Structure of the Arabidopsis thaliana NADPH-cytochrome P450 reductase 2 (ATR2) provides insight into its function

FEBS Journal

Volumn 284, Issue 5, 2017, Pages 754-765

  Niu, Guoqi ^a   Zhao, Shun ^b,c   Wang, Lei ^a   Dong, Wei ^b,c   Liu, Lin ^b   He, Yikun ^a  

^a CAPITAL NORMAL UNIVERSITY   (China)

^b INSTITUTE OF BOTANY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

conformational change; crystallography; electron transfer; flavoprotein; reduction oxidation

Indexed keywords

CYTOCHROME P450 REDUCTASE; FLAVINE MONONUCLEOTIDE; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; ARABIDOPSIS PROTEIN; ATR2 PROTEIN, ARABIDOPSIS; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; RIBOFLAVIN DERIVATIVE;

ARABIDOPSIS THALIANA; ARTICLE; ELECTRON TRANSPORT; ENZYME ACTIVITY; NONHUMAN; PLANT STRUCTURES; PROTEIN FUNCTION; ARABIDOPSIS; CATALYSIS; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MUTATION; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CATALYSIS; CRYSTALLOGRAPHY, X-RAY; FLAVINS; KINETICS; MUTATION; OXIDATION-REDUCTION; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85012037092     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.14017     Document Type: Article

References (46)

