Cytochromes P450 in nanodiscs

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1814, Issue 1, 2011, Pages 223-229

  Denisov, Ilia G ^a   Sligar, Stephen G ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Cytochrome P450; Membrane protein; Monooxygenase; Nanodisc; Reaction intermediates

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 3A4; MEMBRANE PROTEIN; NANODISC;

BILAYER MEMBRANE; FLOW KINETICS; PRIORITY JOURNAL; REVIEW; SPECTROSCOPY; STEADY STATE; STEROIDOGENESIS; XENOBIOTIC METABOLISM;

BIOCATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME STABILITY; HUMANS; LIPID BILAYERS; MEMBRANE PROTEINS; NANOSTRUCTURES; SOLUBILITY; SPECTROPHOTOMETRY; SUBSTRATE SPECIFICITY;

EID: 78649450188     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.05.017     Document Type: Review

References (71)

1. K. Ruckpaul Early years of cytochrome P450 research in Berlin-Buch: its present state and origin of the biochemical and biophysical conferences Biochem. Biophys. Res. Commun. 312 2003 65 74
2. K. Ruckpaul, and R. Renneberg Ron Estabrook-a catalyst of scientific interactions between East and West Drug Metab. Rev. 39 2007 267 270
3. K. Ruckpaul, H. Rein, Cytochrome P450 1984 Akademie Verlag Berlin 405 pp.
4. H. Rein, O. Ristau, J. Friedrich, G.R. Janig, and K. Ruckpaul Evidence for the existence of a high spin-low spin equilibrium in liver microsomal cytochrome P-450 FEBS Lett. 75 1977 19 22
5. O. Ristau, H. Rein, G.R. Janig, and K. Ruckpaul Quantitative analysis of the spin equilibrium of cytochrome P-450 LM-2 fraction from rabbit liver microsomes Biochim. Biophys. Acta 536 1978 226 234
6. M. Ziegler, J. Blanck, S. Greschner, K. Lenz, A. Lau, and K. Ruckpaul Kinetics of elementary steps in the cytochrome P-450 reaction sequence. V. Laser temperature-jump investigation of the spin relaxation kinetics of cytochrome P-450 LM2 Biomed. Biochim. Acta 42 1983 641 649
7. R. Bernhardt, K. Pommerening, and K. Ruckpaul Modification of carboxyl groups on NADPH-cytochrome P-450 reductase involved in binding of cytochromes c and P-450 LM2 Biochem. Int. 14 1987 823 832
8. J. Blanck, G.R. Janig, D. Schwarz, and K. Ruckpaul Role of lipid in the electron transfer between NADPH-cytochrome P-450 reductase and cytochrome P-450 from mammalian liver cells Xenobiotica 19 1989 1231 1246
9. R.M. Davydov, S. Greshner, S.N. Magonov, K. Ruckpaul, and L.A. Blyumenfel'd Absorption spectra of cytochrome P-450 nonequilibrium states formed during the low-temperature reduction of protein Dokl. Akad. Nauk SSSR 241 1978 707 709
10. A. Sharonov Yu, V.F. Pismensky, S. Greschner, and K. Ruckpaul Low- and ultralow-temperature magnetic circular dichroism studies of reduced cytochromes P-450-LM2 and P-420-LM2 and of photo-products of their co-complexes. The spin-state and axial ligation of heme iron Biochem. Biophys. Res. Commun. 146 1987 165 172
11. R.M. Davydov, S. Greschner, and K. Ruckpaul Study of absorption and magnetic circular dichroism spectra of hemoproteins in conformationally nonequilibrium states. V. Cytochrome P 450 and its complexes with substrates Molek. Biol. 13 1979 1397 1406
12. D. Schwarz, J. Pirrwitz, H.W. Meyer, M.J. Coon, and K. Ruckpaul Membrane topology of microsomal cytochrome P-450: saturation transfer EPR and freeze-fracture electron microscopy studies Biochem. Biophys. Res. Commun. 171 1990 175 181
13. T.H. Bayburt, and S.G. Sligar Single-molecule height measurements on microsomal cytochrome P450 in nanometer-scale phospholipid bilayer disks Proc. Natl. Acad. Sci. U. S. A. 99 2002 6725 6730
