Probing the geometric and electronic structures of the low-temperature azide adduct and the product-inhibited form of oxidized manganese superoxide dismutase

Biochemistry

Volumn 44, Issue 5, 2005, Pages 1504-1520

  Jackson, Timothy A ^a   Karapetian, Anush ^b   Miller, Anne Frances ^b   Brunold, Thomas C ^a,c  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPUTATIONAL COMPLEXITY; MANGANESE; OXIDATION; SPECTROSCOPY;

AXIAL SOLVENTS; SUPEROXIDES;

ELECTRONIC STRUCTURE;

MANGANESE SUPEROXIDE DISMUTASE;

ARTICLE; CHEMICAL REACTION KINETICS; CIRCULAR DICHROISM; DENSITY FUNCTIONAL THEORY; ELECTRON TRANSPORT; LOW TEMPERATURE; OXIDATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; PROTON TRANSPORT; SPECTROSCOPY;

AZIDES; BINDING SITES; CIRCULAR DICHROISM; COLD; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ELECTRONS; ESCHERICHIA COLI PROTEINS; MANGANESE; MODELS, CHEMICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; SUPEROXIDE DISMUTASE; SUPEROXIDES; TEMPERATURE; THERMUS THERMOPHILUS;

EID: 13444257644     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048639t     Document Type: Article

References (77)

