Role of the interface between the FMN and FAD domains in the control of redox potential and electronic transfer of NADPH-cytochrome P450 reductase

Biochemical Journal

Volumn 435, Issue 1, 2011, Pages 197-206

  Aigrain, Louise ^a   Pompon, Denis ^a   Truan, Gilles ^a  

^a CNRS   (France)

Author keywords

Electron transfer; Flavin mononucleotide (FMN); Flavin adenine dinucleotide (FAD); NADPH cytochrome P450 reductase (CPR); Redox potential

Indexed keywords

CYTOCHROME P450 REDUCTASE; FLAVINE ADENINE NUCLEOTIDE; FLAVINE MONONUCLEOTIDE; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BIOCHEMISTRY; CATALYSIS; CHIMERA; ELECTRONIC TRANSFER; ELECTRONICS; HUMAN; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT; YEAST;

BIOCATALYSIS; CYTOCHROME P-450 CYP3A; CYTOCHROMES C; FERRICYANIDES; FLAVIN MONONUCLEOTIDE; FLAVIN-ADENINE DINUCLEOTIDE; FUNGAL PROTEINS; HUMANS; KINETICS; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 79952819519     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101984     Document Type: Article

References (50)

1. Copley, R. R., Ponting, C. P., Schultz, J. and Bork, P. (2002) Sequence analysis of multidomain proteins: past perspectives and future directions. Adv. Protein Chem. 61, 75-98
2. Apic, G., Gough, J. and Teichmann, S. A. (2001) Domain combinations in archaeal, eubacterial and eukaryotic proteomes. J. Mol. Biol. 310, 311-325
3. Jones, S., Marin, A. and Thornton, J. M. (2000) Protein domain interfaces: characterization and comparison with oligomeric protein interfaces. Protein Eng. 13, 77-82
4. Han, J. H., Batey, S., Nickson, A. A., Teichmann, S. A. and Clarke, J. (2007) The folding and evolution of multidomain proteins. Nat. Rev. Mol. Cell Biol. 8, 319-330
5. Janin, J. and Wodak, S. J. (2002) Protein modules and protein-protein interaction. Introduction. Adv. Protein Chem. 61, 1-8
6. Kuriyan, J. and Eisenberg, D. (2007) The origin of protein interactions and allostery in colocalization. Nature 450, 983-990 (Pubitemid 350273628)
7. Wolf, Y. I., Kondrashov, A. S. and Koonin, E. V. (2000) Interkingdom gene fusions. Genome Biol. 1, RESEARCH0013
8. Garnaud, P. E., Koetsier, M., Ost, T. W. and Daff, S. (2004) Redox properties of the isolated flavin mononucleotide- and flavin adenine dinucleotide-binding domains of neuronal nitric oxide synthase. Biochemistry 43, 11035-11044 (Pubitemid 39433692)
9. Wolthers, K. R., Basran, J., Munro, A. W. and Scrutton, N. S. (2003) Molecular dissection of human methionine synthase reductase: determination of the flavin redox potentials in full-length enzyme and isolated flavin-binding domains. Biochemistry 42, 3911-3920 (Pubitemid 36402684)
10. + oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 18, 710-720
11. Kwasnicka, D. A., Krakowiak, A., Thacker, C., Brenner, C. and Vincent, S. R. (2003) Coordinate expression of NADPH-dependent flavin reductase, Fre-1, and Hint-related 7meGMP-directed hydrolase, DCS-1. J. Biol. Chem. 278, 39051-39058
12. Gruez, A., Pignol, D., Zeghouf, M., Coves, J., Fontecave, M., Ferrer, J. L. and Fontecilla-Camps, J. C. (2000) Four crystal structures of the 60 kDa flavoprotein monomer of the sulfite reductase indicate a disordered flavodoxin-like module. J. Mol. Biol. 299, 199-212
13. Murataliev, M. B., Feyereisen, R. and Walker, F. A. (2004) Electron transfer by diflavin reductases. Biochim. Biophys. Acta 1698, 1-26
14. 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
15. Hannemann, F., Bichet, A., Ewen, K. M. and Bernhardt, R. (2007) Cytochrome P450 systems: biological variations of electron transport chains. Biochim. Biophys. Acta 1770, 330-344
16. Grunau, A., Geraki, K., Grossmann, J. G. and Gutierrez, A. (2007) Conformational dynamics and the energetics of protein-ligand interactions: role of interdomain loop in human cytochrome P450 reductase. Biochemistry 46, 8244-8255 (Pubitemid 47075964)
17. Hawkins, A. R. and Lamb, H. K. (1995) The molecular biology of multidomain proteins: selected examples. Eur. J. Biochem. 232, 7-18
18. Lamb, D. C., Kim, Y., Yermalitskaya, L. V., Yermalitsky, V. N., Lepesheva, G. I., Kelly, S. L., Waterman, M. R. and Podust, L. M. (2006) A second FMN binding site in yeast NADPH-cytochrome P450 reductase suggests a mechanism of electron transfer by diflavin reductases. Structure 14, 51-61
19. 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
20. Hamdane, D., Xia, C., Im, S. C., Zhang, H., Kim, J. J. and Waskell, L. (2009) Structure and function of an NADPH-cytochrome P450 oxidoreductase in an open conformation capable of reducing cytochrome P450. J. Biol. Chem. 284, 11374-11384
21. Aigrain, L., Pompon, D., Morera, S. and Truan, G. (2009) Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase. EMBO Rep. 10, 742-747
