Spectral, kinetic, and thermodynamic properties of Cu(I) and Cu(II) binding by methanobactin from methylosinus trichosporium OB3b

Biochemistry

Volumn 45, Issue 5, 2006, Pages 1442-1453

  Choi, Dong W ^a   Zea, Corbin J ^a   Do, Young S ^a   Semrau, Jeremy D ^b   Antholine, William E ^c   Hargrove, Mark S ^a   Pohl, Nicola L ^a   Boyd, Eric S ^a   Geesey, G G ^d   Hartsel, Scott C ^e   Shafe, Peter H ^e   McEllistrem, Marcus T ^e   Kisting, Clint J ^a   Campbell, Damon ^e   Rao, Vinay ^e   De La Mora, Arlene M ^a   DiSpirito, Alan A ^a  

^a IOWA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d MONTANA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF WISCONSIN EAU CLAIRE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY CHROMATOGRAPHY; BINDING ENERGY; COPPER; FLUORESCENCE; MONOMERS; SOLUBILITY; THERMODYNAMIC PROPERTIES;

ACQUISITION SYSTEM; CIRCULAR DICHROISM; METHANOBACTIN (MB); THIOCARBONYL-5-HYDROXY IMIDAZOLATE (THI);

PROTEINS;

4 HYDROXY 5 THIOCARBONYLIMIDAZOLATE; 4 THIOCARBONYL 5 HYDROXYIMIDAZOLATE; BACTERIAL PROTEIN; CARBONYL DERIVATIVE; CUPRIC ION; CUPROUS ION; EDETIC ACID; IMIDAZOLE DERIVATIVE; METHANOBACTIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; CIRCULAR DICHROISM; COPPER METABOLISM; FLUORESCENCE SPECTROSCOPY; METHYLOSINUS TRICHOSPORIUM; NONHUMAN; PRIORITY JOURNAL; REDUCTION; SOLUBILIZATION; THERMODYNAMICS; ULTRAVIOLET SPECTROSCOPY;

CIRCULAR DICHROISM; COPPER; IMIDAZOLES; KINETICS; METHYLOSINUS TRICHOSPORIUM; MOLECULAR STRUCTURE; OLIGOPEPTIDES; ORGANOMETALLIC COMPOUNDS; SENSITIVITY AND SPECIFICITY; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, X-RAY EMISSION; SPECTROPHOTOMETRY, ULTRAVIOLET; THERMODYNAMICS; TIME FACTORS;

BACTERIA (MICROORGANISMS); METHYLOSINUS TRICHOSPORIUM;

EID: 32244436303     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051815t     Document Type: Article

References (78)

