmitt, M.P., and Holmes, R.K. (1993) Analysis of diphtheria toxin repressor-operator interactions and characterization of a mutant repressor with decreased binding activity for divalent metals. Mol Microbiol 9: 173-181.
41. Slack, F.J., Mueller, J.P., and Sonenshein, A.L. (1993) Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon. J Bacteriol 175: 4605-4614.
42. Spatafora, G., Moore, M., Landgren, S., Stonehouse, E., and Michalek, S. (2001) Expression of Streptococcus mutans fimA is iron-responsive and regulated by a DtxR homologue. Microbiology 147: 1599-1610.
43. Tao, X., Boyd, J., and Murphy, J.R. (1992) Specific binding of the diphtheria tox regulatory element DtxR to the tox operator requires divalent heavy metal ions and a 9-base-pair interrupted palindromic sequence. Proc Natl Acad Sci USA 89: 5897-5901.
44. Tao, X., and Murphy, J.R. (1993) Cysteine-102 is positioned in the metal binding activation site of the Corynebacterium diphtheriae regulatory element DtxR. Proc Natl Acad Sci USA 90: 8524-8528.
45. Tao, X., Schiering, N., Zeng, H.-y., Ringe, D., and Murphy, J.R. (1994) Iron, DtxR, and the regulation of diphtheria toxin expression. Mol Microbiol 14: 191-197.
46. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
47. Vander Horn, P.B., and Zahler, S.A. (1992) Cloning and nucleotide sequence of the leucyl-tRNA synthetase gene of Bacillus subtilis. J Bacteriol 174: 3928-3935.
48. Vellanoweth, R.L., and Rabinowitz, J.C. (1992) The influence of ribosome-binding-site elements on translational efficiency in Bacillus subtilis and Escherichia coli. Mol Microbiol 6: 1105-1114.
49. White, A., Ding, X., vanderSpek, J.C., Murphy, J.R., and Ringe, D. (1998) Structure of the metal-ion-activated diphtheria toxin repressor/tox operator complex. Nature 394: 502-506.
50. Zuber, P., and Losick, R. (1987) Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis. J Bacteriol 169: 2223-2230.