Global effects of the energetics of coenzyme binding: NADPH controls the protein interaction properties of human cytochrome P450 reductase

Biochemistry

Volumn 45, Issue 5, 2006, Pages 1421-1434

  Grunau, Alex ^a   Paine, Mark J ^b   Ladbury, John E ^c   Gutierrez, Aldo ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOCHEMISTRY; CALORIMETRY; PROTEINS; REDOX REACTIONS; SPECIFIC HEAT; THERMODYNAMICS; TITRATION;

ADENOSINE MOIETY; CYTOCHROME P450 REDUCTASE (CPR); PROTEIN INTERACTION PROPERTIES; RAPID MIXING MEASUREMENTS;

ENZYMES;

2',5' ADENOSINE DINUCLEOTIDE PHOSPHATE; ADENOSINE; CYTOCHROME C; CYTOCHROME P450 REDUCTASE; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CALORIMETRY; COENZYME; DIFFUSION; ENERGY TRANSFER; ENTROPY; ENZYME BINDING; HALF LIFE TIME; HUMAN; ISOTHERMAL TITRATION CALORIMETRY; KINETICS; MOLECULAR RECOGNITION; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SPECTROPHOTOMETRY; STOICHIOMETRY; TEMPERATURE; THERMODYNAMICS;

ADENOSINE DIPHOSPHATE; CALORIMETRY; COENZYMES; CYTOCHROMES C; HUMANS; KINETICS; NADP; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDATION-REDUCTION; PHOSPHATES; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; TEMPERATURE; THERMODYNAMICS; TITRIMETRY;

EID: 32244437847     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052115r     Document Type: Article

References (60)

