Redox equilibria in hydroxylamine oxidoreductase. Electrostatic control of electron redistribution in multielectron oxidative processes

Biochemistry

Volumn 44, Issue 6, 2005, Pages 1856-1863

  Kurnikov, Igor V ^a   Ratner, Mark A ^a   Pacheco, A Andrew ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELECTROCHEMISTRY; ELECTROSTATICS; ENZYMES; HYDROXYLATION; OXIDATION; PROTEINS; REDOX REACTIONS; SOLVENTS; TITRATION;

ELECTRON TRANSFER; ELECTROSTATIC INTERACTIONS; HYDROXYLAMINE OXIDOREDUCTASE (HAO); REDOX POTENTIALS;

AMINES;

HEME DERIVATIVE; HYDROXYLAMINE OXIDASE;

ARTICLE; CALCULATION; ELECTROCHEMICAL ANALYSIS; ELECTRON; ELECTRON TRANSPORT; ENZYME MECHANISM; ENZYME SUBUNIT; OXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL;

BACTERIAL PROTEINS; COMPUTER SIMULATION; ELECTRON TRANSPORT; ELECTROSTATICS; HEME; MODELS, CHEMICAL; MODELS, MOLECULAR; OXIDATION-REDUCTION; OXIDOREDUCTASES; POTENTIOMETRY; PROTONS;

EID: 13644249873     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048060v     Document Type: Article

References (52)

