Metal binding studies and EPR spectroscopy of the manganese transport regulator MntR

Biochemistry

Volumn 45, Issue 51, 2006, Pages 15359-15372

  Golynskiy, Misha V ^a   Gunderson, William A ^b   Hendrich, Michael P ^b   Cohen, Seth M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MANGANESE HOMEOSTASIS; MANGANESE TRANSPORT REGULATOR (MNTR); METAL BINDING AFFINITIES; METAL ION CONCENTRATIONS;

CHEMICAL BONDS; CONCENTRATION (PROCESS); DNA; ELECTRON SPIN RESONANCE SPECTROSCOPY; MANGANESE;

BACTERIA;

BACTERIAL PROTEIN; CADMIUM; COBALT; DIPHTHERIA TOXIN REPRESSOR; DYE; FURA 2; FURAPTRA; MANGANESE; MANGANESE TRANSPORT REGULATOR; NICKEL; PROTEIN ANTR; TRANSCRIPTION FACTOR; TRANSITION ELEMENT; UNCLASSIFIED DRUG; ZINC;

ARTICLE; BACILLUS ANTHRACIS; BACILLUS SUBTILIS; BINDING AFFINITY; BINDING COMPETITION; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CRYSTAL STRUCTURE; ELECTRON SPIN RESONANCE; HOMEOSTASIS; ION TRANSPORT; METAL BINDING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FAMILY; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; STOICHIOMETRY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; CADMIUM; CATIONS, DIVALENT; DNA-BINDING PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; MANGANESE; PROTEIN BINDING; REPRESSOR PROTEINS;

BACILLUS ANTHRACIS; BACILLUS SUBTILIS;

EID: 33845916036     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0607406     Document Type: Article

References (64)