1. Sem, D. S., and Kasper, C. B. (1994) Kinetic mechanism for the model reaction of NADPH-cytochrome P450 oxidoreductase with cytochrome c, Biochemistry 33, 12012-12021.
2. Enoch, H. G., and Strittmatter, P. (1979) Cytochrome b5 reduction by NADPH-cytochrome P-450 reductase, J. Biol. Chem. 254, 8976-8981.
3. Schacter, B. A., Nelson, E. B., Marver, H. S., and Masters, B. S. (1972) Immunochemical evidence for an association of heme oxygenase with the microsomal electron transport system, J. Biol. Chem. 247, 3601-3607.
4. Ilan, Z., Ilan, R., and Cinti, D. L. (1981) Evidence for a new physiological role of hepatic NADPH:ferricytochrome (P-450) oxidoreductase. Direct electron input to the microsomal fatty acid chain elongation system, J. Biol. Chem. 256, 10066-10072.
5. Bailey, S. M., Lewis, A. D., Patterson, L. H., Fisher, G. R., Knox, R. J., and Workman, P. (2001) Involvement of NADPH:cytochrome P450 reductase in the activation of indoloquinone EO9 to free radical and DNA damaging species, Biochem. Pharmacol. 62, 461-468.
6. Saunders, M. P., Jaffar, M., Patterson, A. V., Nolan, J., Naylor, M. A., Phillips, R. M., Harris, A. L., and Stratford, I. J. (2000) The relative importance of NADPH:cytochrome c (P450) reductase for determining the sensitivity of human tumour cells to the indolequinone EO9 and related analogues lacking functionality at the C-2 and C-3 positions, Biochem. Pharmacol. 59, 993-996.
7. Jaffar, M., Williams, K. J., and Stratford, I. J. (2001) Bioreductive and gene therapy approaches to hypoxic diseases, Adv. Drug Delivery Rev. 53, 217-228.
8. Rooseboom, M., Commandeur, J. N., and Vermeulen, N. P. (2004) Enzyme-catalyzed activation of anticancer prodrugs, Pharmacol. Rev. 56, 53-102.
9. Porter, T. D., and Kasper, C. B. (1986) NADPH-cytochrome P-450 oxidoreductase: Flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins, Biochemistry 25, 1682-1687.
10. Gutierrez, A., Grunau, A., Paine, M., Munro, A. W., Wolf, C. R., Roberts, G. C., and Scrutton, N. S. (2003) Electron transfer in human cytochrome P450 reductase, Biochem. Soc. Trans. 31, 497-501.
11. Gutierrez, A., Paine, M., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2002) Relaxation kinetics of cytochrome P450 reductase: Internal electron transfer is limited by conformational change and regulated by coenzyme binding, Biochemistry 41, 4626-4637.
12. Gutierrez, A., Munro, A. W., Grunau, A., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2003) Interflavin electron transfer in human cytochrome P450 reductase is enhanced by coenzyme binding. Relaxation kinetic studies with coenzyme analogues, Eur. J. Biochem. 270, 2612-2621.
13. Murataliev, M., Klein, M., Fulco, A., and Feyeresien, R. (1997) Functional interactions in cytochrome P450BM3: Flavin semiquinone intermediates, role of NADP(H), and mechanism of electron transfer by the flavoprotein domain, Biochemistry 36, 8401-8412.
14. Murataliev, M. B., and Feyereisen, R. (2000) Interaction of NADP-(H) with oxidized and reduced P450 reductase during catalysis. Studies with nucleotide analogues, Biochemistry 39, 5066-5074.
15. Craig, H. D., Chapman, S. K., and Daff, S. (2002) Calmodulin activates electron transfer through neuronal nitric-oxide synthase reductase domain by releasing an NADPH-dependent conformational lock, J. Biol. Chem. 277, 33987-33994.
16. Murataliev, M. B., Feyereisen, R., and Walker, F. A. (2004) Electron transfer by diflavin reductases, Biochim. Biophys. Acta 1698, 1-26.
17. Dill, K., and Bromberg, S. (2003) Molecular driving forces, Garland Science, London.
18. Smith, G. C., Tew, D. G., and Wolf, C. R. (1994) Dissection of NADPH-cytochrome P450 oxidoreductase into distinct functional domains, Proc. Natl. Acad. Sci. U.S.A. 91, 8710-8714.
19. Gutierrez, A., Lian, L.-Y., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2001) Stopped-flow kinetic studies of flavin reduction in human cytochrome P450 reductase and its component domains, Biochemistry 40, 1964-1975.
20. Fisher, H. F., and Singh, N. (1995) Calorimetric methods for interpreting protein-ligands interactions, Methods Enzymol. 259, 194-221.
21. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter, Anal. Biochem. 179, 131-137.
22. Ellis, K. J., and Morrison, J. F. (1982) Buffers of constant ionic strength for studying pH-dependent processes, Methods Enzymol. 87, 405-426.
23. Bielmann, J.-F., and Jung, M. J. (1971) Mechanism of alcohol dehydrogenases from yeast and horse liver, Eur. J. Biochem. 19, 130-134.
24. Munro, A. W., Noble, M. A., Robledo, L., Daff, S. N., and Chapman, S. K. (2001) Determination of the redox properties of human NADPH-cytochrome P450 reductase, Biochemistry 40, 1956-1963.
25. Pettigrew, G. W., and Moore, G. R (1987) Cytochromes c. Biological aspects, pp 83-84, Springer-Verlag, Berlin.
26. + reductase revealed by protein engineering and crystallographic studies, Nat. Struct. Biol. 6, 847-853.
27. + reductase, J. Biol. Chem. 275, 10472-10476.
28. Roitel, O., Scrutton, N. S., and Munro, A. W. (2003) Electron transfer in flavocytochrome P450BM3: Kinetics of flavin reduction and oxidation, the role of cysteine 999, and relationships with mammalian cytochrome P450 reductase, Biochemistry 42, 10809-10821.
29. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd ed., Chapter 3, pp 63-65, Kluwer Academic/Plenum Publishers: New York.
30. Wang, M., Roberts, D. L., Paschke, R., Shea, T. M., Masters, B. S., and Kim, J. J. (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: Prototype for FMN- and FAD-containing enzymes, Proc. Natl. Acad. Sci. U.S.A. 94, 8411-8416.
