Solution structure of the cytochrome P450 reductase–cytochrome c complex determined by neutron scattering

Journal of Biological Chemistry

Volumn 293, Issue 14, 2018, Pages 5210-5219

  Freeman, Samuel L ^a,b   Martel, Anne ^b   Devos, Juliette M ^b   Basran, Jaswir ^a   Raven, Emma L ^a   Roberts, Gordon C K ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGY; ELECTRON TRANSITIONS; PROTEINS;

CATALYTIC MECHANISMS; CYTOCHROME P450 REDUCTASE; DEUTERATED PROTEINS; ELECTRON TRANSFER; ELECTRON-TRANSFER STEP; PROTEIN COMPLEXES; SELECTIVE ELECTRON TRANSFER; SOLUTION STRUCTURES;

NEUTRON SCATTERING;

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

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STRUCTURE; HUMAN; NEUTRON SCATTERING; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIZE EXCLUSION CHROMATOGRAPHY; CHEMISTRY; KINETICS; METABOLISM; NEUTRON; NEUTRON DIFFRACTION; OXIDATION REDUCTION REACTION; PROCEDURES; PROTEIN TERTIARY STRUCTURE; SMALL ANGLE SCATTERING; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS; ULTRASTRUCTURE;

CYTOCHROMES C; ELECTRON TRANSPORT; FLAVIN MONONUCLEOTIDE; FLAVIN-ADENINE DINUCLEOTIDE; KINETICS; NADP; NADPH-FERRIHEMOPROTEIN REDUCTASE; NEUTRON DIFFRACTION; NEUTRONS; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY; SCATTERING, SMALL ANGLE; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 85045068583     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.RA118.001941     Document Type: Article

References (59)