14. N.R. Civjan, T.H. Bayburt, M.A. Schuler, and S.G. Sligar Direct solubilization of heterologously expressed membrane proteins by incorporation into nanoscale lipid bilayers Biotechniques 35 2003 556 563
15. B.J. Baas, I.G. Denisov, and S.G. Sligar Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment Arch. Biochem. Biophys. 430 2004 218 228
16. A. Chougnet, Y. Grinkova, D. Ricard, S. Sligar, and W.-D. Woggon Fluorescent probes for rapid screening of potential drug-drug interactions at the CYP3A4 level ChemMedChem 2 2007 717 724
17. D.R. Davydov, B.J. Baas, S.G. Sligar, and J.R. Halpert Allosteric mechanisms in cytochrome P450 3A4 studied by high-pressure spectroscopy: pivotal role of substrate-induced changes in the accessibility and degree of hydration of the heme pocket Biochemistry 46 2007 7852 7864
18. D.R. Davydov, H. Fernando, B.J. Baas, S.G. Sligar, and J.R. Halpert Kinetics of dithionite-dependent reduction of cytochrome P450 3A4: heterogeneity of the enzyme caused by its oligomerization Biochemistry 44 2005 13902 13913
19. D.R. Davydov, E.V. Sineva, S. Sistla, N.Y. Davydova, D.J. Frank, S.G. Sligar, and J.R. Halpert Electron transfer in the complex of membrane-bound human cytochrome P450 3A4 with the flavin domain of P450BM-3: the effect of oligomerization of the heme protein and intermittent modulation of the spin equilibrium Biochim. Biophys. Acta 1797 2010 378 390
20. I.G. Denisov, B.J. Baas, Y.V. Grinkova, and S.G. Sligar Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation J. Biol. Chem. 282 2007 7066 7076
21. I.G. Denisov, Y.V. Grinkova, B.J. Baas, and S.G. Sligar The ferrous-dioxygen intermediate in human cytochrome P450 3A4: substrate dependence of formation of decay kinetics J. Biol. Chem. 281 2006 23313 23318
22. I.G. Denisov, Y.V. Grinkova, M.A. McLean, and S.G. Sligar The one-electron autoxidation of human cytochrome P450 3A4 J. Biol. Chem. 282 2007 26865 26873
23. D.J. Frank, I.G. Denisov, and S.G. Sligar Mixing apples and oranges: analysis of heterotropic cooperativity in cytochrome P450 3A4 Arch. Biochem. Biophys. 488 2009 146 152
24. A. Nath, Y.V. Grinkova, S.G. Sligar, and W.M. Atkins Ligand binding to cytochrome P450 3A4 in phospholipid bilayer nanodiscs: the effect of model membranes J. Biol. Chem. 282 2007 28309 28320
25. A. Nath, P.K. Koo, E. Rhoades, and W.M. Atkins Allosteric effects on substrate dissociation from cytochrome P450 3A4 in Nanodiscs observed by ensemble and single-molecule fluorescence spectroscopy J. Am. Chem. Soc. 130 2008 15746 15747
26. H. Duan, N.R. Civjan, S.G. Sligar, and M.A. Schuler Co-incorporation of heterologously expressed Arabidopsis cytochrome P450 and P450 reductase into soluble nanoscale lipid bilayers Arch. Biochem. Biophys. 424 2004 141 153
27. S.L. Gantt, I.G. Denisov, Y.V. Grinkova, and S.G. Sligar The critical iron-oxygen intermediate in human aromatase Biochem. Biophys. Res. Commun. 387 2009 169 173
28. Y.V. Grinkova, I.G. Denisov, M.R. Waterman, M. Arase, N. Kagawa, and S.G. Sligar The ferrous-oxy complex of human aromatase Biochem. Biophys. Res. Commun. 372 2008 379 382
29. H. Duan, and M.A. Schuler Heterologous expression and strategies for encapsulation of membrane-localized plant P450s Phytochem. Rev. 5 2006 507 523
30. T. Boldog, M. Li, and G.L. Hazelbauer Using Nanodiscs to create water-soluble transmembrane chemoreceptors inserted in lipid bilayers Methods Enzymol. 423 2007 317 335