1. Anthony, C. (1982) The Biochemistry of Methylotrophs, Academic Press, London.
2. 1 Compounds (Crawford, R. L., and Hanson, R. S., Eds.) pp 75-82, American Society for Microbiology, Washington, DC.
3. DiSpirito, A. A., Gulledge, J., Schiemke, A. K., Murrell, J. C., and Lidstrom, M. E. (1992) Trichloroethylene oxidation by the membrane-associated methane monooxygenase in type I, type II, and type X methanotrophs, Biodegradation 2, 151-164.
4. Hanson, R. L., and Hanson, T. E. (1996) Methanotrophic bacteria, Microbiol. Rev. 60, 439-471.
5. Lontoh, S., DiSpirito, A. A., and Semrau, J. D. (1999) Dichloromethane and trichloroethylene inhibition of methane oxidation by the membrane-associated methane monooxygenase of Methylosinus trichosporium OB3b, Arch. Microbiol. 173, 29-34.
6. Basu, P., Katterle, B., Anderson, K. A., and Dalton, H. (2002) The membrane-associated form of methane monooxygenase from Methylococcus capsulatus (Bath) is a copper/iron protein, Biochem. J. 369, 417-427.
7. Chan, S. I., Chen, K. H.-C., Yu, S. S.-F., Chen, C.-L., and Kuo, S. S.-J. (2004) Tword delineating the structure and function of the particulate methane monooxygenase from methanotrophic bacteria, Biochemistry 43, 4421-4430.
8. Choi, D.-W., Antholine, W. A., Do, Y. S., Semrau, J. D., Kisting, C. J., Kunz, R. C., Campbell, D., Rao, V., Hartsel, S. C., and DiSpirito, A. A. (2005) Effect of methanobactin on methane oxidation by the membrane-associated methane monooxygenase in Methylococcus capsulatus Bath, Microbiology 151, 3417-3426.
9. Choi, D.-W., Kunz, R. C., Boyd, E. S., Semrau, J. D., Antholine, W. A., Han, J.-I., Zahn, J. A., Boyd, J. M., de la Mora, A. M., and DiSpirito, A. A. (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase from Methylococcus capsulatus Bath, J. Bacteriol. 185, 5755-5764.
10. DiSpirito, A. A., Kunz, R. C., Choi, D. W., and Zahn, J. A. (2004) Electron flow during methane oxidation in methanotrophs, in Respiration in Archaea and Bacteria (Zannoni, D., Ed.) pp 141-169, Kluwer Scientific, Dordrecht, The Netherlands.
11. Morton, J. D., Hayes, K. F., and Semrau, J. D. (2000) Bioavailability of chelated and soil-absorbed copper to Methylosinus trichosporium OB3b, Environ. Sci. Technol 34, 4917-4922.
12. Nguyen, A.-N., Schiemke, A. K., Jacobs, S. J., Hales, B. J., Lidstrom, M. E., and Chan, S. I. (1994) The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath), J. Biol. Chem. 269, 14995-15005.
13. Nguyen, H.-H., Elliott, S. J., Yip, J. H.-K., and Chan, S. I. (1998) The particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a novel copper-containing three-subunit enzyme, J. Biol. Chem. 273, 7957-7966.
14. Takeguchi, M., Miyakawa, K., and Okura, I. (1998) Purification and properties of particulate methane monooxygenase from Methylosinus trichosporium OB3b, J. Mol. Catal. 132, 145-153.
15. Zahn, J. A., and DiSpirito, A. A. (1996) Membrane associated methane monooxygenase from Methylococcus capsulatus (Bath), J. Bacteriol. 178, 1018-1029.
16. Han, J.-I., and Semrau, J. D. (2001) Quantification of the expression of pmoA in methanotrophs using RT-PCR, Proc. Am. Chem. Soc. Abstract no. 221.
17. Han, J.-I., and Semrau, J. D. (2004) Quantification of gene expression in methanotrophs by competitive reverse transcriptionpolymerase chain reaction, Environ. Microbiol. 6, 388-399.
18. Lontoh, S., and Semrau, J. D. (1998) Methane and trichloroethylene degradation by Methylosinus trichosporium expressing particulate methane monooxygenase, Appl. Environ. Microbiol. 64, 1106-1114.