1. Bashir, Q., Scanu, S., and Ubbink, M. (2011) Dynamics in electron transfer protein complexes. FEBS J. 278, 1391–1400 CrossRef Medline
2. Schilder, J., and Ubbink, M. (2013) Formation of transient protein complexes. Curr. Opin. Struct. Biol. 23, 911–918 CrossRef Medline
3. Ahuja, S., Jahr, N., Im, S. C., Vivekanandan, S., Popovych, N., Le Clair, S. V., Huang, R., Soong, R., Xu, J., Yamamoto, K., Nanga, R. P., Bridges, A., Waskell, L., and Ramamoorthy, A. (2013) A model of the membrane-bound cytochrome b5-cytochrome P450 complex from NMR and mutagenesis data. J. Biol. Chem. 288, 22080 –22095 CrossRef Medline
4. Worrall, J. A., Liu, Y., Crowley, P. B., Nocek, J. M., Hoffman, B. M., and Ubbink, M. (2002) Myoglobin and cytochrome b5: a nuclear magnetic resonance study of a highly dynamic protein complex. Biochemistry 41, 11721–11730 CrossRef Medline
5. Deep, S., Im, S. C., Zuiderweg, E. R., and Waskell, L. (2005) Characterization and calculation of a cytochrome c-cytochrome b5 complex using NMR data. Biochemistry 44, 10654 –10668 CrossRef Medline
6. Volkov, A. N., Worrall, J. A., Holtzmann, E., and Ubbink, M. (2006) Solution structure and dynamics of the complex between cytochrome c and cytochrome c peroxidase determined by paramagnetic NMR. Proc. Natl. Acad. Sci. U.S.A. 103, 18945–18950 CrossRef Medline
7. Volkov, A. N. (2015) Structure and function of transient encounters of redox proteins. Acc. Chem. Res. 48, 3036 –3043 CrossRef Medline
8. Hiruma, Y., Hass, M. A., Kikui, Y., Liu, W. M., Ölmez, B., Skinner, S. P., Blok, A., Kloosterman, A., Koteishi, H., Löhr, F., Schwalbe, H., Nojiri, M., and Ubbink, M. (2013) The structure of the cytochrome p450cam-puti-daredoxin complex determined by paramagnetic NMR spectroscopy and crystallography. J. Mol. Biol. 425, 4353– 4365 CrossRef Medline
9. Aigrain, L., Fatemi, F., Frances, O., Lescop, E., and Truan, G. (2012) Dynamic control of electron transfer in diflavin reductases. Int. J. Mol. Sci. 13, 15012–15041 CrossRef Medline
10. 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 CrossRef Medline
11. Waskell, L., and Kim, J.-J. P. (2015) Electron-transfer partners of cytochrome P450, in Cytochrome P450 (Ortiz de Montellano, P. R., ed) pp. 33– 68, Springer International Publishing, Basel, Switzerland
12. Xia, C., Panda, S. P., Marohnic, C. C., Martásek, P., Masters, B. S., and Kim, J. J. (2011) Structural basis for human NADPH-cytochrome P450 oxidoreductase deficiency. Proc. Natl. Acad. Sci. U.S.A. 108, 13486 –13491 CrossRef Medline
13. Riddick, D. S., Ding, X., Wolf, C. R., Porter, T. D., Pandey, A. V., Zhang, Q.-Y., Gu, J., Finn, R. D., Ronseaux, S., McLaughlin, L. A., Henderson, C. J., Zou, L., and Flück, C. E. (2013) NADPH-cytochrome P450 oxidoreductase: roles in physiology, pharmacology and toxicology. Drug Metab. Dis-pos. 41, 12–23 CrossRef Medline
14. Iyanagi, T., Xia, C., and Kim, J. J. (2012) NADPH-cytochrome P450 oxidoreductase: prototypic member of the diflavin reductase family. Arch. Biochem. Biophys. 528, 72– 89 CrossRef Medline
15. Farooq, Y., and Roberts, G. C. (2010) Kinetics of electron transfer between NADPH-cytochrome P450 reductase and cytochrome P450 3A4. Biochem. J. 432, 485– 493 CrossRef Medline
16. Makris, T. M., Denisov, I., Schlichting, I., and Sligar, S. G. (2005) Activation of molecular oxygen by cytochrome P450, in Cytochrome P450: Structure Mechanism and Biochemistry (Ortiz de Montellano, P. R., ed) 3rd Ed., pp. 149 –182, Kluwer Academic/Plenum, New York
17. Murataliev, M. B., Feyereisen, R., and Walker, F. A. (2004) Electron transfer by diflavin reductases. Biochim. Biophys. Acta 1698, 1–26 CrossRef Medline
18. Haque, M. M., Fadlalla, M. A., Aulak, K. S., Ghosh, A., Durra, D., and Stuehr, D. J. (2012) Control of electron transfer and catalysis in neuronal nitric-oxide synthase (nNOS) by a hinge connecting its FMN and FAD-NADPH domains. J. Biol. Chem. 287, 30105–30116 CrossRef Medline