31. J. Borch, and T. Hamann The Nanodisc: a novel tool for membrane protein studies Biol. Chem. 390 2009 805 814
32. A. Nath, W.M. Atkins, and S.G. Sligar Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins Biochemistry 46 2007 2059 2069
33. T.K. Ritchie, Y.V. Grinkova, T.H. Bayburt, I.G. Denisov, J.K. Zolnerciks, W.M. Atkins, and S.G. Sligar Reconstitution of membrane proteins in phospholipid bilayer nanodiscs Methods Enzymol. 464 2009 211 231
34. T.H. Bayburt, and S.G. Sligar Membrane protein assembly into Nanodiscs FEBS Lett. 584 2010 1721 1727
35. T.H. Bayburt, J.W. Carlson, and S.G. Sligar Reconstitution and imaging of a membrane protein in a nanometer-size phospholipid bilayer J. Struct. Biol. 123 1998 37 44
36. T.H. Bayburt, J.W. Carlson, and S.G. Sligar Single molecule height measurements on a membrane protein in nanometer-scale phospholipid bilayer disks Langmuir 16 2000 5993 5997
37. A. Das, Y.V. Grinkova, and S.G. Sligar Redox potential control by drug binding to cytochrome P 450 3A4 J. Am. Chem. Soc. 129 2007 13778 13779
38. A. Das, J. Zhao, G.C. Schatz, S.G. Sligar, and R.P. Van Duyne Screening of Type I and II drug binding to human cytochrome P450-3A4 in Nanodiscs by localized surface plasmon resonance spectroscopy Anal. Chem. 81 2009 3754 3759
39. A. Das, and S.G. Sligar Modulation of the cytochrome P450 reductase redox potential by the phospholipid bilayer Biochemistry 48 2009 12104 12112
40. T.H. Bayburt, Y.V. Grinkova, and S.G. Sligar Assembly of single bacteriorhodopsin trimers in bilayer nanodiscs Arch. Biochem. Biophys. 450 2006 215 222
41. T.H. Bayburt, A.J. Leitz, G. Xie, D.D. Oprian, and S.G. Sligar Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins J. Biol. Chem. 282 2007 14875 14881
42. T.H. Bayburt, and S.G. Sligar Self-assembly of single integral membrane proteins into soluble nanoscale phospholipid bilayers Protein Sci. 12 2003 2476 2481
43. T. Boldog, S. Grimme, M. Li, S.G. Sligar, and G.L. Hazelbauer Nanodiscs separate chemoreceptor oligomeric states and reveal their signaling properties Proc. Natl. Acad. Sci. U. S. A. 103 2006 11509 11514
44. V.L. Marin, T.H. Bayburt, S.G. Sligar, and M. Mrksich Functional assays of membrane-bound proteins with SAMDI-TOF mass spectrometry Angew. Chem. Int. Ed. 46 2007 8796 8798
45. E.D. Goluch, A.W. Shaw, S.G. Sligar, and C. Liu Microfluidic patterning of nanodisc lipid bilayers and multiplexed analysis of protein interaction Lab Chip 8 2008 1723 1728
46. A.Z. Kijac, Y. Li, S.G. Sligar, and C.M. Rienstra Magic-angle spinning solid-state NMR spectroscopy of Nanodisc-embedded human CYP3A4 Biochemistry 46 2007 13696 13703
47. D.R. Davydov, and J.R. Halpert Allosteric P450 mechanisms: multiple binding sites, multiple conformers or both? Expert Opin. Drug Metab. Toxicol. 4 2008 1523 1535
48. I.G. Denisov, D.J. Frank, and S.G. Sligar Cooperative properties of cytochromes P450 Pharmacol. Ther. 124 2009 151 167
49. S.G. Sligar, and I.G. Denisov Understanding cooperativity in human P450 mediated drug-drug interactions Drug Metab. Rev. 39 2007 567 579
50. B.J. Baas, Characterization of monomeric human cytochrome P450 3A4 and cytochrome P450 reductase in nanoscale phospholipid bilayer discs, Ph.D. Thes., 2006, University of Illinois: Urbana. 180 pp.
51. A. Nath, Thermodynamics and kinetics of ligand binding to cytochrome P450 3A4 in membrane nanodiscs, Ph.D. Thes., 2008, University of Washington: Seattle. 120 pp.
52. N.A. Hosea, G.P. Miller, and F.P. Guengerich Elucidation of distinct ligand binding sites for cytochrome P450 3A4 Biochemistry 39 2000 5929 5939