19. Murrell, J. C., McDonald, I. R., and Gilbert, B. (2000) Regulation of expression of methane monooxygenases by copper ions, Trends Microbiol. 5, 221-225.
20. Prior, S. D., and Dalton, H. (1985) Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane oxidizing organisms: Studies in batch and continuous culture, J. Gen. Microbiol. 131, 155-163.
21. Stanley, S. H., Prior, S. D., Leak, D. J., and Dalton, H. (1983) Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures, Biotechnol. Lett. 5, 487-492.
22. DiSpirito, A. A., Zahn, J. A., Graham, D. W., Kim, H. J., Larive, C. K., Derrick, T. S., Cox, C. D., and Taylor, A. (1998) Copper-binding compounds from Methylosinus trichosporium OB3b, J. Bacteriol. 180, 3606-3616.
23. Kim, H. J., Galeva, N., Larive, C. K., Alterman, M., and Graham, D. W. (2005) Purification and physical-chemical properties of methanobactin: A chalkophore from Methylosinus trichosporium OB3b, Biochemistry 44, 5140-5148.
24. Kim, H. J., Graham, D. W., DiSpirito, A. A., Alterman, M., Galeva, N., Asunskis, D., Sherwood, P., and Larive, C. K. (2004) Methanobactin, a copper-acquisition compound in methane-oxidizing bacteria, Science 305, 1612-1615.
25. Tellez, C. M., Gaus, K. P., Graham, D. W., Arnold, R. G., and Guzman, R. Z. (1998) Isolation of copper biochelates from Methylosinus trichosporium OB3b, Appl. Environ. Microbiol. 64, 1115-1122.
26. Phelps, P. A., Agarwal, G. E., Speitel, G. E. J., and Georgiou, G. (1992) Methylosinus trichosporium OB3b mutants having constitutive expression of soluble methane monooxygenase in the presence of high levels of copper, Appl. Environ. Microbiol. 58, 3701-3708.
27. Bielli, P., and Calabrese, L. (2002) Structure to function relationships in ceruloplasmin: A 'moonlighting' protein, Cell. Mol. Life Sci. 59, 1413-1427.
28. Jeffery, C. J. (1999) Moonlighting Proteins, Trends Biochem. Sci. 24, 8-11.
29. Jeffery, C. J. (2003) Moonlighting proteins: Old proteins learning new tricks, Trends Genet. 19, 415-417.
30. Jeffery, C. J. (2004) Molecular mechanisms for multitasking: Recent crystal structures of moonlighting proteins, Curr. Opin. Struct. Biol. 14, 663-668.
31. Moor, B. D. (2004) Bifunctional and moonlighting enzymes: Lighting the way to regulatory control, Trends Plant Sci. 9, 221-228.
32. Tompa, P., Szasz, C., and Buday, L. (2005) Structural disorder throws a new light on moonlighting, Trends Biochem. Sci. 30, 484-489.
33. Neilands, J. B. (1995) Siderophores: Structure and function of microbial iron transport compounds, J. Biol. Chem. 270, 26723-26726.
34. Nielands, J. B. (1983) Siderophores, Adv. Inorg. Biochem. 5, 138-166.
35. Bonomo, R. P., Cali, R., Cucinotta, V., Impellizzeri, G., and Rizzarelli, E. (1986) Copper(II) complexes of diastereoisomeric dipeptides in aqueous solutions. Effects of side-chain groups on the thermodynamic sterioselectivity, Inorg. Chem. 25, 1641-1646.
36. Letter, J. E., and Bauman, J. E. J. (1970) A thermodynamic study of the complexation and coordinated ligand deprotonation reactions for a series of tyrosine isomer with copper(II), J. Am. Chem. Soc. 92, 443-447.
37. Livera, C., Pettit, L. D., Bataille, M., Bal, W., and Kozlowskim, H. (1988) Copper(II) complexes with some tetrapeptides containing the 'break-point' prolyl residue in the third position, J. Chem. Soc., Dalton Trans., 1357-1360.
