Analysis of a DtxR-like metalloregulatory protein, MntR, from Corynebacterium diphtheriae that controls expression of an ABC metal transporter by an Mn2+-dependent mechanism

Journal of Bacteriology

Volumn 184, Issue 24, 2002, Pages 6882-6892

  Schmitt, Michael P ^a,b  

^a Laboratory of Bacterial Toxins   (United States)

^b CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BETA GALACTOSIDASE; COPPER; DEOXYRIBONUCLEASE I; IRON; MANGANESE; METAL; METALLOPROTEIN; PROTEIN DTXR; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; CORYNEBACTERIUM DIPHTHERIAE; DNA FOOTPRINTING; GENE CONSTRUCT; GENE EXPRESSION; GENE FUNCTION; GENE FUSION; GENE IDENTIFICATION; GENE MUTATION; GENE REPRESSION; GENE STRUCTURE; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; WILD TYPE;

ATP-BINDING CASSETTE TRANSPORTERS; BACTERIAL PROTEINS; BASE SEQUENCE; CORYNEBACTERIUM DIPHTHERIAE; DNA; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MANGANESE; MOLECULAR SEQUENCE DATA; OPERON; PROMOTER REGIONS (GENETICS); REPETITIVE SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); CORYNEBACTERIUM; CORYNEBACTERIUM DIPHTHERIAE; PROKARYOTA; UNCULTURED ACTINOMYCETE;

EID: 0036947742     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.184.24.6882-6892.2002     Document Type: Article

References (55)