19. 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 CrossRef Medline
20. Wolthers, K. R., Lou, X., Toogood, H. S., Leys, D., and Scrutton, N. S. (2007) Mechanism of coenzyme binding to human methionine synthase reductase revealed through the crystal structure of the FNR-like module and isothermal titration calorimetry. Biochemistry 46, 11833–11844 CrossRef Medline
21. 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 CrossRef Medline
22. Freeman, S. L., Martel, A., Raven, E. L., and Roberts, G. C. K. (2017) Orchestrated domain movement in catalysis by cytochrome P450 reductase. Sci. Rep. 7, 9741–9752 CrossRef Medline
23. 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 CrossRef Medline
24. Hamdane, D., Xia, C., Im, S.-C., Zhang, H., Kim, J.-J. P., 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 CrossRef Medline
25. 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 CrossRef Medline
26. Hedison, T. M., Hay, S., and Scrutton, N. S. (2015) Real-time analysis of conformational control in electron transfer reactions of human cytochrome P450 reductase with cytochrome c. FEBS J. 282, 4357– 4375 CrossRef Medline
27. Huang, W. C., Ellis, J., Moody, P. C., Raven, E. L., and Roberts, G. C. (2013) Redox-linked domain movements in the catalytic cycle of cytochrome p450 reductase. Structure 21, 1581–1589 CrossRef Medline
28. Jenner, M., Ellis, J., Huang, W.-C., Raven, E. L., Roberts, G. C., and Old-ham, N. J. (2011) Detection of a protein conformational equilibrium by electrospray ionisation-ion mobility-mass spectrometry. Angew. Chem. Int. Ed. Engl. 50, 8291– 8294 CrossRef Medline
29. Horecker, B. L. (1950) Triphosphopyridine nucleotide-cytochrome c reductase in liver. J. Biol. Chem. 183, 593– 605
30. 2) as a competitive inhibitor of NADPH-dependent reduction of cytochrome P450 LM2: locating protein-protein interaction sites in micro-somal electron carriers. Arch. Biochem. Biophys. 297, 304–313 CrossRef Medline
31. Tamburini, P. P., and Schenkman, J. B. (1986) Differences in the mechanism of functional interaction between NADPH-cytochrome P-450 reductase and its redox partners. Mol. Pharmacol. 30, 178 –185 Medline
32. Haque, M. M., Bayachou, M., Tejero, J., Kenney, C. T., Pearl, N. M., Im, S. C., Waskell, L., and Stuehr, D. J. (2014) Distinct conformational behaviors of four mammalian dual-flavin reductases (cytochrome P450 reductase, methionine synthase reductase, neuronal nitric oxide synthase, en-dothelial nitric oxide synthase) determine their unique catalytic profiles. FEBS J. 281, 5325–5340 CrossRef Medline
33. Schneidman-Duhovny, D., Hammel, M., Tainer, J. A., and Sali, A. (2016) FoXS, FoXSDock and MultiFoXS: single-state and multi-state structural modeling of proteins and their complexes based on SAXS profiles. Nucleic Acids Res. 44, W424 –W429 CrossRef Medline
34. Stuhrmann, H. B. (1974) Neutron small-angle scattering of biological macromolecules in solution. J. Appl. Crystallogr. 7, 173–178 CrossRef
35. Svergun, D. I., Koch, M. H. J., Timmins, P. A., and May, R. P. (2013) Small-angle X-ray and neutron scattering from solutions of biological macromolecules, Oxford University Press, Oxford
36. Dunne, O., Weidenhaupt, M., Callow, P., Martel, A., Moulin, M., Perkins, S. J., Haertlein, M., and Forsyth, V. T. (2017) Matchout deuterium label-ling of proteins for small-angle neutron scattering studies using prokary-otic and eukaryotic expression systems and high cell-density cultures. Eur. Biophys. J. 46, 425– 432 CrossRef Medline
37. Jacrot, B., Pfeiffer, P., and Witz, J. (1976) The structure of a spherical plant virus (bromegrass mosaic virus) established by neutron diffraction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 276, 109 –112 CrossRef Medline
38. Bushnell, G. W., Louie, G. V., and Brayer, G. D. (1990) High-resolution three-dimensional structure of horse heart cytochrome c. J. Mol. Biol. 214, 585–595 CrossRef Medline