1. Moore, C. M., and Helmann, J. D. (2005) Metal ion homeostasis in Bacillus subtilis, Curr. Opin. Microbiol. 8, 188-195.
2. Outten, F. W., Outten, C. E., and O'Halloran, T. V. (2000) Metalloregulatory systems at the interface between bacterial metal homeostasis and resistance, in Bacterial Stress Responses (Storz, G., Hengge-Aronis, R., Eds.) pp 145-157, ASM Press: Washington, DC.
3. O'Halloran, T. V. (1993) Transition metals in control of gene expression, Science 261, 715-725.
4. Rangachari, V., Marin, V., Bienkiewicz, E. A., Semavina, M., Guerrero, L., Love, J. F., Murphy, J. R., and Logan, T. M. (2005) Sequence of ligand binding and structure change in the diphtheria toxin repressor upon activation by divalent transition metals, Biochemistry 44, 5672-5682.
5. Bloom, S. L., and Zamble, D. B. (2004) Metal-selective DNA-binding response of Escherichia coli NikR, Biochemistry 43, 10029-10038.
6. Wang, S. C., Dias, A. V., Bloom, S. L., and Zamble, D. B. (2004) Selectivity of metal binding and metal-induced stability of Escherichia coli NikR, Biochemistry 43, 10018-10028.
7. Mills, S. A., and Marletta, M. A. (2005) Metal binding characteristics and role of iron oxidation in the ferric uptake regulator from Escherichia coli, Biochemistry 44, 13553-13559.
8. Liu, T., Golden, J. W., and Giedroc, D. P. (2005) A zinc(II)/lead(II)/ cadmium(II)-inducible operon from the cyanobacterium Anabaena is regulated by AztR, an α3N ArsR/SmtB metalloregulator, Biochemistry 44, 8673-8683.
9. Chou, C. J., Wisedchaisri, G., Monfeli, R. R., Oram, D. M., Holmes, R. K., Hol, W. G. J., and Beeson, C. (2004) Functional studies of the Mycobacterium tuberculosis iron-dependent regulator, J. Biol. Chem. 279, 53554-53561.
10. D'Aquino, J. A., Tetenbaum-Novatt, J., White, A., Berkovitch, F., and Ringe, D. (2005) Mechanism of metal ion activation of the diphtheria toxin repressor DtxR, Proc. Natl. Acad. Sci. U.S.A. 102, 18408-18413.
11. 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.
12. Lieser, S. A., Davis, T. C., Helmann, J. D., and Cohen, S. M. (2003) DNA-binding and oligomerization studies of the manganese(II) metalloregulatory protein MntR from Bacillus subtilis, Biochemistry 42, 12634-12642.
13. Glasfeld, A., Guedon, E., Helmann, J. D., and Brennan, R. G. (2003) Structure of the manganese-bound manganese transport regulator of Bacillus subtilis, Nat. Struct. Biol. 10, 652-657.
14. Pohl, E., Holmes, R. K., and Hol, W. G. J. (1998) Motion of the DNA-binding domain with respect to the core of the diphtheria toxin repressor (DtxR) revealed in the crystal structures of apo- and holo-DtxR, J. Biol. Chem. 273, 22420-22427.
15. Kliegman, J. I., Griner, S. L., Helmann, J. D., Brennan, R. G., and Glasfeld, A. (2006) Structural basis for the metal-selective activation of the manganese transport regulator of Bacillus subtilis, Biochemistry 45, 3493-3505.
16. Boyd, J., Oza, M. N., and Murphy, J. R. (1990) Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae, Proc. Natl. Acad. Sci. U.S.A. 87, 5968-5972.
17. Golynskiy, M. V., Davis, T. C., Helmann, J. D., and Cohen, S. M. (2005) Metal-induced structural organization and stabilization of the metalloregulatory protein MntR, Biochemistry 44, 3380-3389.
18. Sen, K. I., Sienkiewicz, A., Love, J. F., vanderSpek, J. C., Fajer, P. G., and Logan, T. M. (2006) Mn(II) binding by the anthracis repressor from Bacillus anthracis, Biochemistry 45, 4295-4303.
19. Connors, K. A. (1987) Binding Constants: The Measurement of Molecular Complex Stability, John Wiley & Sons, Inc., New York.
20. Kwan, C.-Y., and Putney, J. W., Jr. (1990) Uptake and intracellular sequestration of divalent cations in resting and methacholine-stimulated mouse lacrimal acinar cells, J. Biol. Chem. 265, 678-684.
21. Raju, B., Murphy, E., Levy, L. A., Hall, R. D., and London, R. E. (1989) A fluorescent indicator for measuring cytosolic free magnesium, Am. J. Physiol. 256, C540-C548.
22. Martell, A. E., and Smith, R. M. (1974) Critical Stability Constants, Vol. 4, Plenum Press: New York.
23. Lattanzio, F. A., Jr. and Bartschat, D. K. (1991) The effect of pH on rate constants, ion selectivity and thermodynamic properties of fluorescent calcium and magnesium indicators, Biochem. Biophys. Res. Comm. 177, 184-191.
24. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase, Anal. Biochem. 237, 260-273.
25. Kuzmic, P. (2006) A generalized numerical approach to rapid-equilibrium enzyme kinetics: Application to 17 beta-HSD, Mol. Cell. Endocrinol. 248, 172-181.
26. Mely, Y., Cornille, F., Fournie-Zaluski, M.-C., Darlix, J. L., Roques, B. P., and Gerard, D. (1991) Investigation of zinc-binding affinities of Moloney murine leukemia-virus nucleocapsid protein and its related zinc finger and modified peptides, Biopolymers 31, 899-906.
27. Walkup, G. K., and Imperiali, B. (1997) Fluorescent chemosensors for divalent zinc based on zinc finger domains. Enhanced oxidative stability, metal binding affinity, and structural and functional characterization, J. Am. Chem. Soc. 119, 3443-3450.
28. Golombek, A. P., and Hendrich, M. P. (2003) Quantitative analysis of dinuclear manganese(II) EPR spectra, J. Magn. Reson. 165, 33-48.
29. Henry, E. R., and Hofrichter, J. (1992) Singular value decomposition: application to analysis of experimental-data, Methods Enzymol. 210, 129-192.
30. Pierce, B. S., Elgren, T. E., and Hendrich, M. P. (2003) Mechanistic implications for the formation of the diiron cluster in ribonucleotide reductase provided by quantitative EPR spectroscopy, J. Am. Chem. Soc. 125, 8748-8759.