22. Ellis, J., Gutierrez, A., Barsukov, I. L., Huang, W. C., Grossmann, J. G. and Roberts, G. C. (2009) Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small-angle X-ray scattering. J. Biol. Chem. 284, 36628-36637
23. Hay, S., Brenner, S., Khara, B., Quinn, A. M., Rigby, S. E. and Scrutton, N. S. (2010) Nature of the energy landscape for gated electron transfer in a dynamic redox protein. J. Am. Chem. Soc. 132, 9738-9745
24. 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
25. Louerat-Oriou, B., Perret, A. and Pompon, D. (1998) Differential redox and electron-transfer properties of purified yeast, plant and human NADPH-cytochrome P-450 reductases highly modulate cytochrome P-450 activities. Eur. J. Biochem. 258, 1040-1049
26. Garcin, E. D., Bruns, C. M., Lloyd, S. J., Hosfield, D. J., Tiso, M., Gachhui, R., Stuehr, D. J., Tainer, J. A. and Getzoff, E. D. (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J. Biol. Chem. 279, 37918-37927
27. Ilagan, R. P., Tiso, M., Konas, D. W., Hemann, C., Durra, D., Hille, R. and Stuehr, D. J. (2008) Differences in a conformational equilibrium distinguish catalysis by the endothelial and neuronal nitric-oxide synthase flavoproteins. J. Biol. Chem. 283, 19603-19615
28. Stuehr, D. J., Tejero, J. and Haque, M. M. (2009) Structural and mechanistic aspects of flavoproteins: electron transfer through the nitric oxide synthase flavoprotein domain. FEBS J. 276, 3959-3974
29. Welland, A., Garnaud, P. E., Kitamura, M., Miles, C. S. and Daff, S. (2008) Importance of the domain-domain interface to the catalytic action of the NO synthase reductase domain. Biochemistry 47, 9771-9780
30. Roman, L. J., McLain, J. and Masters, B. S. (2003) Chimeric enzymes of cytochrome P450 oxidoreductase and neuronal nitric-oxide synthase reductase domain reveal structural and functional differences. J. Biol. Chem. 278, 25700-25707
31. 5-encoding gene which suppresses ketoconazole hypersensitivity in a NADPH-P-450 reductase-deficient strain. Gene 142, 123-127
32. 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
33. 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
34. Das, A. and Sligar, S. G. (2009) Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer. Biochemistry 48, 12104-12112
35. Vermilion, J. L., Ballou, D. P., Massey, V. and Coon, M. J. (1981) Separate roles for FMN and FAD in catalysis by liver microsomal NADPH-cytochrome P-450 reductase. J. Biol. Chem. 256, 266-277
36. Shen, A. L., Porter, T. D., Wilson, T. E. and Kasper, C. B. (1989) Structural analysis of the FMN binding domain of NADPH-cytochrome P-450 oxidoreductase by site-directed mutagenesis. J. Biol. Chem. 264, 7584-7589
37. 5 rules uncoupling mechanisms. Biochemistry 37, 11412-11424
38. Backes, W. L. and Kelley, R. W. (2003) Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes. Pharmacol. Ther. 98, 221-233
39. + reductase with NADP(H) specificity and oxidation-reduction properties. J. Biol. Chem. 261, 11214-11223
40. Brenner, S., Hay, S., Munro, A. W. and Scrutton, N. S. (2008) Inter-flavin electron transfer in cytochrome P450 reductase: effects of solvent and pH identify hidden complexity in mechanism. FEBS J. 275, 4540-4557
41. 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
42. Barber, M. J., Pollock, V. and Spence, J. T. (1988) Microcoulometric analysis of trimethylamine dehydrogenase. Biochem. J. 256, 657-659
43. 1 electron-transferring flavoprotein (ETF) hydroquinone in the trimethylamine dehydrogenase · ETF protein complex. J. Biol. Chem. 275, 12546-12552
44. 1) electron-transferring flavoprotein affords approximately 200-millivolt stabilization of the FAD anionic semiquinone and a kinetic block on full reduction to the dihydroquinone. J. Biol. Chem. 276, 20190-20196
45. Murataliev, M. B. and Feyereisen, R. (2000) Functional interactions in cytochrome P450BM3: evidence that NADP(H) binding controls redox potentials of the flavin cofactors. Biochemistry 39, 12699-12707
46. 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 (Pubitemid 30241627)
47. 5. Biochem. Biophys. Res. Commun. 284, 937-941
48. Higashimoto, Y., Sato, H., Sakamoto, H., Takahashi, K., Palmer, G. and Noguchi, M. (2006) The reactions of heme- and verdoheme-heme oxygenase-1 complexes with FMN-depleted NADPH-cytochrome P450 reductase: electrons required for verdoheme oxidation can be transferred through a pathway not involving FMN. J. Biol. Chem. 281, 31659-31667
49. 145) are important for reconstitution of cytochrome P450 17α-hydroxylase activity. J. Biol. Chem. 272, 22509-22513
50. Jenkins, C. M. and Waterman, M.R. (1998) NADPH-flavodoxin reductase and flavodoxin from Escherichia coli: characteristics as a soluble microsomal P450 reductase. Biochemistry 37, 6106-6113 (Pubitemid 28196767)