38. Osz, K., Boka, B., Vamagy, K., Sovago, I., Kurtan, T., and Antus, S. (2002) The application of circular dichroism spectroscopy for the determination of metal ion speciation and coordination modes of peptide complexes, Polyhedron 21, 2149-2159.
39. Pecci, L., Molntefoschi, G., Musci, G., and Cavallini, D. (1997) Novel findings on the copper catalyzed oxidation of cysteine, Amino Acids 13, 355-367.
40. Pettit, L. D., Steel, I., Formica-Kozlowski, G., Tatarowski, T., and Bataille, M. (1985) The L-proline residue as a 'break-point' in metal-peptide systems, J. Chem. Soc., Dalton Trans., 535-539.
41. Rigo, A., Corazza, A., de Paolo, M. L., Rossetto, M., Ugolini, R., and Scarpa, M. (2004) Interaction of copper with cysteine: Stability of cuprous complexes and catalytic role of cupric ions in anaerobic thiol oxidation, J. Inorg. Biochem. 98, 1495-1501.
42. Greenstein, J. P., and Winitz, M. (1961) Chemistry of the Amino Acids, Vol. 2, John Wiley & Sons, Inc., New York.
43. Hefford, R. J. W., and Pettit, L. D. (1981) Potentiometric and spectrophotometric study of the co-ordination compounds formed between copper(II) and dipeptides containing tyrosine, J. Chem. Soc., Dalton Trans., 1331-1335.
44. Kozlowska, H., Benzer, M., Pettit, L. D., and Hecquet, B. (1983) Coordination abilities of tetrapeptides containing proline and tyrosine-a spectrometric and potentiometric study, J. Inorg. Biochem. 18, 231-240.
45. Pettit, L. D., Steel, I., Kowalik, T., Kozlowski, H., and Bataille, M. (1985) Specific binding of the tyrosine residue in copper(II) complexes of tyr-pro-gly-tyr and tyr-gly-pro-tyr, J. Chem. Soc., Dalton Trans., 1201-1205.
46. Neu, A. L., Techkarinjanarukm, S., Dohnalkova, A., McCready, D., Peyton, B. M., and Geesey, G. G. (2001) Iron sulfides and sulfur species produced at hematite surfaces in the presence of sulfate-reducing bacteria, Goechim. Cosmochim. Acta 65, 223-235.
47. Edsall, J. T., Felsenfeld, G., Goodman, D. S., and Gurd, F. R. N. (1954) The association of imidazole with the ions of zinc and cupric copper, J. Am. Chem. Soc. 76, 3054-3061.
48. Sigel, H., and Martin, R. B. (1982) Coordinating properties of the amide bond. Stability and structure of metal ion complexes of peptides and related ligands, Chem. Rev. 82, 385-426.
49. Tsangaris, J. M., Chang, J. W., and Martin, R. B. (1969) Ultraviolet circular dichroism of cupric and nickel complexes of amino acids and peptides, J. Am. Chem. Soc. 91, 726-731.
50. Byrd, J., Berger, R. M., McMillin, D. R., Wright, C. F., Hamer, D., and Winge, D. R. (1988) Characterization of the copper-thiolate cluster in yeast metallothionein and two truncated mutants, J. Biol. Chem. 263, 6688-6694.
51. Hasler, D. W., Faller, P., and Vasak, M. (1998) Metal-thiolate clusters in the C-terminal domain of human neuronal growth inhibitory factor (GIF), Biochemistry 37, 14966-14973.
52. Nielson, K. B., Atkin, C. L., and Winge, D. R. (1985) Distinct metal-binding conformations in metallothionein, J. Biol. Chem. 260, 5342-5350.
53. Nielson, K. B., and Winge, D. R. (1984) Preferential binding of copper to the β domain of metallothionein, J. Biol. Chem. 259, 4941-4946.
54. 4-thiolate clusters, Biochemistry 33, 9699-9705.
55. Formica-Kozlowski, G., Kozlowska, H., Siemion, I. Z., Sobczyk, K., and Nawrocka, E. (1984) The coordination of copper(II) with β-casomorphin and its fragments, J. Inorg. Biochem. 22, 155-163.
56. Pettit, L. D., Bataille, M., Gregor, J. E., and Kozlowska, H. (1991) Complex formation between metal ions and peptides, in Perspectives on Bioinorganic Chemistry (Hat, R. W., Dilworth, J. R., and Noland, K. B., Eds.) pp 1-41, JAI Press Ltd., Greenwich, CT.