31. Sturtevant, J. M. (1977) Heat capacity and entropy changes in processes involving proteins, Proc. Natl. Acad. Sci. U.S.A. 74, 2236-2240.
32. Luque, I., Todd, M. J., Gomez, J., Semo, N., and Freire, E. (1998) Molecular basis of resistance to HIV-1 protease inhibition: A plausible hypothesis, Biochemistry 37, 5791-5797.
33. Spolar, R. S., and Record, M. T., Jr. (1994) Coupling of local folding to site-specific binding of proteins to DNA, Science 263, 777-784.
34. Gomez, J., Hilser, V. J., Xie, D., and Freire, E. (1995) The heat capacity of proteins, Proteins 22, 404-412.
35. Sem, D. S., and Kasper, C. B. (1993) Enzyme-substrate binding interactions of NADPH-cytochrome P-450 oxidoreductase characterized with pH and alternate substrate/inhibitor studies, Biochemistry 32, 11539-11547.
36. Bastiaens, P. I., Bonants, P. J., Muller, F., and Visser, A. J. (1989) Time-resolved fluorescence spectroscopy of NADPH-cytochrome P-450 reductase: Demonstration of energy transfer between the two prosthetic groups, Biochemistry 28, 8416-8425.
37. Bergqvist, S., Williams, M. A., O'Brien, R., and Ladbury, J. E. (2004) Heat capacity effects of water molecules and ions at a protein-DNA interface, J. Mol. Biol. 336, 829-842.
38. Gutierrez, A., Doehr, O., Paine, M., Wolf, C. R., Scrutton, N. S., and Roberts, G. C. (2000) Trp-676 facilitates nicotinamide coenzyme exchange in the reductive half-reaction of human cytochrome P450 reductase: Properties of the soluble W676H and W676A mutant reductases, Biochemistry 39, 15990-15999.
39. Mathews, F. S., Mauk, A. G., and Moore, G. R. (2000) Protein-protein complexes formed by electron transfer proteins. In Protein-Protein Recognition (Kleanthous, C., Ed.) Frontiers in Molecular Biology Series, Oxford Press, Oxford, U.K.
40. Koppenol, W. H., Rush, J. D., Mills, J. D., and Margoliash, E. (1991) The dipole moment of cytochrome c, Mol. Biol. Evol 8, 545-558.
41. Zhao, Q., Modi, S., Smith, G., Paine, M., McDonagh, P. D., Wolf, C. R., Tew, D., Lian, L.-Y., Roberts, G. C., and Driessen, H. P. (1999) Crystal structure of the FMN-binding domain of human cytochrome P450 reductase at 1.93 Å resolution, Protein Sci. 8, 298-306.
42. 13C NMR resonance assignment, secondary structure and global fold of the FMN-binding domain of human cytochrome P450 reductase, J. Biol. NMR 10, 63-75.
43. Murataliev, M. B., and Feyereisen, R. (1999) Mechanism of cytochrome P450 reductase from the housefly: Evidence for an FMN semiquinone as electron donor, FEBS Lett. 453, 201-204.
44. Pettigrew, G. W., Goodhew, C. F., Cooper, A., Nutley, M., Jumel, K., and Harding, S. E. (2003) The electron transfer complexes of cytochrome c peroxidase from Paracoccus denitrificans, Biochemistry 42, 2046-2055.
45. Nisimoto, Y. (1986) Localization of cytochrome c-binding domain on NADPH-cytochrome P-450 reductase, J. Biol. Chem. 261, 14232-14239.
46. 5, cytochrome c, and cytochrome P450 interactions with NADPH-cytochrome P450 reductase in phospholipids vesicles, Biochemistry 27, 5869-5876.
47. + reductase by site-directed mutagenesis, J. Biol. Chem. 276, 11902-11912.
48. Knight, K., and Scrutton, N. S. (2002) Stopped-flow kinetic studies of electron transfer in the reductase domain of neuronal nitric oxide synthase: Re-evaluation of the kinetic mechanism reveals new enzyme intermediates and variation with cytochrome P450 reductase, Biochem. J. 367, 19-30.
49. McLean, K. I., Scrutton, N. S., and Munro, A. W. (2003) Kinetic, spectroscopic and thermodynamic characterization of the Mycobacterium tuberculosis adrenodoxin reductase homologue FprA, Biochem. J. 372, 317-327.
50. Hubbard, P. A., Shen, A. L., Paschke, R., Kasper, C. B., and Kim, J. J. (2001) NADPH-cytochrome P450 oxidoreductase. Structural basis for hydride and electron transfer, J. Biol. Chem. 276, 29163-29170.
51. Zhang, J., Martasek, P., Paschke, R., Shea, T., Siler Masters, B. S., and Kim, J. J. (2001) Crystal structure of the FAD/NADPH-binding domain of rat neuronal nitric-oxide synthase. Comparisons with NADPH-cytochrome P450 oxidoreductase, J. Biol. Chem. 276, 37506-37513.
52. Daff, S. (2004) An appraisal of multiple NADPH binding-site models proposed for cytochrome P450 reductase, NO synthase, and related diflavin reductase systems, Biochemistry 43, 3929-3932.
53. Page, C. C., Moser, C. C., and Dutton, P. L. (2003) Mechanism for electron transfer within and between proteins, Curr. Opin. Chem. Biol. 7, 551-556.
54. Leys, D., Basran, J., Talfournier, F., Sutcliffe, M. J., and Scrutton, N. S. (2003) Extensive conformational sampling in a ternary electron-transfer complex, Nat. Struct. Biol. 10, 219-225.
55. 5, J. Am. Chem. Soc. 124, 6849-6859.
56. Shen, A. L., and Kasper, C. B. (1995) Role of Acidic Residues in the Interaction of NADPH-Cytochrome P450 Oxidoreductase with Cytochrome P450 and Cytochrome c, J. Biol. Chem. 270, 27475-27480.
57. Hall, D. A., Vander Kooi, C. W., Stasik, C. N., Stevens, S. Y., Zuiderweg, E. R. P., and Matthews, R. G. (2001) Mapping the interactions between flavodoxin and its physiological partners flavodoxin reductase and cobalamin-dependent methionine synthase, Proc. Natl. Acad. Sci. U.S.A. 98, 9521-9526.
58. BM3. Evidence that NADP(H) binding controls redox potentials of the flavin cofactors, Biochemistry 39, 12699-12707.
59. Oprian, D. D., and Coon, M. J. (1982) Oxidation-reduction states of FMN and FAD in NADPH-cytochrome P-450 reductase during reduction by NADPH, J. Biol. Chem. 257, 8935-8944.
60. Kraut, D. A., Carroll, K. S., and Herschlag, D. (2003) Challenges in enzyme mechanism and energetics, Annu. Rev. Biochem. 72, 517-571.