Real-time analysis of conformational control in electron transfer reactions of human cytochrome P450 reductase with cytochrome c

FEBS Journal

Volumn 282, Issue 22, 2015, Pages 4357-4375

  Hedison, Tobias M ^a   Hay, Sam ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

cytochrome P450 reductase; diflavin oxidoreductase; electron transfer; F rster resonance energy transfer; protein domain dynamics

Indexed keywords

CYTOCHROME C; CYTOCHROME P450 REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME CONFORMATION; ENZYME MECHANISM; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENCE SPECTROSCOPY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN DOMAIN; STOICHIOMETRY; STRUCTURE ANALYSIS; CHEMISTRY; HUMAN; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; SPECTROFLUOROMETRY;

CYTOCHROMES C; ELECTRON TRANSPORT; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; NADPH-FERRIHEMOPROTEIN REDUCTASE; OXIDATION-REDUCTION; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE;

EID: 84955199886     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13501     Document Type: Article

References (43)

1. Zhuravlev PI, &, Papoian GA, (2010) Functional versus folding landscapes: the same yet different. Curr Opin Struct Biol 20, 16-22.
2. Henzler-Wildman K, &, Kern D, (2007) Dynamic personalities of proteins. Nature 450, 964-972.
3. Villali J, &, Kern D, (2010) Choreographing an enzyme's dance. Curr Opin Chem Biol 14, 636-643.
4. Benkovic SJ, Hammes GG, &, Hammes-Schiffer S, (2008) Free-energy landscape of enzyme catalysis. Biochemistry 47, 3317-3322.
5. Davidson VL, (2008) Protein control of true, gated, and coupled electron transfer reactions. Acc Chem Res 41, 730-738.
6. Leys D, Basran J, Talfournier F, Sutcliffe MJ, &, Scrutton NS, (2003) Extensive conformational sampling in a ternary electron transfer complex. Nat Struct Biol 10, 219-225.
7. Sobolewska-Stawiarz A, Leferink NGH, Fisher K, Heyes DJ, Hay S, Rigby SEJ, &, Scrutton NS, (2014) Energy landscapes and catalysis in nitric oxide synthase. J Biol Chem 289, 11725-11738.
8. Campbell MG, Smith BC, Potter CS, Carragher B, &, Marletta MA, (2014) Molecular architecture of mammalian nitric oxide synthases. Proc Natl Acad Sci USA 111, E3614-E3623.
9. Yokom AL, Morishima Y, Lau M, Su M, Glukhova A, Osawa Y, &, Southworth DR, (2014) Architecture of the nitric-oxide synthase holoenzyme reveals large conformational changes and a calmodulin-driven release of the FMN domain. J Biol Chem 289, 16855-16865.
10. Rigby SEJ, Lou X, Toogood HS, Wolthers KR, &, Scrutton NS, (2011) ELDOR spectroscopy reveals that energy landscapes in human methionine synthase reductase are extensively remodelled following ligand and partner protein binding. ChemBioChem 12, 863-867.
11. Munro AW, Leys DG, McLean KJ, Marshall KR, Ost TWB, Daff S, Miles CS, Chapman SK, Lysek DA, Moser CC, et al,. (2002) P450 BM3: the very model of a modern flavocytochrome. Trends Biochem Sci 27, 250-257.
12. Gruez A, Pignol D, Zeghouf M, Coves J, Fontecave M, Ferrer JL, &, Fontecilla-Camps JC, (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. Pudney CR, Heyes DJ, Khara B, Hay S, Rigby SEJ, &, Scrutton NS, (2012) Kinetic and spectroscopic probes of motions and catalysis in the cytochrome P450 reductase family of enzymes. FEBS J 279, 1534-1544.
14. Pudney CR, Khara B, Johannissen LO, &, Scrutton NS, (2011) Coupled motions direct electrons along human microsomal P450 chains. PLoS Biol 9, e1001222.
15. Iyanagi T, &, Mason HS, (1973) Some properties of hepatic reduced nicotinamide adenine dinucleotide phosphate-cytochrome c reductase. Biochemistry 12, 2297-2308.
16. Schacter BA, Nelson EB, Masters BSS, &, Marver HS, (1972) Immunochemical evidence for an association of heme oxygenase with the microsomal electron transport system. J Biol Chem 247, 3601-3607.
17. Ilan Z, Ilan R, &, Cinti DL, (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.
18. Williams CH, &, Kamin H, (1962) Microsomal triphosphopyridine nucleotide-cytochrome c reductase of liver. J Biol Chem 237, 587-595.
19. Wang M, Roberts DL, Paschke R, Shea TM, Masters BSS, &, Kim JJP, (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94, 8411-8416.
20. Vincent B, Morellet N, Fatemi F, Aigrain L, Truan G, Guittet E, &, Lescop E, (2012) The closed and compact domain organization of the 70-kDa human cytochrome P450 reductase in its oxidized state as revealed by NMR. J Mol Biol 420, 296-309.