1. Miller, A.-F., and Sorkin, D. L. (1997) Superoxide dismutases: A molecular perspective, Comments Mol. Cell. Biophys. 9, 1-48.
2. Packer, L. (2002) in Methods in Enzymology (Abelson, J. N., and Simon, M. I., Eds.) pp 400, Academic Press, San Diego, CA.
3. Miller, A.-F. (2004) in Comprehensive Coordination Chemistry II (McCleverty, J. A., and Meyer, T. J., Eds.) pp 479-506, Elsevier Ltd., Oxford, U.K.
4. Ludwig, M. L., Metzger, A. L., Pattridge, K. A., and Stallings, W. C. (1991) Manganese superoxide-dismutase from Thermus thermophilus. A structural model refined at 1.8 Å resolution, J. Mol. Biol. 219, 335-358.
5. Lah, M. S., Dixon, M. M., Pattridge, K. A., Stellings, W. C., Fee, J. A., and Ludwig, M. L. (1995) Structure-function in Escherichia coli iron superoxide dismutase: Comparisons with the manganese enzyme from Thermus thermophilus, Biochemistry 34, 1646-1660.
6. Edwards, R. A., Baker, H. M., Whittaker, M. M., Whittaker, J. W., Jameson, G. B., and Baker, E. N. (1998) Crystal structure of Escherichia coli manganese superoxide dismutase at 2.1 Å resolution, J. Biol. Inorg. Chem. 3, 161-171.
7. Han, W.-G., Lovell, T., and Noodleman, L. (2002) Coupled redox potentials in manganese and iron superoxide dismutases from reaction kinetics and density functional/electrostatics calculations, Inorg. Chem. 41, 205-218.
8. Miller, A.-F., Padmakumar, F., Sorkin, D., Karapetian, A., and Vance, C. K. (2003) Proton-coupled electron transfer in Fesuperoxide dismutase and Mn-superoxide dismutase, J. Inorg. Biochem. 93, 71-83.
9. Pick, M., Rabani, J., Yost, F., and Fridovich, I. (1974) The catalytic mechanism of the manganese-containing superoxide dismutase of Escherichia coli studied by pulse radiolysis, J. Am. Chem. Soc. 96, 7329-7333.
10. McAdam, M. E., Fox, R. A., Lavelle, F., and Fielden, E. M. (1977) A pulse-radiolysis study of the manganese-containing superoxide dismutase from Bacillus stearothermophilus. A kinetic model for the enzyme action, Biochem. J. 165, 71-79.
11. McAdam, M. E., Lavelle, F., Fox, R. A., and Fielden, E. M. (1977) A pulse-radiolysis study of the manganese-containing superoxide dismutase from Bacillus stearothermophilus. Further studies on the properties of the enzyme, Biochem. J. 165, 81-87.
12. Bull, C., Niederhoffer, E. C., Yoshida, T., and Fee, J. A. (1991) Kinetic studies of superoxide dismutases: Properties of the manganese-containing protein from Thermus themophilus, J. Am. Chem. Soc. 113, 4069-4076.
13. Hearn, A. S., Tu, C. K., Nick, H. S., and Silverman, D. N. (1999) Characterization of the product inhibited complex in catalysis by human manganese superoxide dismutase, J. Biol. Chem. 274, 24457-24460.
14. Davis, C. A., Hearn, A. S., Fletcher, B., Bickford, J., Garcia, J. E., Lévêque, V., Melendez, J. A., Silverman, D. N., Zucali, J., Aganval, A., and Nick, H. S. (2004) Potent anti-tumor effects of an active site mutant of human manganese-superoxide dismutase, J. Biol. Chem. 279, 12769-12776.
15. Whittaker, M. M., and Whittaker, J. W. (1996) Low-temperature thermochromism marks a change in coordination for the metal ion in manganese superoxide dismutase, Biochemistry 35, 6762-6770.
16. 3), J. Am. Chem. Soc. 116, 11596-11597.
17. 3-: Electronic structure of the side-on ferric-peroxide bond and its relevance to reactivity, J. Am. Chem. Soc. 120, 12829-12848.
18. Whittaker, M. M., and Whittaker, J. W. (1997) A "thermophilic shift" in ligand interactions for Thermus thermophilus manganese superoxide dismutase, J. Biol. Inorg. Chem. 2, 661-671.
19. Whittaker, J. W. (1997) A model for local melting of metalloprotein structure, J. Phys. Chem. B 101, 674-677.
20. Jackson, T. A., Karapetian, A., Miller, A.-F., and Brunold, T. C. (2004) Spectroscopic and computational studies of the azide-adduct of manganese superoxide dismutase: Definitive assignment of the ligand responsible for the low-temperature thermochromism, J. Am. Chem. Soc. 126, 12477-12491.
21. Hsu, J. L., Hsieh, Y. S., Tu, C. K., O'Connor, D., Nick, H. S., and Silverman, D. N. (1996) Catalytic properties of human manganese superoxide dismutase, J. Biol. Chem. 271, 17687-17691.
22. Whittaker, J. W., and Whittaker, M. M. (1991) Active site spectral studies on manganese superoxide dismutase, J. Am. Chem. Soc. 113, 5528-5540.
23. III center of oxidized manganese superoxide dismutase, J. Am. Chem. Soc. 121, 4714-4715.
24. Vance, C. K., and Miller, A.-F. (1998) Spectroscopic comparisons of the pH dependencies of Fe-substituted (Mn)superoxide dismutase and Fe-superoxide dismutase, Biochemistry 37, 5518-5527.
25. Vance, C. K., and Miller, A.-F. (1998) A simple proposal that can explain the inactivity of metal-substituted superoxide dismutases, J. Am. Chem. Soc. 120, 461-467.
26. Neese, F., and Solomon, E. I. (1999) MCD C-term signs, saturation behavior, and determination of band polarizations in randomly oriented systems with spin S ≥ 1/2. Application to S = 1/2 and S = 5/2, Inorg. Chem. 38, 1847-1865.