1. Ehrlich, H. L. (2002) Geomicrobiology, Marcel Dekker, New York.
2. Fenchel, T., King, G. M., and Blackburn, T. H. (1998) Bacterial Biogeochemistry, 2nd ed., Academic Press, London.
3. Hooper, A. B., and Nason, A. (1965) Characterization of hydroxylamine-cytochrome c reductase from chemoautotrophs Nitrosomonas europaea and Nitrosocystis oceanus, J. Biol. Chem. 240, 4044-4057.
4. 3 by Nitrosomonas: N-15-NMR evidence, FEBS Lett. 164, 236-240.
5. Ferguson, S. J. (1998) Nitrogen cycle enzymology, Curr. Opin. Chem. Biol. 2, 182-193.
6. Hooper, A. B. (1989) Biochemistry of the Nitrifying Lithoautotrophic Bacteria, in Autotrophic Bacteria (Schlegel, H. G., and Bowien, B., Eds.) pp 239-265, Science Tech Publishers, Madison, WI.
7. Prince, R. C., and George, G. N. (1997) The remarkable complexity of hydroxylamine oxidoreductase, Nat. Struct. Biol. 4, 247-250.
8. Kroneck, P. M. H., Beuerle, J., and Schumacher, W. (1992) Metal Dependent Conversion of Inorganic Nitrogen and Sulfur Compounds, in Metal Ions in Biological Systems (Sigel, H., and Sigel, A., Eds.) pp 455-505, Marcel Dekker, New York.
9. Wood, P. M. (1988) Monooxygenase and free radical mechanisms for biological ammonia oxidation, in The Nitrogen and Sulfur Cycles (Cole, J. A., and Ferguson, S. J., Eds.) pp 219-243, Cambridge University Press, New York.
10. Bock, E., Koops, H.-P., Harms, H., and Ahlers, B. (1991) The biochemistry of nitrifying organisms, in Variations in Autotrophic Life (Shively, J. M., and Barton, L. L., Eds.) pp 171-200, Academic Press, San Diego.
11. Schlegel, H. G. (1981) Microorganisms involved in the nitrogen and sulfur cycles, in Biology of Inorganic Nitrogen and Sulfur (Bothe, H., and Trebst, A., Eds.) pp 3-12, Springer-Verlag, New York.
12. Biological Nitrogen Fixation (1994) pp 6-32, National Academy Press, Washington, DC.
13. Burns, R. C., and Hardy, R. W. F. (1975) Nitrogen Fixation in Bacteria and Higher Plants, Springer-Verlag, New York.
14. Einsle, O., Messerschmidt, A., Stach, P., Bourenkov, G. P., Bartunik, H. D., Huber, R., and Kroneck, P. M. H. (1999) Structure of cytochrome c nitrite reductase, Nature 400, 476-480.
15. Leys, D., Meyer, T. E., Tsapin, A. S., Nealson, K. H., Cusanovich, M. A., and Van Beeumen, J. J. (2002) Crystal structures at atomic resolution reveal the novel concept of "electron-harvesting" as a role for the small tetraheme cytochrome c, J. Biol. Chem. 277, 35703-35711.
16. Iverson, T. M., Arciero, D. M., Hsu, B. T., Logan, M. S. P., Hooper, A. B., and Rees, D. C. (1998) Heme packing motifs revealed by the crystal structure of the tetra-heme cytochrome c554 from Nitrosomonas europaea, Nat. Struct. Biol. 5, 1005-1012.
17. Leys, D., Tsapin, A. S., Nealson, K. H., Meyer, T. E., Cusanovich, M. A., and Van Beeumen, J. J. (1999) Structure and mechanism of the flavocytochrome c fumarate reductase of Shewanella putrefaciens MR-1, Nat. Struct. Biol. 6, 1113-1117.
18. Hooper, A. B., Maxwell, P. C., and Terry, K. R. (1978) Hydroxylamine oxidoreductase from Nitrosomonas: Absorption-spectra and content of heme and metal, Biochemistry 17, 2984-2989.
19. Yamanaka, T., Shinra, M., Takahashi, K., and Shibasaka, M. (1979) Highly purified hydroxylamine oxidoreductase derived from Nitrosomonas europaea, J. Biochem. 86, 1101-1108.
20. Igarashi, N., Moriyama, H., Fujiwara, T., Fukumori, Y., and Tanaka, N. (1997) The 2.8 Å structure of hydroxylamine oxidoreductase from a nitrifying chemoautotrophic bacterium, Nitrosomonas europaea, Nat. Struct. Biol. 4, 276-284.
21. Hooper, A. B., and Terry, K. R. (1977) Hydroxylamine Oxidoreductase from Nitrosomonas: Inactivation by Hydrogen Peroxide, Biochemistry 16, 455-459.
22. Hendrich, M. P., Logan, M., Andersson, K. K., Arciero, D. M., Lipscomb, J. D., and Hooper, A. B. (1994) The Active-Site of Hydroxylamine Oxidoreductase from Nitrosomonas: Evidence for a New Metal Cluster in Enzymes. J. Am. Chem. Soc. 116, 11961-11968.
23. Logan, M. S. P., Balny, C., and Hooper, A. B. (1995) Reaction with cyanide of hydroxylamine oxidoreductase of Nitrosomonas europaea, Biochemistry 34, 9028-9037.
24. Logan, M. S. P., and Hooper, A. B. (1995) Suicide inactivation of hydroxylamine oxidoreductase of Nitrosomonas europaea by organohydrazines, Biochemistry 34, 9257-9264.
