Monitoring shifts in the conformation equilibrium of the membrane protein cytochrome P450 reductase (POR) in nanodiscs

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34596-34603

  Wadsäter, Maria ^a   Laursen, Tomas ^a   Singha, Aparajita ^a   Hatzakis, Nikos S ^a   Stamou, Dimitrios ^a   Barker, Robert ^b   Mortensen, Kell ^c   Feidenhans'l, Robert ^c   Møller, Birger Lindberg ^a   Cárdenas, Marité ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b INSTITUT LAUE LANGEVIN   (France)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHIPATHIC; COFACTORS; CONFORMATIONAL EQUILIBRIUM; CONTROLLED ORIENTATION; CYTOCHROME P450 REDUCTASE; DENSE FILMS; ELECTRON-TRANSFER REACTIONS; EXTENDED FORM; KEY ENZYMES; LABEL FREE; MECHANISM OF ACTION; MEMBRANE PROTEINS; NANODISCS; NEUTRON REFLECTOMETRY; NON DESTRUCTIVE; PROOF OF CONCEPT; SECONDARY METABOLITES; SELF-ASSEMBLED; SUPPORTED LIPID BILAYERS;

BIOCHEMISTRY; CONFORMATIONS; ENZYMES; LIPID BILAYERS; NEUTRON REFLECTION;

PROTEINS;

CYTOCHROME P450 REDUCTASE; FLAVINE MONONUCLEOTIDE; MEMBRANE PROTEIN; NANODISC; NANOFILM; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; CATALYSIS; CELL VACUOLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME SYNTHESIS; LIPID BILAYER; MOLECULAR MECHANICS; NEUTRON REFLECTOMETRY; NONHUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN ISOLATION; REFLECTOMETRY;

FLAVIN MONONUCLEOTIDE; MEMBRANES, ARTIFICIAL; NADP; NADPH-FERRIHEMOPROTEIN REDUCTASE; NANOSTRUCTURES; NEUTRON DIFFRACTION; OXIDATION-REDUCTION; PLANT PROTEINS; PROTEIN CONFORMATION; SORGHUM;

EID: 84867261080     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.400085     Document Type: Article

References (50)

