Resolving complexity in the interactions of redox enzymes and their inhibitors: Contrasting mechanisms for the inhibition of a cytochrome c nitrite reductase revealed by protein film voltammetry

Biochemistry

Volumn 43, Issue 47, 2004, Pages 15086-15094

  Gwyer, James D ^a   Richardson, David J ^a   Butt, Julea N ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CATALYSIS; COMPUTATIONAL COMPLEXITY; CYANIDES; DIMERS; OXIDATION; PROTEINS; REDUCTION;

CATALYTIC PROPERTIES; PROTEIN FILM VOLTAMMETRY (PFV); REDOX ENZYMES;

ENZYMES;

CYANIDE; CYTOCHROME C; CYTOCHROME C NITRITE REDUCTASE; ENZYME; ENZYME INHIBITOR; NITRITE REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME MECHANISM; MICHAELIS CONSTANT; NONHUMAN; OXIDATION; POTENTIOMETRY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REDUCTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AZIDES; BINDING SITES; CATALYSIS; CYANIDES; CYTOCHROME C GROUP; CYTOCHROMES A1; CYTOCHROMES C1; DIMERIZATION; ELECTROCHEMISTRY; ENZYME ACTIVATION; ENZYME INHIBITORS; ESCHERICHIA COLI; HEME; KINETICS; MODELS, MOLECULAR; NITRATE REDUCTASES; NITRITES; OXIDATION-REDUCTION; POTENTIOMETRY; SPECTROPHOTOMETRY;

EID: 9744272379     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049085x     Document Type: Article

References (34)