53. E.M. Isin, and F.P. Guengerich Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4 J. Biol. Chem. 281 2006 9127 9136
54. I.G. Denisov, T.M. Makris, S.G. Sligar, and I. Schlichting Structure and chemistry of cytochrome P 450 Chem. Rev. 105 2005 2253 2277
55. R. Davydov, R. Kappl, J. Huettermann, and J.A. Peterson EPR-spectroscopy of reduced oxyferrous-P450cam FEBS Lett. 295 1991 113 115
56. R. Davydov, T.M. Makris, V. Kofman, D.E. Werst, S.G. Sligar, and B.M. Hoffman Hydroxylation of camphor by reduced oxy-cytochrome P450cam: mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes J. Am. Chem. Soc. 123 2001 1403 1415
57. R. Davydov, R. Razeghifard, S.C. Im, L. Waskell, and B.M. Hoffman Characterization of the microsomal cytochrome P450 2B4 O2 activation intermediates by cryoreduction and electron paramagnetic resonance Biochemistry 47 2008 9661 9666
58. I.G. Denisov, J.H. Dawson, L.P. Hager, and S.G. Sligar The ferric-hydroperoxo complex of chloroperoxidase Biochem. Biophys. Res. Commun. 363 2007 954 958
59. I.G. Denisov, T.M. Makris, and S.G. Sligar Cryoradiolysis for the study of P450 reaction intermediates Meth. Enzymol. 357 2002 103 115
60. I.G. Denisov, D.C. Victoria, and S.G. Sligar Cryoradiolytic reduction of heme proteins: maximizing dose dependent yield Radiat. Phys. Chem. 76 2007 714 721
61. M. Ibrahim, I.G. Denisov, T.M. Makris, J.R. Kincaid, and S.G. Sligar Resonance Raman spectroscopic studies of hydroperoxo-myoglobin at cryogenic temperatures J. Am. Chem. Soc. 125 2003 13714 13718
62. P.J. Mak, I.G. Denisov, D. Victoria, T.M. Makris, T. Deng, S.G. Sligar, and J.R. Kincaid Resonance Raman detection of the hydroperoxo intermediate in the cytochrome P450 enzymatic cycle J. Am. Chem. Soc. 129 2007 6382 6383
63. P.J. Mak, and J.R. Kincaid Resonance Raman spectroscopic studies of hydroperoxo derivatives of cobalt-substituted myoglobin J. Inorg. Biochem. 102 2008 1952 1957
64. J.D. Lipscomb, S.G. Sligar, M.J. Namtvedt, and I.C. Gunsalus Autooxidation and hydroxylation reactions of oxygenated cytochrome P-450cam J. Biol. Chem. 251 1976 1116 1124
65. R.C. Tuckey, and H. Kamin The oxyferro complex of adrenal cytochrome P-450scc. Effect of cholesterol and intermediates on its stability and optical characteristics J. Biol. Chem. 257 1982 9309 9314
66. I.G. Denisov, P.J. Mak, T.M. Makris, S.G. Sligar, and J.R. Kincaid Resonance Raman characterization of the peroxo and hydroperoxo intermediates in cytochrome P450 J. Phys. Chem. A 112 2008 13172 13179
67. T. Sjodin, J.F. Christian, I.D.G. Macdonald, R. Davydov, M. Unno, S.G. Sligar, B.M. Hoffman, and P.M. Champion Resonance Raman and EPR investigations of the D251N oxycytochrome P450cam/putidaredoxin complex Biochemistry 40 2001 6852 6859
68. H. Heller, M. Schaefer, and K. Schulten Molecular dynamics simulation of a bilayer of 200 lipids in the gel and in the liquid-crystal phases J. Phys. Chem. 97 1993 83434 88360
69. I.G. Denisov, Y.V. Grinkova, A.A. Lazarides, and S.G. Sligar Directed self-assembly of monodisperse phospholipid bilayer Nanodiscs with controlled size J. Am. Chem. Soc. 126 2004 3477 3487
70. J.K. Yano, M.R. Wester, G.A. Schoch, K.J. Griffin, C.D. Stout, and E.F. Johnson The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05-A resolution J. Biol. Chem. 279 2004 38091 38094
71. M. Wang, D.L. Roberts, R. Paschke, T.M. Shea, B.S. Masters, and J.J. Kim Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes Proc. Natl. Acad. Sci. U. S. A. 94 1997 8411 8416