39. Jang, H.-H., Jamakhandi, A. P., Sullivan, S. Z., Yun, C.-H., Hollenberg, P. F., and Miller, G. P. (2010) sheet 2– helix C loop of cytochrome P450 reductase serves as a docking site for redox partners. Biochim. Biophys. Acta 1804, 1285–1293 CrossRef Medline
40. Nisimoto, Y. (1986) Localization of cytochrome c-binding domain on NADPH-cytochrome P-450 reductase. J. Biol. Chem. 261, 14232–14239 Medline
41. Shen, A. L., and Kasper, C. B. (1995) Role of acidic residues in the interaction of NADPH-cytochrome P450 oxidoreductase with cytochrome P450 and cytochrome c. J. Biol. Chem. 270, 27475–27480 CrossRef Medline
42. Zhao, Q., Modi, S., Smith, G., Paine, M., McDonagh, P. D., Wolf, C. R., Tew, D., Lian, L. Y., Roberts, G. C., and Driessen, H. P. (1999) Crystal structure of the FMN-binding domain of human cytochrome P450 reductase at 1.93 Å resolution. Protein Sci. 8, 298 –306 Medline
43. Huang, R., Zhang, M., Rwere, F., Waskell, L., and 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 CrossRef Medline
44. van Zundert, G. C. P., Rodrigues J. P. G. L. M., Trellet, M., Schmitz, C., Kastritis, P. L., Karaca, E., Melquiond, A. S. J., van Dijk, M., de Vries, S. J., and Bonvin, A. M. J. J. (2016) The HADDOCK2.2 web server: user-friendly integrative modeling of biomolecular complexes. J. Mol. Biol. 428, 720 –725 CrossRef Medline
45. Sugishima, M., Sato, H., Higashimoto, Y., Harada, J., Wada, K., Fukuyama, K., and 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. U.S.A. 111, 2524 –2529 CrossRef Medline
46. 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 CrossRef Medline
47. Grunau, A., Paine, M. J., Ladbury, J. E., and Gutierrez, A. (2006) Global effects of the energetics of coenzyme binding: NADPH controls the protein interaction properties of human cytochrome P450 reductase. Biochemistry 45, 1421–1434 CrossRef Medline
48. Haertlein, M., Moulin, M., Devos, J. M., Laux, V., Dunne, O., and Forsyth, V. T. (2016) Biomolecular deuteration for neutron structural biology and dynamics. Methods Enzymol. 566, 113–157 CrossRef Medline
49. Svergun, D. I., Richards, S., Koch, M. H., Sayers, Z., Kuprin, S., and Zaccai, G. (1998) Protein hydration in solution: experimental observation by x-ray and neutron scattering. Proc. Natl. Acad. Sci. U.S.A. 95, 2267–2272 CrossRef Medline
50. Kline, S. R. (2006) Reduction and analysis of SANS and USANS data using IGOR Pro. J. Appl. Crystallogr. 39, 895–900 CrossRef
51. Petoukhov, M. V., Franke, D., Shkumatov, A. V., Tria, G., Kikhney, A. G., Gajda, M., Gorba, C., Mertens, H. D., Konarev, P. V., and Svergun, D. I. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342–350 CrossRef Medline
52. Konarev, P., Volkov, V., Sokolova, A., Koch, M., and Svergun, D. (2003) PRIMUS: a windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277–1282 CrossRef
53. Svergun, D. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495–503 CrossRef
54. Franke, D., and Svergun, D. I. (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342–346 CrossRef Medline
55. Volkov, V. V., and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860 – 864 CrossRef
56. Konarev, P. V., Petoukhov, M. V., and Svergun, D. I. (2016) Rapid automated superposition of shapes and macromolecular models using spherical harmonics. J. Appl. Crystallogr. 49, 953–960 CrossRef Medline
57. Panjkovich, A., and Svergun, D. I. (2016) SASpy: a PyMOL plugin for manipulation and refinement of hybrid models against small angle X-ray scattering data. Bioinformatics 32, 2062–2064 CrossRef Medline
58. DeLano, W. (2015) The PyMOL Molecular Graphics System, version 1.7.4, Schrödinger, LLC, New York
59. Russel, D., Lasker, K., Webb, B., Velázquez-Muriel, J., Tjioe, E., Schneidman-Duhovny, D., Peterson, B., and Sali, A. (2012) Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies. PLoS Biol. 10, e1001244 CrossRef Medline