31. Press, W. H., Teukolsky, S. A., Vetterling, W. T., and Flannery, B. P. (1992) Numerical Recipes in FORTRAN: The Art of Scientific Computing, 2nd ed., Cambridge University Press, Cambridge.
32. 2+ indicators with greatly improved fluorescence properties, J. Biol. Chem. 260, 3440-3450.
33. Hinkle, P. M., Shanshala, E. D., II and Nelson, E. J. (1992) Measurement of intracellular cadmium with fluorescent dyes, J. Biol. Chem. 267, 25553-25559.
34. Atar, D., Backx, P. H., Appel, M. M., Gao, W. D., and Marban, E. (1995) Excitation-transcription coupling mediated by zinc influx through voltage-dependent calcium channels, J. Biol. Chem. 270, 2473-2477.
35. 2+ ion concentration with the fluorescent probe mag-fura-2 (furaptra), J. Biochem. Biophys. Meth. 27, 25-37.
36. Fahrni, C. J., and O'Halloran, T. V. (1999) Aqueous coordination chemistry of quinoline-based fluorescence probes for the biological chemistry of zinc, J. Am. Chem. Soc. 121, 11448-11458.
37. VanZile, M. L., Cosper, N. J., Scott, R. A., and Giedroc, D. P. (2000) The zinc metalloregulatory protein Synechococcus PCC7942 SmtB binds a single zinc ion per monomer with high affinity in a tetrahedral coordination geometry, Biochemistry 39, 11818-11829.
38. Reed, G. H., and Cohn, M. (1970) Electron paramagnetic resonance spectra of manganese(II)-protein complexes, J. Biol. Chem. 245, 662-667.
39. Reiter, N. J., White, D. J., and Rusnak, F. (2002) Inhibition of bacteriophage lambda protein phosphatase by organic and oxoan-ion inhibitors, Biochemistry 41, 1051-1059.
40. Busenlehner, L. S., Pennella, M. A., and Giedroc, D. P. (2003) The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance, FEMS Microbiol. Rev. 27, 131-143.
41. Sigel, H., and McCormick, D. B. (1970) On the discriminating behavior of metal ions and ligands with regard to their biological significance, Acc. Chem. Res. 3, 201-208.
42. Caneschi, A., Ferraro, F., Gatteschi, D., Melandri, M. C., Rey, P., and Sessoli, R. (1989) Synthesis, structure and magnetic-properties of a dinuclear manganese(II) complex with one μ-Aqua and 2 μ-carboxylato bridges, Angew. Chem. Int. Ed. 28, 1365-1367.
43. Yu, S.-B., Lippard, S. J., Shweky, I., and Bino, A. (1992) Dinuclear manganese(II) complexes with water and carboxylate bridges, Inorg. Chem. 31, 3502-3504.
44. 2O containing an unprecedented short Mn⋯Mn distance of 2.296 Å, J. Am. Chem. Soc. 110, 7398-7411.
45. 2 (bipy=2,2′-bipyridine), J. Chem. Soc. Dalton 3465-3469.
46. Nepveu, F., Gaultier, N., Korber, N., Jaud, J., and Castan, P. (1995) New polynuclear manganese(II) complexes with orotic acid and some of its derivatives: crystal structures, spectroscopic and magnetic studies, J. Chem. Soc. Dalton 4005-4013.
47. 3CN (tpa = tris(2-pyridylmethyl)amine), Inorg. Chem. 32, 5697-5703.
48. Chen, X.-M., Tong, Y.-X., Xu, Z.-T., and Mak, T. C. W. (1995) Synthesis, structure and magnetic properties of a singly carboxylate-bridged dinuclear manganese(II) complex, J. Chem. Soc. Dalton 4001-4004.
49. 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, J. Biol. Chem. 277, 38441-38448.
50. Tottey, S., Harvie, D. R., and Robinson, N. J. (2005) Understanding how cells allocate metals using metal sensors and metallochaperones, Acc. Chem. Res. 38, 775-783.
51. Pennella, M. A., and Giedroc, D. P. (2005) Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators, BioMetals 18, 413-428.
52. Brown, N. L., Stoyanov, J. V., Kidd, S. P., and Hobman, J. L. (2003) The MerR family of transcriptional regulators, FEMS Microbiol. Rev. 27, 145-163.
53. 5) heavy metal-binding sites in Staphylococcus aureus pI258 CadC: evolutionary implications for metal ion selectivity of ArsR/SmtB metal sensor proteins, J. Mol. Biol. 319, 685-701.
54. Changela, A., Chen, K., Xue, Y., Holschen, J., Outten, C. E., O'Halloran, T. V., and Mondragón, A. (2003) Molecular basis of metal-ion selectivity and zeptomolar sensitivity by CueR, Science 301, 1383-1387.
55. Eicken, C., Pennella, M. A., Chen, X., Koshlap, K. M., VanZile, M. L., Sacchettini, J. C., and Giedroc, D. P. (2003) A metal-ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins, J. Mol. Biol. 333, 683-695.
56. Outten, C. E., and O'Halloran, T. V. (2001) Femtomolar Sensitivity of Metalloregulatory Proteins Controlling Zinc Homeostasis, Science 292, 2488-2492.
57. VanZile, M. L., Chen, X., and Giedroc, D. P. (2002) Allosteric negative regulation of smt O/P binding of the zinc sensor, SmtB, by metal ions: a coupled equilibrium analysis, Biochemistry 41, 9776-9786.
58. Hantke, K. (2001) Iron and metal regulation in bacteria, Curr. Opin. Microbiol. 4, 172-177.
59. Kehres, D. G., and Maguire, M. E. (2003) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria, FEMS Microbiol. Rev. 27, 263-290.
60. Finney, L. A., and O'Halloran, T. V. (2003) Transition metal speciation in the cell: insights from the chemistry of metal ion receptors, Science 300, 931-936.
61. Keyer, K., and Imlay, J. A. (1996) Superoxide accelerates DNA damage by elevating free-iron levels, Proc. Natl. Acad. Sci. U.S.A. 93, 13635-13640.
62. Guedon, E., and Hermann, J. D. (2003) Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators, Mol. Microbiol. 48, 495-506.
63. Nies, D. H. (1999) Microbial heavy metal resistance, Appl. Microbiol. Biotechnol. 51, 730-750.
64. Weinberg, E. D. (1964) Manganese requirement for sporulation and other secondary biosynthetic processes of Bacillus, Appl. Microbiol. 12, 436-441.