1. Iyanagi T, Xia C & Kim JJ (2012) NADPH-cytochrome P450 oxidoreductase: prototypic member of the diflavin reductase family. Arch Biochem Biophys 528, 72–89.
2. 5 by NADPH-cytochrome P450 reductase. Arch Biochem Biophys 440, 204–211.
3. Porter TD & Kasper CB (1985) Coding nucleotide sequence of rat NADPH-cytochrome P-450 oxidoreductase cDNA and identification of flavin-binding domains. Proc Natl Acad Sci USA 82, 973–977.
4. Porter TD & Kasper CB (1986) NADPH-cytochrome P-450 oxidoreductase: flavin mononucleotide and flavin adenine dinucleotide domains evolved from different flavoproteins. Biochemistry 25, 1682–1687.
5. 2+/calmodulin-independent diaphorase and reductase activities. Biochemistry 31, 3243–3249.
6. Sevrioukova IF, Li H, Zhang H, Peterson JA & Poulos TL (1999) Structure of a cytochrome P450-redox partner electron-transfer complex. Proc Natl Acad Sci USA 96, 1863–1868.
7. Eschenbrenner M, Covès J & Fontecave M (1995) NADPH-sulfite reductase flavoprotein from Escherichia coli: contribution to the flavin content and subunit interaction. FEBS Lett 374, 82–84.
8. Olteanu H & Banerjee R (2001) Human methionine synthase reductase, a soluble P-450 reductase-like dual flavoprotein, is sufficient for NADPH-dependent methionine synthase activation. J Biol Chem 276, 35558–35563.
9. Paine MJ, Garner AP, Powell D, Sibbald J, Sales M, Pratt N, Smith T, Tew DG & Wolf CR (2000) Cloning and characterization of a novel human dual flavin reductase. J Biol Chem 275, 1471–1478.
10. Wang M, Roberts DL, Paschke R, Shea TM, Masters BS & Kim JJ (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc Natl Acad Sci USA 94, 8411–8416.
11. Smith GC, Tew DG & Wolf CR (1994) Dissection of NADPH-cytochrome P450 oxidoreductase into distinct functional domains. Proc Natl Acad Sci USA 91, 8710–8714.
12. 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.
13. Lamb DC, Kim Y, Yermalitskaya LV, Yermalitsky VN, Lepesheva GI, Kelly SL, Waterman MR & Podust LM (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.
14. Xia C, Panda SP, Marohnic CC, Martásek P, Masters BS & Kim JJ (2011) Structural basis for human NADPH-cytochrome P450 oxidoreductase deficiency. Proc Natl Acad Sci USA 108, 13486–13491.
15. Laursen T, Jensen K & Møller 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.
16. Aigrain L, Fatemi F, Frances O, Lescop E & Truan G (2012) Dynamic control of electron transfers in diflavin reductases. Int J Mol Sci 13, 15012–15041.
17. Hamdane D, Xia C, Im SC, Zhang H, Kim JJ & 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.
18. Sugishima M, Sato H, Higashimoto Y, Harada J, Wada K, Fukuyama K & Noguchi M (2014) Structural basis for the electron transfer from an open form of NADPH-cytochrome P450 oxidoreductase to heme oxygenase. Proc Natl Acad Sci USA 111, 2524–2529.
19. Aigrain L, Pompon D, Moréra S & Truan G (2009) Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase. EMBO Rep 10, 742–747.
20. Xia C, Hamdane D, Shen AL, Choi V, Kasper CB, Pearl NM, Zhang H, Im SC, Waskell L & Kim JJ (2011) Conformational changes of NADPH-cytochrome P450 oxidoreductase are essential for catalysis and cofactor binding. J Biol Chem 286, 16246–16260.
21. Pudney CR, Heyes DJ, Khara B, Hay S, Rigby SE & Scrutton NS (2012) Kinetic and spectroscopic probes of motions and catalysis in the cytochrome P450 reductase family of enzymes. FEBS J 279, 1534–1544.
22. Jensen K & Møller BL (2010) Plant NADPH-cytochrome P450 oxidoreductases. Phytochemistry 71, 132–141.
23. Mizutani M & Ohta D (2010) Diversification of P450 genes during land plant evolution. Annu Rev Plant Biol 61, 291–315.
24. Bak S, Beisson F, Bishop G, Hamberger B, Höfer R, Paquette S & Werck-Reichhart D (2011) Cytochromes p450. Arabidopsis Book 9, e0144.
25. Urban P, Mignotte C, Kazmaier M, Delorme F & Pompon D (1997) Cloning, yeast expression, and characterization of the coupling of two distantly related Arabidopsis thaliana NADPH-cytochrome P450 reductases with P450 CYP73A5. J Biol Chem 272, 19176–19186.
26. Mizutani M & Ohta D (1998) Two isoforms of NADPH:cytochrome P450 reductase in Arabidopsis thaliana. Gene structure, heterologous expression in insect cells, and differential regulation. Plant Physiol 116, 357–367.
27. Sundin L, Vanholme R, Geerinck J, Goeminne G, Höfer R, Kim H, Ralph J & Boerjan W (2014) Mutation of the inducible Arabidopsis thaliana cytochrome P450 reductase2 alters lignin composition and improves saccharification. Plant Physiol 166, 1956–1971.
28. Varadarajan J, Guilleminot J, Saint-Jore-Dupas C, Piégu B, Chabouté ME, Gomord V, Coolbaugh RC, Devic M & Delorme V (2010) ATR3 encodes a diflavin reductase essential for Arabidopsis embryo development. New Phytol 187, 67–82.
29. Whitelaw DA, Tonkin R, Meints CE & Wolthers KR (2015) Kinetic analysis of electron flux in cytochrome P450 reductases reveals differences in rate-determining steps in plant and mammalian enzymes. Arch Biochem Biophys 584, 107–115.
30. Joyce MG, Ekanem IS, Roitel O, Dunford AJ, Neeli R, Girvan HM, Baker GJ, Curtis RA, Munro AW & Leys D (2012) The crystal structure of the FAD/NADPH-binding domain of flavocytochrome P450 BM3. FEBS J 279, 1694–1706.
31. Hsieh YC, Chia TS, Fun HK & Chen CJ (2013) Crystal structure of dimeric flavodoxin from Desulfovibrio gigas suggests a potential binding region for the electron-transferring partner. Int J Mol Sci 14, 1667–1683.
32. Rwere F, Xia C, Im S, Haque MM, Stuehr DJ, Waskell L & Kim JJ (2016) Mutants of cytochrome P450 reductase lacking either Gly-141 or Gly-143 destabilize its FMN semiquinone. J Biol Chem 291, 14639–14661.
33. Hubbard PA, Shen AL, Paschke R, Kasper CB & Kim JJ (2001) NADPH-cytochrome P450 oxidoreductase. Structural basis for hydride and electron transfer. J Biol Chem 276, 29163–29170.
34. +/H. Biochemistry 44, 13477–13490.
35. Page CC, Moser CC, Chen X & Dutton PL (1999) Natural engineering principles of electron tunnelling in biological oxidation-reduction. Nature 402, 47–52.
36. Krissinel E & Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372, 774–797.
37. Ellis J, Gutierrez A, Barsukov IL, Huang WC, Grossmann JG & Roberts GC (2009) Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small-angle x-ray scattering. J Biol Chem 284, 36628–36637.
38. Frances O, Fatemi F, Pompon D, Guittet E, Sizun C, Pérez J, Lescop E & Truan G (2015) A well-balanced preexisting equilibrium governs electron flux efficiency of a multidomain diflavin reductase. Biophys J 108, 1527–1536.
39. 6-tag and maltose-binding-protein double-affinity fusion system. Protein Expr Purif 10, 309–319.
40. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC & Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658–674.
41. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67, 235–242.
42. Terwilliger TC, Grosse-Kunstleve RW, Afonine PV, Moriarty NW, Zwart PH, Hung LW, Read RJ & Adams PD (2008) Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr D Biol Crystallogr 64, 61–69.
43. Emsley P, Lohkamp B, Scott WG & Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66, 486–501.
44. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213–221.
45. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, Mustyakimov M, Terwilliger TC, Urzhumtsev A, Zwart PH & Adams PD (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68, 352–367.
46. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS & Richardson DC (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12–21.