57. Yamauchi, O., Tsujide, K., and Odani, A. (1985) Copper(II) complexes of tyrosine-containing dipeptides. Effects of side chain groups on spectral and solution chemical properties and their structural implications, J. Am. Chem. Soc. 107, 659-666.
58. Becker, R. S. (1969) Theory and Interpretation of Fluorescence and Phosphorescence, John Wiley & Sons, Inc., New York.
59. Guilbault, G. G. (1967) Fluorescence Theory, Instrumentation, and Practice, Marcel Dekker, New York.
60. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd ed., Kluwer Academic/Plenum Publishers, New York.
61. Schulman, S. G. (1977) Fluorescence and Phosphorescence Spectroscopy; Physiolochemical Principles and Practice, Pergamon Press, Inc., New York.
62. Valeur, B. (2002) Molecular Fluorescence, Wiley-VCH, Weinheim, Germany.
63. Fasman, G. D. (1996) Circular Dichroism and the Conformational Analysis of Biomolecules, Plenum Press, New York.
64. Kowalik-Jankowska, T., Ruta-Dolejsz, M., Wisniewska, K., and Lankiewicz, L. (2002) Coordination of copper(II) ions by the 11-20 and 11-28 fragments of human and mouse β-amyloid peptide, J. Inorg. Biochem. 92, 1-10.
65. Berova, N., Nakanishi, K., and Woody, R. W. (2000) Circular Dichroism; Principles and Applications, 2nd ed., Wiley-VCH, New York.
66. Bain, C. D., Biebuyck, A., and Whitesides, G. M. (1989) Comparison of self-assembled monolayers on gold: Coadsorption of thiols and disulfides, Langmuir 5, 725-727.
67. Riga, J., and Verbist, J. J. (1983) The Bisulphide Group in Organic Compounds: Conformational Dependence of Core and Valence Sulphur Electronic Levels by X-ray Photoelectron Spectroscopy, J. Chem. Soc., Perkin Trans. 2, 1545-1553.
68. Wagner, C. D., Naumkin, A. V., Kraut-Vass, A., Allison, J. W., Powell, C. J., and Rumble, J. R. J. (2005) U.S. National Institute of Standards and Technology.
69. Singh, R., Blatler, W. A., and Collinson, A. R. (1993) An amplified assay for thiols based on reactivation of papain, Anal. Biochem. 91, 49-56.
70. Martin, R. B. (1977) Complexes of α-amino acids with chelatable side chain donor atoms, Ions Biol. Syst. 9, 1-40.
71. May, P. M., and Williams, D. A. (1981) Role of low molecular weight copper complexes in the control of rheumatoid arthritis, Met. Ions Biol. Syst. 12, 283-317.
72. Pettit, L. D., and Hefford, R. J. W. (1979) Stereoselectivity in the metal complexes of amino acids and dipeptides, Met. Ions Biol. Syst. 9, 173-212.
73. Smith, R. M., and Martell, A. E. (1975) Critical Stability Constants, Vol. 2, Plenum Press, New York.
74. Smith, R. M., and Martell, A. E. (1989) Critical Stability Constants, Vol. 6, Plenum Press, New York.
75. Martell, A. E., and Smith, R. M. (1984) Critical Stability Constants, Vol. 1, Plenum Press, New York.
76. Burns, C. S., Aronoff-Spencer, E., Legname, G., Prusiner, S. B., Antholine, W. E., Gerfen, G. J., Peisach, J., and Millhauser, G. L. (2003) Cooper coordination in the full-length, recombinant prion protein, Biochemistry 42, 6794-6803.
77. Morante, S., Gonzalez-Igesias, A., Potrich, C., Meneghin, C., Meyer-Klaucke, W., Menestrain, G., and Gasset, M. (2004) Inter- and intra-octarepeat Cu(II) site geometries in the prion protein, J. Biol. Chem. 279, 11753-11759.
78. Wong, B.-S., Venien-Bryan, C., Williamson, R. A., Burton, D. R., Gambetti, P., Sy, M.-S., Browin, D. R., and Jones, I. M. (2000) Copper refolding of prion protein, Biochem. Biophys. Res. Commun. 267, 1217-1224.