1. Bayburt, T. H., Grinkova, Y. V., and Sligar, S. G. (2002) Self-assembly of discoidal phospholipid bilayer nanoparticles with membrane scaffold proteins. Nano Lett. 2, 853-856 (Pubitemid 135706448)
2. Denisov, I. G., Grinkova, Y. V., Lazarides, A. A., and Sligar, S. G. (2004) Directed self-assembly of monodisperse phospholipid bilayer nanodiscs with controlled size. J. Am. Chem. Soc. 126, 3477-3487 (Pubitemid 38366738)
3. Nath, A., Atkins, W. M., and Sligar, S. G. (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane protein. Biochemistry 46, 2059-2069 (Pubitemid 46355317)
4. Ritchie, T. K., Grinkova, Y. V., Bayburt, T. H., Denisov, I. G., Zolnerciks, J. K., Atkins, W. M., and Sligar, S. G. (2009) Chapter 11 - Reconstitution of membrane proteins in phospholipid bilayer nanodiscs. Methods Enzymol. 464, 211-231
5. Borch, J., and Hamann, T. (2009) The nanodisc: A novel tool for membrane protein studies. Biol. Chem. 390, 805-814
6. Skar-Gislinge, N., Simonsen, J. B., Mortensen, K., Feidenhans'l, R., Sligar, S. G., Lindberg Møller, B., Bjørnholm, T., and Arleth, L. (2010) Elliptical structure of phospholipid bilayer nanodiscs encapsulated by scaffold proteins: Casting the roles of the lipids and the protein. J. Am. Chem. Soc. 132, 13713-13722
7. Denisov, I. G., McLean, M. A., Shaw, A. W., Grinkova, Y. V., and Sligar, S. G. (2005) Thermotropic phase transition in soluble nanoscale lipid bilayers. J. Phys. Chem. B 109, 15580-15588 (Pubitemid 41260809)
8. Nakano, M., Fukuda, M., Kudo, T., Miyazaki, M., Wada, Y., Matsuzaki, N., Endo, H., and Handa, T. (2009) Static and dynamic properties of phospholipid bilayer nanodiscs. J. Am. Chem. Soc. 131, 8308-8312
9. Bayburt, T. H., Leitz, A. J., Xie, G., Oprian, D. D., and Sligar, S. G. (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 282, 14875-14881 (Pubitemid 47093370)
10. Baas, B. J., Denisov, I. G., and Sligar, S. G. (2004) Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 430, 218-228 (Pubitemid 39208969)
11. Wadsäter, M., Simonsen, J. B., Lauridsen, T., Tveten, E. G., Naur, P., Bjørnholm, T., Wacklin, H., Mortensen, K., Arleth, L., Feidenhans'l, R., and Cárdenas, M. (2011) Aligning nanodiscs at the air-water interface, a neutron reflectivity study. Langmuir 27, 15065-15073
12. Jones, P. R., Moller, B. L., and Hoj, P. B. (1999) The UDP-glucose:p-hydroxymandelonitrile- O-glucosyltransferase that catalyzes the last step in synthesis of the cyanogenic glucoside dhurrin in Sorghum bicolor - Isolation, cloning, heterologous expression, and substrate specificity. J. Biol. Chem. 274, 35483-35491 (Pubitemid 129512841)
13. Phillips, A. H., and Langdon, R. G. (1962) Hepatic triphosphopyridine nucleotide-cytochrome c reductase: Isolation, characterization, and kinetic studies. J. Biol. Chem. 237, 2652-2660
14. Williams, C. H., Jr., and Kamin, H. (1962) Microsomal triphosphopyridine nucleotide-cytochrome c reductase of liver. J. Biol. Chem. 237, 587-595
15. Jensen, K., and Møller, B. L. (2010) Plant NADPH-cytochrome P450 oxidoreductases. Phytochemistry 71, 132-141
16. Iyanagi, T., Makino, N., and Mason, H. S. (1974) Redox properties of the reduced nicotinamide adenine dinucleotide phosphate-cytochrome P-450 and reduced nicotinamide adenine dinucleotide-cytochrome b5 reductases. Biochemistry 13, 1701-1710
17. Murataliev, M. B., Feyereisen, R., and Walker, A. (2004) Electron transfer by diflavin reductases. Bba-Proteins Proteom. 1698, 1-26 (Pubitemid 38446896)
18. 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 (Pubitemid 27335052)
19. Laursen, T., Jensen, K., and Møller, B. L. (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
20. 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 (Pubitemid 34275664)
21. 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
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. Bayburt, T. H., Carlson, J. W., and Sligar, S. G. (2000) Single molecule height measurements on a membrane protein in nanometer-scale phospholipid bilayer disks. Langmuir 16, 5993-5997
24. 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
25. 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 FMNbinding site in yeast NADPH-cytochrome P450 reductase suggests a mechanism of electron transfer by diflavin reductases. Structure 14, 51-61 (Pubitemid 43350073)
26. Ivanov, A. S., Gnedenko, O. V., Molnar, A. A., Archakov, A. I., and Podust, L. M. (2010) FMN binding site of yeast NADPH-cytochrome P450 reductase exposed at the surface is highly specific. ACS Chem. Biol. 5, 767-776
27. Møller, B. L., and Conn, E. E. (1980) The biosynthesis of cyanogenic glucosides in higher plants. Channeling of intermediates in dhurrin biosynthesis by a microsomal system from Sorghum bicolor (Linn.) Moench. J. Biol. Chem. 255, 3049-3056