27. Hearn, A. S., Stroupe, M. E., Cabelli, D. E., Ramilo, C. A., Luba, J. P., Tainer, J. A., Nick, H. S., and Silverman, D. N. (2003) Catalytic and structural effects of amino acid substitution at histidine 30 in human manganese superoxide dismutase: Insertion of valine Cγy into the substrate access channel. Biochemistry 42, 2781-2789.
28. Whittaker, M. M., Ekberg, C. A., Edwards, R. A., Baker, E. N., Jameson, G. B., and Whittaker, J. W. (1998) Single-crystal polarized spectroscopy of manganese superoxide dismutase and electronic structure of the active site metal complex, J. Phys. Chem. B 102, 4668-4677.
29. Li, J., Fisher, C. L., Konecny, R., Lovell, T., Bashford, D., and Noodleman, L. (1999) Density functional and electrostatic calculations of manganese superoxide dismutase active site complexes in protein environments, Inorg. Chem. 38, 929-939.
30. Jackson, T. A., Xie, J., Yikilmaz, E., Miller, A.-F., and Brunold, T. C. (2002) Spectroscopic and computational studies on iron and manganese superoxide dismutases: Nature of the chemical events associated with active site pKs, J. Am. Chem. Soc. 124, 10833-10845.
31. -, Chem. Commun. 436-437.
32. te Velde, G., Bickelhaupt, F. M., van Gisbergen, S. J. A., Guerra, C. F., Baerends, E. J., Snijders, J. G., and Ziegler, T. (2001) Chemsitry with ADF, J. Comput. Chem. 22, 931-967.
33. Guerra, C. F., Snijders, J. G., te Velde, G., and Baerends, E. J. (1998) Towards an order-n DFT method, Theor. Chem. Acc. 99, 391-403.
34. ADF2003.01, SCM, Theoretical Chemistry, Vrije Universiteit, Amsterdam, The Netherlands, http://www.scm.com.
35. Vosko, S. H., Wilk, L., and Nusair, M. (1980) Accurate spin-dependent electron liquid correlation energies for local spin density calculations: A critical analysis, Can. J. Phys. 58, 1200-1211.
36. Becke, A. D. (1986) Density functional calculations of molecular bond energies, J. Chem. Phys. 84, 4524-4529.
37. Perdew, J. P. (1986) Density functional approximation for the correlation energy of the inhomogeneous electron gas, Phys. Rev. B 33, 8822-8824.
38. Neese, F. (2002) Orca - An ab initio, density functional, and semiempirical program package, Version 2.2, Max Planck Institut für Strahlenchemie, Mülheim, Germany.
39. Ridley, J., and Zerner, M. C. (1973) An intermediate neglect of differential overlap technique for spectroscopy: Pyrrole and the azines, Theor. Chim. Acta 32, 111-134.
40. Zerner, M. C., Loew, G. H., Kirchner, R. F., and Mueller-Westerhof, U. T. (1980) An intermediate neglect of differential overlap technique for spectra of transition-metal complexes: Ferrocene, J. Am. Chem. Soc. 102, 589-599.
41. Bacon, A. D., and Zerner, M. C. (1979) An intermediate neglect of differential overlap theory for transition-metal complexes, Theor. Chim. Acta 53, 21-54.
42. Becke, A. D. (1993) A new mixing of Hartree-Fock and localdensity- functional theories, J. Chem. Phys. 98, 1372-1377.
43. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys. 98, 5648-5652.
44. Lee, C., Yang, W., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
45. Schäfer, A., Horn, H., and Ahlrichs, R. (1992) Fully optimized contracted Gaussian basis sets for atoms lithium to krypton, J. Chem. Phys. 97, 2571-2577.
46. The Ahlrichs auxiliary basis sets were obtained from the turbomole basis set library under ftp.chemie.uni-karlsruhe.de/pub/cbasen. Weigend, F.; Häser, M. (1997) 97, 331-340.
47. Schäfer, G., Huber, C., and Ahlrichs, R. (1994) Fully optimized contracted Gaussian basis sets of triple-ζ valence quality for atoms Li to Kr, J. Chem. Phys. 100, 5829-5835.
48. Laaksonen, L. (1992) A graphics program for the analysis and display of molecular dynamics trajectories, J. Mol. Graphics 10, 33-34.
49. Bergman, D. L., Laaksonen, L., and Laaksonen, A. (1997) Visualization of solvation structures in liquid mixtures, J. Mol. Graphics Modell. 15, 301-306.
50. Bauemschmitt, R., and Ahlrichs, R. (1996) Treatment of electronic excitations within the adiabatic approximation of time dependent density functional theory, Chem. Phys. Lett. 256, 454-464.
51. Casida, E. M., Jamorski, C., Casida, K. C., and Salahub, D. R. (1998) Molecular excitation energies to high-lying bound states from time-dependent density-functional response theory: Characterization and correction of the time-dependent local density approximation ionization threshold, J. Chem. Phys. 108, 4439-4449.
52. Stratman, R. E., Scuseria, G. E., and Frisch, M. J. (1998) An efficient implementation of time-dependent density-functional theory for the calculation of excitation energies of large molecules, J. Chem. Phys. 109, 8218-8224.
53. Hirata, S., and Head-Gordon, M. (1999) Time-dependent density functional theory for radicals: An improved description of excited states with substantial double excitation character, Chem. Phys. Lett. 302, 375-382.