21. Xia C, Panda SP, Marohnic CC, Martasek P, Masters BS, &, Kim J-JP, (2011) Structural basis for human NADPH-cytochrome P450 oxidoreductase deficiency. Proc Natl Acad Sci USA 108, 13486-13491.
22. Gutierrez A, Lian LY, Wolf CR, Scrutton NS, &, Roberts GCK, (2001) Stopped-flow kinetic studies of flavin reduction in human cytochrome P450 reductase and its component domains. Biochemistry 40, 1964-1975.
23. Haque MM, Bayachou M, Tejero J, Kenney CT, Pearl NM, Im S-C, Waskell L, &, Stuehr DJ, (2014) Distinct conformational behaviors of four mammalian dual-flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, endothelial nitric oxide synthase) determine their unique catalytic profiles. FEBS J 281, 5325-5340.
24. Brenner S, Hay S, Munro AW, &, Scrutton NS, (2008) Inter-flavin electron transfer in cytochrome P450 reductase-effects of solvent and pH identify hidden complexity in mechanism. FEBS J 275, 4540-4557.
25. Marcus RA, &, Sutin N, (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811, 265-322.
26. Moser CC, Keske JM, Warncke K, Farid RS, &, Dutton PL, (1992) Nature of biological electron transfer. Nature 355, 796-802.
27. Page CC, Moser CC, Chen XX, &, Dutton PL, (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47-52.
28. Gutierrez A, Paine M, Wolf CR, Scrutton NS, &, Roberts GCK, (2002) Relaxation kinetics of cytochrome P450 reductase: internal electron transfer is limited by conformational change and regulated by coenzyme binding. Biochemistry 41, 4626-4637.
29. Bhattacharyya AK, Lipka JJ, Waskell L, &, Tollin G, (1991) Laser flash photolysis studies of the reduction kinetics of NADPH:cytochrome P-450 reductase. Biochemistry 30, 759-765.
30. Heyes DJ, Quinn A-M, Cullis PM, Lee M, Munro AW, &, Scrutton NS, (2009) Internal electron transfer in multi-site redox enzymes is accessed by laser excitation of thiouredopyrene-3,6,8-trisulfonate (TUPS). Chem Commun 2009, 1124-1126.
31. Jenner M, Ellis J, Huang W-C, Raven EL, Roberts GCK, &, Oldham NJ, (2011) Detection of a protein conformational equilibrium by electrospray ionisation-ion mobility-mass spectrometry. Angew Chem 50, 8291-8294.
32. Ellis J, Gutierrez A, Barsukov IL, Huang W-C, Grossmann JG, &, Roberts GCK, (2009) Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small-angle X-ray scattering. J Biol Chem 284, 36628-36637.
33. Huang W-C, Ellis J, Moody PCE, Raven EL, &, Roberts GCK, (2013) Redox-linked domain movements in the catalytic cycle of cytochrome p450 reductase. Structure 21, 1581-1589.
34. Smith CI, Convery JH, Harrison P, Khara B, Scrutton NS, &, Weightman P, (2014) Conformational change in cytochrome P450 reductase adsorbed at a Au(110)-phosphate buffer interface induced by interaction with nicotinamide adenine dinucleotide phosphate. Phys Rev E Stat Nonlin Soft Matter Phys 90, 022708.
35. Aigrain L, Pompon D, Morera S, &, Truan G, (2009) Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase. EMBO Rep 10, 742-747.
36. Hay S, Brenner S, Khara B, Quinn AM, Rigby SEJ, &, Scrutton NS, (2010) Nature of the energy landscape for gated electron transfer in a dynamic redox protein. J Am Chem Soc 132, 9738-9745.
37. Hamdane D, Xia C, Im S-C, Zhang H, Kim J-JP, &, 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.
38. Xia C, Hamdane D, Shen AL, Choi V, Kasper CB, Pearl NM, Zhang H, Im S-C, Waskell L, &, Kim J-JP, (2011) Conformational changes of NADPH-cytochrome P450 oxidoreductase are essential for catalysis and cofactor binding. J Biol Chem 286, 16246-16260.
39. Huang R, Zhang M, Rwere F, Waskell L, &, Ramamoorthy A, (2015) Kinetic and structural characterization of the interaction between the FMN binding domain of cytochrome P450 reductase and cytochrome c. J Biol Chem 290, 4843-4855.
40. Smith GCM, Tew DG, &, Wolf CR, (1994) Dissection of NADPH-cytochrome P450 oxidoreductase into distinct functional domains. Proc Natl Acad Sci USA 91, 8710-8714.
41. Munro AW, Noble MA, Robledo L, Daff SN, &, Chapman SK, (2001) Determination of the redox properties of human NADPH-cytochrome P450 reductase. Biochemistry 40, 1956-1963.
42. Iyanagi T, Xia C, &, Kim J-JP, (2012) NADPH-cytochrome P450 oxidoreductase: prototypic member of the diflavin reductase family. Arch Biochem Biophys 528, 72-89.
43. Laursen T, Jensen K, &, Moller BL, (2011) Conformational changes of the NADPH-dependent cytochrome P450 reductase in the course of electron transfer to cytochromes P450. Biochim Biophys Acta 1814, 132-138.