1. Altschul, S. F., G. Warren, W. Miller, E. W. Meyers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Bearden, S. W., and R. D. Perry. 1999. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32:403-414.
3. Boyd, J. M., O. N. Manish, and J. R. Murphy. 1990. Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae. Proc. Natl. Acad. Sci. USA 87:5968-5972.
4. Bsat, N., A. Herbig, L. Casillas-Martinez, P. Setlow, and J. D. Helmann. 1998. Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol. Microbiol. 29:189-198.
5. Claverys, J.-P. 2001. A new family of high-affinity ABC manganese and zinc permeases. Res. Microbiol. 152:231-243.
6. Ding, X., H. Zeng, N. Schiering, D. Ringe, and J. R. Murphy. 1996. Identification of the primary, metal ion-activation sites of the diphtheria tox repressor by X-ray crystallography and site-directed mutational analysis. Nat. Struct. Biol. 3:382-387.
7. Doukhan, L., M. Predich, G. Nair, O. Dussurget, I. Mandic-Mulec, and S. T. Cole. 1995. Genomic organization of the mycobacterial sigma gene cluster. Gene 165:67-70.
8. Drazek, E. S., C. A. Hammack, and M. P. Schmitt. 2000. Corynebacterium diphtheriae genes required for acquisition of iron from hemin and hemoglobin are homologous to ABC hemin transporters. Mol. Microbiol. 36:68-84.
9. Gold, B., G. M. Rodriguez, S. A. Marras, M. Pentecost, and I. Smith. 2001. The Mycobacterium tuberculosis IdeR is a dual functional regulator that controls transcription of genes involved in iron acquisition, iron storage and survival in macrophages. Mol. Microbiol. 42:851-865.
10. Groman, N., and K. Judge. 1979. Effect of metal ions on diphtheria toxin production. Infect. Immun. 26:1065-1070.
11. Gunter-Seeboth, K., and T. Schupp. 1995. Cloning and sequence analysis of the Corynebacterium diphtheriae dtxR homologue from Streptomyces lividans and S. pilosus encoding a putative iron repressor protein. Gene 166:117-119.
12. Hantke, K. 1984. Cloning of the repressor protein gene of iron regulated systems in Escherichia coli K-12. Mol. Gen. Genet. 197:337-341.
13. Haynes, J. A., and M. L. Britz. 1989. Electrotransformation of Brevibacterium lactofermentum and Corynebacterium glutamicum: growth in Tween 80 increases transformation frequencies. FEMS Microbiol. Lett. 61:329-334.
14. Holmes, R. K. 2000. Biology and molecular epidemiology of diphtheria toxin and the tox gene. 2000. J. Infect. Dis. 181:56-67.
15. + and tox bacteriophages of Corynebacterium diphtheriae. J. Virol. 3:586-598.
16. Horsburgh, M. J., E. Ingham, and S. J. Foster. 2001. In Staphylococcus aureus, Fur is an interactive regulator with PerR, contributes to virulence, and is necessary for oxidative stress resistance through positive regulation of catalase and iron homeostasis. J. Bacteriol. 183:468-475.
17. Horsburgh, M. J., S. J. Wharton, A. G. Cox, E. Ingham, S. Peacock, and S. J. Foster. 2002. MntR modulates expression of the PerR regulon and superoxide resistance in Staphylococcus aureus through control of manganese uptake. Mol. Microbiol. 44:1269-1286.
18. 2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR. Mol. Microbiol. 38:140-153.
19. Keen, C. L., B. Lonnerdal, and L. S. Hurley. 1984. Manganese, p. 89-132. In I. Frieden (ed.), Biochemistry of the essential ultratrace elements. Plenum Press, New York, N.Y.
20. 2+. J. Bacteriol. 184:3151-3158.
21. Kitten, T., C. L. Munro, S. M. Michalek, and F. L. Macrina. 2000. Genetic characterization of a Streptococcus mutans LraI family operon and role in virulence. Infect. Immun. 68:4441-4451.
22. 2+ uptake. J. Bacteriol. 180:290-295.
23. Lee, J. H., T. Wang, K. Ault, J. Liu, M. P. Schmitt, and R. K. Holmes. 1997. Identification and characterization of three new promoter/operators from Corynebacterium diphtheriae that are regulated by the diphtheria toxin repressor (DtxR) and iron. Infect. Immun. 65:4273-4280.
24. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
25. Pappenheimer, A. M., Jr. 1977. Diphtheria toxin. Annu. Rev. Biochem. 46:69-94.
26. 2+ transporter in Escherichia coli. J. Bacteriol. 183:4806-4813.
27. Pohl, E., R. K. Holmes, and W. G. Hol. 1999. Crystal structure of the iron-dependent regulator (IdeR) from Mycobacterium tuberculosis shows both metal binding sites fully occupied. J. Mol. Biol. 285:1145-1156.
28. Pohl, E., R. K. Holmes, and W. G. Hol. 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.
29. Posey, J. E., J. M. Hardham, S. J. Norris, and F. C. Gherardini. 1999. Characterization of a manganese-dependent regulatory protein, TroR, from Treponema pallidum. Proc. Natl. Acad. Sci. USA 96:10887-10892.