28. Jensen, K., Osmani, S. A., Hamann, T., Naur, P., and Møller, B. L. (2011) Homology modeling of the three membrane proteins of the dhurrin metabolon: Catalytic sites, membrane surface association, and proteinprotein interactions. Phytochemistry 72, 2113-2123
29. Nielsen, K. A., Tattersall, D. B., Jones, P. R., and Møller, B. L. (2008) Metabolon formation in dhurrin biosynthesis. Phytochemistry 69, 88-98 (Pubitemid 350256789)
30. Kent, M. S., Murton, J. K., Sasaki, D. Y., Satija, S., Akgun, B., Nanda, H., Curtis, J. E., Majewski, J., Morgan, C. R., and Engen, J. R. (2010) Neutron reflectometry study of the conformation of HIV Nef bound to lipid membranes. Biophys. J. 99, 1940-1948
31. Kent, M. S., Yim, H., Murton, J. K., Satija, S., Majewski, J., and Kuzmenko, I. (2008) Oligomerization of membrane-bound diphtheria toxin (CRM197) facilitates a transition to the open form and deep insertion. Biophys. J. 94, 2115-2127
32. Clifton, L. A., Johnson, C. L., Solovyova, A. S., Callow, P., Weiss, K. L., Ridley, H., Le Brun, A. P., Kinane, C. J., Webster, J. R., Holt, S. A., and Lakey, J. H. (2012) Low resolution structure and dynamics of a colicin-receptor complex determined by neutron scattering. J. Biol. Chem. 287, 337-346
33. Chenal, A., Prongidi-Fix, L., Perier, A., Aisenbrey, C., Vernier, G., Lambotte, S., Haertlein, M., Dauvergne, M. T., Fragneto, G., Bechinger, B., Gillet, D., Forge, V., and Ferrand, M. (2009) Deciphering membrane insertion of the diphtheria toxin T domain by specular neutron reflectometry and solid-state NMR spectroscopy. J. Mol. Biol. 391, 872-883
34. Nanda, H., Datta, S. A., Heinrich, F., Lösche, M., Rein, A., Krueger, S., and Curtis, J. E. (2010) Electrostatic interactions and binding orientation of HIV-1 matrix studied by neutron reflectivity. Biophys. J. 99, 2516-2524
35. McGillivray, D. J., Valincius, G., Heinrich, F., Robertson, J. W., Vanderah, D. J., Febo-Ayala, W., Ignatjev, I., Lösche, M., and Kasianowicz, J. J. (2009) Structure of functional Staphylococcus aureus α-hemolysin channels in tethered bilayer lipid membranes. Biophys. J. 96, 1547-1553
36. Aliverti, A., Curti, B., and Vanoni, M. A. (1999) Identifying and quantitating FAD and FMN in simple and in iron-sulfur-containing flavoproteins. Methods Mol. Biol. 131, 9-23
37. Campbell, R. A., Wacklin, H. P., Sutton, I., Cubitt, R., and Fragneto, G. (2011) FIGARO: The new horizontal neutron reflectometer at the ILL. Eur. Phys. J. Plus 126
38. Thomas, R. K. (2004) Neutron reflection from liquid interfaces. Annu. Rev. Phys. Chem. 55, 391-426
39. Jacrot, B. (1976) The study of biological structures by neutron scattering from solution. Rep. Prog. Phys. 39, 911-953
40. Nelson, A. (2006) Co-refinement of multiple-contrast neutron/x-ray reflectivity data using MOTOFIT. J. Appl. Crystallogr. 39, 273-276
41. Abeles, F. (1948) Sur la propagation des ondes electromagnetiques dans les milieux stratifies. Ann. Phys. 3, 504-520
42. Carlson, J. W., Jonas, A., and Sligar, S. G. (1997) Imaging and manipulation of high-density lipoproteins. Biophys. J. 73, 1184-1189 (Pubitemid 27360707)
43. Åkesson, A., Lind, T., Ehrlich, N., Stamou, D., Wacklin, H., and Cardenas, M. (2012) Composition and structure of mixed phospholipid supported bilayers formed by POPC and DPPC. Soft Matter 8 5658-5665
44. Changeux, J. P., and Edelstein, S. J. (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428
45. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat. Chem. Biol. 5, 789-796
46. Hatzakis, N. S., Wei, L., Jorgensen, S. K., Kunding, A. H., Bolinger, P. Y., Ehrlich, N., Makarov, I., Skjot, M., Svendsen, A., Hedegard, P., and Stamou, D. (2012) Single enzyme studies reveal the existence of discrete functional states for monomeric enzymes and how they are "selected" upon allosteric regulation. JACS 134, 9296-9302
47. Groves, J. T., and Kuriyan, J. (2010) Molecular mechanisms in signal transduction at the membrane. Nat. Struct. Mol. Biol. 17, 659-665
48. Das, A., and Sligar, S. G. (2009) Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer. Biochemistry 48, 12104-12112
49. Koch, B. M., Sibbesen, O., Halkier, B. A., Svendsen, I., and Møller, B. L. (1995) The primary sequence of cytochroma P450TYR, the multifunctional N-hydroxylase catalyzing the conversion of L-tyrosine to P-hydroxyphenylaldehyde oxime in the biosynthesis of the cyanogenic glucoside dhurrinin Sorghum bicolor (L) Moench. Arch. Biochem. Biophys. 323, 177-186
50. Bak, S., Kahn, R. A., and Nielsen, H. L. (1998) Cloning of three A-type cytochromes p450, CYP71E1, CYP98, and CYP99 from Sorghum bicolor (L.) Moench by a PCR approach and identification by expression in Escherichia coli of CYP71E1 as a multifunctional cytochrome p450 in the biosynthesis of the cyanogenic glucoside dhurrin. Plant Mol. Biol. 36, 393-405 (Pubitemid 28077013)