54. Hirata, S., and Head-Gordon, M. (1999) Time-dependent density functional theory within the Tamm-Dancoff approximation, Chem. Phys. Lett. 314, 291-299.
55. Neese, F., and Olbrich, G. (2002) Efficient use of the resolution of the identity approximation in time-dependent density functional calculations with hybrid density functionals, Chem. Phys. Lett. 362, 170-178.
56. 7 system: Exploring the geometric and electronic structures of the nitrosyl adduct of iron superoxide dismutase, J. Am. Chem. Soc. 125, 8348-8363.
57. Konecny, R., Li, J., Fisher, C. L., Dillet, V., Bashford, D., and Noodleman, L. (1999) CuZn superoxide dismutase geometry optimization, energetics, and redox potential calculations by density functional and electrostatic methods, Inorg. Chem. 38, 940-950.
58. a values of hydrated transition metal cations by a combined density functional and continuum dielectric theory, Inorg. Chem. 35, 4694-4702.
59. Noodleman, L., Lovell, T., Han, W.-G., Li, J., and Himo, F. (2004) Quantum chemical sudies of intermediates and reaction pathways in selected enzymes and catalytic synthetic systems, Chem. Rev. 104, 459-508.
60. Lever, A. B. P. (1984) Inorganic Electronic Spectroscopy, 2nd ed., Elsevier, Amsterdam, The Netherlands.
61. Xie, J., Yikilmaz, E., Miller, A.-F., and Brunold, T. (2002) Second-sphere contributions to substrate-analog binding in iron(III) superoxide dismutase, J. Am. Chem. Soc. 124, 3769-3774.
62. Krzystek, J., Yeagle, G. J., Park, J.-H., Britt, R. D., Meisel, M. W., Brunel, L.-C., and Telser, J. (2003) High-frequency and -field EPR spectroscopy of tris(2,4-pentanedionato)manganese(III): Investigation of solid-state versus solution Jahn-Teller effects, Inorg. Chem. 42, 4610-4618.
63. Voet, D., Voet, J. G., and Pratt, C. W. (1998) Fundamentals of Biochemistry, John Wiley and Sons, Inc., New York.
64. Stallings, W. C., Metzger, A. L., Pattridge, K. A., Fee, J. A., and Ludwig, M. L. (1991) Structure-function relationships in iron and manganese superoxide dismutases, Free Radical Res. Commun. 12-13, 259-268.
65. Dabrowiak, J. C., Nafie, L. A., Bryan, P. S., and Torkelson, A. T. (1977) Accessibility of manganese oxidation states. Control of pentaaza macrocyclic ligands, Inorg. Chem. 16, 540-544.
66. Maliekal, J., Karapetian, A., Vance, C., Yikilmaz, E., Wu, Q., Jackson, T., Brunold, T. C., Spiro, T. G., and Miller, A.-F. (2002) Comparison and contrasts between the active site pKs of Mn-superoxide dismutase and those of Fe-superoxide dismutase, J. Am. Chem. Soc. 124, 15064-15075.
67. Guan, Y., Hickey, M. J., Borgstahl, G. E. O., Hallewell, R. A., Lepock, J. R., O'Connor, D., Hsieh, Y. S., Nick, H. S., Silverman, D. N., and Tainer, J. A. (1998) Crystal structure of Y34F mutant human mitochondrial manganese superoxide dismutase and the functional role of tyrosine 34, Biochemistry 37, 4722-4730.
68. Hsieh, Y. S., Guan, Y., Tu, C. K., Bratt, P. J., Angerhofer, A., Lepock, J. R., Hickey, M. J., Tainer, J. A., Nick, H. S., and Silverman, D. N. (1998) Probing the active site of human manganese superoxide dismutase: The role of glutamine 143, Biochemistry 37, 4731-4739.
69. Lévêque, V. J.-P., Stroupe, M. E., Lepock, J. R., Cabelli, D. E., Tainer, J. A., Nick, H. S., and Silverman, D. N. (2000) Multiple replacements of glutamine 143 in human manganese superoxide dismutase: Effects on structure, stability, and catalysis, Biochemistry 39, 7131-7137.
70. Oganesyan, V. S., George, S. J., Cheesman, M. R., and Thomson, A. J. (1999) A novel, general method of analyzing magnetic circular dichroism spectra and magnetization curves of high-spin metal ions: Application to the protein oxidized rubredoxin, Desulfovibrio gigas, J. Chem. Phys. 110, 762-777.
71. Kirk, M. L., and Peariso, K. (2003) Recent applications of MCD spectroscopy to metalloenzymes, Curr. Opin. Chem. Biol. 7, 220-227.
72. 2O, Inorg. Chem. 18, 3511-3519.
73. Whittaker, M. M., and Whittaker, J. W. (1997) Mutagenesis of a proton linkage pathway in Escherichia coli manganese superoxide dismutase, Biochemistry 36, 8923-8931.
74. Miller, A.-F. (2004) Superoxide dismutases: Active sites that save, but a protein that kills, Curr. Opin. Chem. Biol. 8, 162-168.
75. Hearn, A. S., Fan, L., Lepock, J. R., Luba, J. P., Greenleaf, W. B., Cabelli, D. E., Tainer, J. A., Nick, H. S., and Silverman, D. N. (2004) Amino acid substitution at the dimeric interface of human manganese superoxide dismutase, J. Biol. Chem. 279, 5861-5866.
76. Ramilo, C. A., Lévêque, V., Guan, Y., Lepock, J. R., Tainer, J. A., Nick, H. S., and Silverman, D. N. (1999) Interrupting the hydrogen bond network at the active site of human manganese superoxide dismutase, J. Biol. Chem. 274, 27711-27716.
77. Edwards, R. A., Whittaker, M. M., Whittaker, J. W., Baker, E. N., and Jameson, G. B. (2001) Removing a hydrogen bond in the dimer interface of Escherichia coli manganese superoxide dismutase alters structure and reactivity, Biochemistry 40, 4622-4632.