25. Arciero, D. M., and Hooper, A. B. (1993) Hydroxylamine oxidoreductase from Nitrosomonas europaea is a multimer of an octa-heme subunit, J. Biol. Chem. 268, 14645-14654.
26. Arciero, D. M., Collins, M. J., Haladjian, J., Bianco, P., and Hooper, A. B. (1991) Resolution of the 4 hemes of cytochrome-c554 from Nitrosomonas europaea by redox potentiometry and optical spectroscopy, Biochemistry 30, 11459-11465.
27. Arciero, D. M., Balny, C., and Hooper, A. B. (1991) Spectroscopic and rapid kinetic-studies of reduction of cytochrome-c554 by hydroxylamine oxidoreductase from Nitrosomonas europaea. Biochemistry 30, 11466-11472.
28. Collins, M. J., Arciero, D. M., and Hooper, A. B. (1993) Optical spectropotentiometric resolution of the hemes of hydroxylamine oxidoreductase: Heme quantitation and pH-dependence of E(m), J. Biol. Chem. 268, 14655-14662.
29. Prince, R. C., and Hooper, A. B. (1987) Resolution of the hemes of hydroxylamine oxidoreductase by redox potentiometry and electron-spin-resonance spectroscopy, Biochemistry 26, 970-974.
30. Arciero, D. M., Golombeck, A., Hendrich, M. P., and Hooper, A. B. (1998) Correlation of optical and EPR signals with the P460 heme of hydroxylamine oxidoreductase from Nitrosomonas europaea, Biochemistry 37, 523-529.
31. Hendrich, M. P., Petasis, D., Arciero, D. M., and Hooper, A. B. (2001) Correlations of structure and electronic properties from EPR spectroscopy of hydroxylamine oxidoreductase, J. Am. Chem. Soc. 123, 2997-3005.
32. Popovic, D. M., Zaric, S. D., Rabenstein, B., and Knapp, E. W. (2001) Artificial cytochrome b: Computer modeling and evaluation of redox potentials, J. Am. Chem. Soc. 123, 6040-6053.
33. Mao, J., Hauser, K., and Gunner, M. R. (2003) How cytochromes with different folds control heme redox potentials, Biochemistry 42, 9829-9838.
34. Stephens, P. J., Jollie, D. R., and Warshel, A. (1996) Protein control of redox potentials of iron-sulfur proteins, Chem. Rev. 96, 2491-2513.
35. Simonson, T. (2001) Macromolecular electrostatics: Continuum models and their growing pains, Curr. Opin. Struct. Biol. 11, 243-252.
36. Rogers, N. K., and Moore, G. R. (1988) Spectroscopic identification of the heme ligands of cellobiose oxidase, FEBS Lett. 228, 69-73.
37. Wilson, G. S. (1974) Electrochemical studies of porphyrin redox reactions as cytochrome models, Bioelectrochem. Bioenerg. 1, 172-179.
38. Moore, G. R., and Pettigrew, G. W. (1990) Redox Potentials, in Cytochromes c: Evolutionary, structural and physiological aspects, pp 309-362, Springer, Berlin.
39. Bashford, D., and Karplus, M. (1991) Multiple-site titration curves of proteins: An analysis of exact and approximate methods for their calculation, J. Phys. Chem. 95, 9556-9561.
40. Antosiewicz, J., Mccammon, J. A., and Gilson, M. K. (1994) Prediction of pH-dependent properties of proteins, J. Mol. Biol. 238, 415-436.
41. as in proteins, Biochemistry 35, 7819-7833.
42. as in proteins, Biophys. J. 83, 1731-1748.
43. Beroza, P., and Case, D. (1996) Including side chain flexibility in continuum electrostatic calculations of protein titration, J. Phys. Chem. 100, 20156-20163.
44. Sham, Y. Y., Muegge, I., and Warshel, A. (1998) The effect of protein relaxation on charge-charge interactions and dielectric constants of proteins, Biophys. J. 74, 1744-1753.
45. Mujica, V., Nitzan, A., Mao, Y., Davis, W., Kemp, M., and Ratner, M. A. (1999) Electron transfer in molecules and molecular wires: Geometry dependence, coherent transfer, and control, Adv. Chem. Phys. 107, 403-429.
46. Grabert, H., and Devoret, M. H. (1992) Single Charge Tunneling: Coulomb Blockade Phenomena in Nanostructures, Plenum, New York.
47. 554 from Nitrosomonas europaea, J. Am. Chem. Soc. 125, 1738-1747.
48. 5 is modulated by its exposed heme edge, Biochemistry 37, 1485-1494.
49. 5, Faraday Discuss. 116, 221-234.
50. Marcus, R. A., and Sutin, N. (1985) Electron transfers in chemistry and biology, Biochim. Biophys. Acta 811, 265-322.
51. Bendall, D. S., Ed. (1996) Protein Electron Transfer, Bios Scientific Publishers, Oxford, U.K.
52. Balzani, V., Ed. (2001) Electron Transfer in Chemistry, Vols. 1-5, Wiley, Weinheim, Germany.