30. Qian, Y., J. H. Lee, and R. K. Holmes. 2002. Identification of a DtxR-regulated operon that is essential for siderophore-dependent iron uptake in Corynebacterium diphtheriae. J. Bacteriol. 184:4846-4856.
31. Qiu, X., L. M. Christophe, S. Zhang, M. P. Schmitt, R. K. Holmes, and W. G. Hol. 1995. Three-dimensional structure of the diphtheria repressor in complex with divalent cation co-repressor. Structure 3:87-100.
32. Que, Q., and J. D. Helmann. 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.
33. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
34. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
35. Schmitt, M. P. 1997. Utilization of host iron sources by Corynebacterium diphtheriae: identification of a gene whose product is homologous to eukaryotic heme oxygenase and is required for acquisition of iron from heme and hemoglobin. J. Bacteriol. 179:838-845.
36. Schmitt, M. P. 1997. Transcription of the Corynebacterium diphtheriae hmu O gene is regulated by iron and heme. Infect. Immun. 65:4634-4641.
37. Schmitt, M. P., and E. S. Drazek. 2001. Construction and consequences of directed mutations affecting the hemin receptor in pathogenic Corynebacterium species. J. Bacteriol. 183:1476-1481.
38. Schmitt, M. P., and R. K. Holmes. 1991. Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene dtxR in C. diphtheriae C7 strains. Infect. Immun. 59:1899-1904.
39. Schmitt, M. P., and R. K. Holmes. 1991. Characterization of a defective diphtheria toxin repressor (dtxR) allele and analysis of dtxR transcription in wild-type and mutant strains of Corynebacterium diphtheriae. Infect. Immun. 59:3903-3908.
40. Schmitt, M. P., and R. K. Holmes. 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. Schmitt, M. P., and R. K. Holmes. 1994. Cloning, sequence and footprint analysis of two promoter/operators from Corynebacterium diphtheriae that are regulated by the diphtheria toxin repressor and iron. J. Bacteriol. 176:1141-1149.
42. Schmitt, M. P., M. Predich, L. Doukhan, I. Smith, and R. K. Holmes. 1995. Characterization of an iron-dependent regulatory protein (IdeR) of Mycobacterium tuberculosis as a functional homolog of the diphtheria toxin repressor (DtxR) from Corynebacterium diphtheriae. Infect. Immun. 63:4284-4289.
43. Schmitt, M. P., E. M. Twiddy, and R. K. Holmes. 1992. Purification and characterization of the diphtheria toxin repressor. Proc. Natl. Acad. Sci. USA 89:7576-7580.
44. Serwold-Davis, T. M., N. B. Groman, and M. Rabin. 1987. Transformation of Corynebacterium diphtheriae, Corynebacterium ulcerans, Corynebacterium glutamicum, and Escherichia coli with the C. diphtheriae plasmid pNG2. Proc. Natl. Acad. Sci. USA 84:4964-4968.
45. Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendorff. 1990. Expression in E. coli: use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89.
46. Tai, S.-P. S., A. E. Krafft, P. Nootheti, and R. K. Holmes. 1990. Coordinate regulation of siderophore and diphtheria toxin production by iron in Corynebacterium diphtheriae. Microb. Pathog. 9:267-273.
47. Tao, X., and J. R. Murphy. 1992. Binding of the metalloregulatory protein DtxR to the diphtheria tox operator requires a divalent heavy metal ion and protects the palindromic sequence from DNase I digestion. J. Biol. Chem. 267:21761-21764.
48. Tao, X., and J. R. Murphy. 1994. Determination of the minimal essential nucleotide sequence for diphtheria tox repressor binding by in vitro affinity selection. Proc. Natl. Acad. Sci. USA 91:9646-9650.
49. Tao, X., S. Nikolaus, H. Zeng, D. Ringe, and J. R. Murphy. 1994. Iron, DtxR and the regulation of diphtheria toxin expression. Mol. Microbiol. 14:191-197.
50. Tayarani, I., I. Cloez, M. Clement, and J. M. Bourre. 1989. Antioxidant enzymes and related trace elements in aging brain capillaries and choroids plexus. J. Neurochem. 53:817-824.
51. Tseng, H.-J., A. G. McEwan, J. C. Paton, and M. P. Jennings. 2002. Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect. Immun. 70:1635-1639.
52. Vitek, R. C., and M. Wharton. 1998. Diphtheria in the former Soviet Union: reemergence of a pandemic disease. Emerg. Infect. Dis. 4:539-550.
53. Wang, G., G. P. Wylie, P. D. Twigg, D. L. Caspar, J. R. Murphy, and T. M. Logan. 1999. Solution structure and peptide binding studies of the C-terminal Src homology 3-like domain of the diphtheria toxin repressor protein. Proc. Natl. Acad. Sci. USA 96:6119-6124.
54. White, A., X. Ding, J. C. Vanderspek, J. R. Murphy, and D. Ringe. 1998. Structure of the metal-ion-activated diphtheria toxin repressor/tox operator complex. Nature 394:502-506.
55. Wilks, A., and M. P. Schmitt. 1998. Expression and characterization of a heme oxygenase (HmuO) from Corynebacterium diphtheriae. J. Biol. Chem. 273:837-841.