1. Sharp, R. E., and Chapman, S. K. (1999) Mechanisms for regulating electron transfer in multi-centre redox proteins, Biochim. Biophys. Acta 1432, 143-158.
2. Davidson, V. L. (2002) Chemically gated electron transfer. A means of accelerating and regulating rates of biological electron transfer, Biochemistry 41, 14633-14636.
3. Armstrong, F. A., Heering, H. A., and Hirst, J. (1997) Reactions of complex metalloproteins studied by protein film voltammetry, Chem. Soc. Rev. 26, 169-179.
4. Heering, H. A., Hirst, J., and Armstrong, F. A. (1998) Interpreting the catalytic voltammetry of electroactive enzymes adsorbed on electrodes, J. Phys. Chem. B 102, 6889-6902.
5. Léger, C., Elliott, S. J., Hoke, K. R., Jeuken, L. J. C., Jones, A. K., and Armstrong, F. A. (2003) Enzyme electrokinetics: using protein film voltammetry to investigate redox enzymes and their mechanisms, Biochemistry 42, 8653-8662.
6. Armstrong, F. A. (2002) Insights from protein film voltammetry into mechanisms of complex biological electron-transfer reactions, J. Chem. Soc., Dalton Trans., 661-671.
7. Elliott, S. J., Léger, C., Pershad, H. R., Hirst, J., Heffron, K., Ginet, N., Blasco, F., Rothery, R. A., Weiner, J. H., and Armstrong, F. A. (2002) Detection and interpretation of redox potential optima in the catalytic activity of enzymes, Biochim. Biophys. Acta 1555, 54-59.
8. Butt, J. N. (2003) Fresh perspectives on nitrogen-cycle enzymes from protein film voltammetry, Recent Res. Dev. Biochem. 4, 159-180.
9. + by the catalytic (I λ) subcomplex of mitochondrial NADH:ubiquinone oxidoreductase (complex I), J. Am. Chem. Soc. 125, 6020-6021.
10. Jones, A. K., Lamle, S. E., Pershad, H. R., Vincent, K. A., Albracht, S. P. J., and Armstrong, F. A. (2003) Enzyme electrokinetics: electrochemical studies of the anaerobic interconversions between active and inactive states of Allochromatium vinosum [NiFe]-hydrogenase, J. Am. Chem. Soc. 125, 8505-8514.
11. Anderson, L. J., Richardson, D. J., and Butt, J. N. (2001) Catalytic protein film voltammetry from a respiratory nitrate reductase provides evidence for complex electrochemical modulation of enzyme activity, Biochemistry 40, 11294-11307.
12. Heering, H. A., Weiner, J. H., and Armstrong, F. A. (1997) Direct detection and measurement of electron relays in a multicentered enzyme: voltammetry of electrode-surface films of E. coli fumarate reductase, an iron-sulfur flavoprotein, J. Am. Chem. Soc. 119, 11628-11638.
13. Heffron, K., Léger, C., Rothery, R. A., Weiner, J. H., and Armstrong, F. A. (2001) Determination of an optimal potential window for catalysis by E. coli dimethyl sulfoxide reductase and hypothesis on the role of Mo(V) in the reaction pathway, Biochemistry 40, 3117-3126.
14. Frangioni, B., Arnoux, P., Sabaty, M., Pignol, D., Bertrand, P., Guigliarelli, B., and Léger, C. (2004) In Rhodobacter sphaeroides respiratory nitrate reductase, the kinetics of substrate binding favors intramolecular electron transfer, J. Am. Chem. Soc. 126, 1328-1329.
15. Angove, H., Cole, J. A., Richardson, D. J., and Butt, J. N. (2002) Protein film voltammetry reveals distinctive fingerprints of nitrite and hydroxylamine reduction by a cytochrome c nitrite reductase, J. Biol. Chem. 277, 23374-23381.
16. Bamford, V., Angove, H., Seward, H., Thomson, A. J., Cole, J. A., Butt, J. N., Hemmings, A. M., and Richardson, D. J. (2002) Structure and spectroscopy of the periplasmic cytochrome c nitrite reductase from Escherichia coli, Biochemistry 41, 2921-2931.
17. Einsle, O., Messerschmidt, A., Huber, R., Kroneck, P. M. H., and Neese, F. (2002) Mechanism of the six-electron reduction of nitrite to ammonia by cytochrome c nitrite reductase, J. Am. Chem. Soc. 124, 11737-11745.
18. Elliott, S. J., Hoke, K. R., Heffron, K., Palak, M., Rothery, R. A., Weiner, J. H., and Armstrong, F. A. (2004) Voltammetric studies of the catalytic mechanism of the respiratory nitrate reductase from Escherichia coli: how nitrate reduction and inhibition depend on the oxidation state of the active site, Biochemistry 43, 799-807.
19. Kajie, S., and Anraku, Y. (1986) Purification of a hexaheme cytochrome c552 from Escherichia coli K12 and its properties as a nitrite reductase, Eur. J. Biochem. 154, 457-463.
20. Einsle, O., Stach, P., Messerschmidt, A., Simon, J., Kröger, A., Huber, R., and Kroneck, P. M. H. (2000) Cytochrome c nitrite reductase from Wolinella succinogenes. Structure at 1.6 Å resolution, inhibitor binding, and heme-packing motifs, J. Biol. Chem. 275, 39608-39616.
21. Vogel, A. (1961) A Textbook of Quantitative Inorganic Analysis, pp 271-278, Longmans, London.
22. Cornish-Bowden, A. (2001) Fundamentals of Enzyme Kinetics, pp 93-128, Portland Press, London.
23. Gwyer, J. D., Angove, H. C., Richardson, D. J., and Butt, J. N. (2004) Redox-triggered events in cytochrome c nitrite reductase, Bioelectrochemistry 63, 43-47.
24. 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.
25. 1 nitrite reductase from Paracoccus pantotrophus, J. Biol. Chem. 275, 25089-25094.
26. Crane, B. R., Siegel, L. M., and Getzoff, E. D. (1997) Probing the catalytic mechanism of sulfite reductase by X-ray crystallography: structures of the Escherichia coli hemoprotein in complex with substrates, inhibitors, intermediates, and products, Biochemistry 36, 12120-12137.
27. Leys, D., Backers, K., Meyer, T. E., Hagen, W. R., Cusanovich, M. A., and van Beeumen, J. J. (2000) Crystal structures of an oxygen-binding cytochrome c from Rhodobacter sphaeroides, J. Biol. Chem. 275, 16050-16056.
28. Lawson, D. M., Stevenson, C. E. M., Andrew, C. R., and Eady, R. R. (2000) Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase, EMBO J. 19, 5661-5671.
29. Logan, M. S. P., Balny, C., and Hooper, A. B. (1995) Reaction with cyanide of hydroxylamine oxidoreductase of Nitrosomonas europaea, Biochemistry 34, 9028-9037.
30. 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.
31. Eaves, D. J., Grove, J., Staudenmann, W., James, P., Poole, R. K., White, S. A., Griffiths, I., and Cole, J. A. (1998) Involvement of products of the nrfEFG genes in the covalent attachment of haem c to a novel cysteine-lysine motif in the cytochrome c552 nitrite reductase from Escherichia coli, Mol. Microbiol. 28, 205-216.
32. Pisa, R., Stein, T., Eichler, R., Gross, R., and Simon, J. (2002) The nrfI gene is essential for the attachment of the active site haem group of Wolinella succinogenes cytochrome c nitrite reductase, Mol. Microbiol. 43, 763-770.
33. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification, FEMS Microbiol. Rev. 26, 285-309.
34. Gadsby, P. M. A., and Thomson, A. J. (1990) Assignment of the axial ligands of ferric-ion in low-spin hemoproteins by near-infrared magnetic circular dichroism and electron paramagnetic resonance spectroscopy, J. Am. Chem. Soc. 112, 5003-5011.