Correction: The hinge segment of human NADPH-cytochrome P450 reductase in conformational switching: The critical role of ionic strength [Front. Pharmacol., 8, (2017) (755)] Doi: 10.3389/fphar.2017.00755;The hinge segment of human NADPH-cytochrome P450 reductase in conformational switching: The critical role of ionic strength

Frontiers in Pharmacology

Volumn 8, Issue OCT, 2017, Pages

  Campelo, Diana ^a   Lautier, Thomas ^b   Urban, Philippe ^b   Esteves, Francisco ^a   Bozonnet, Sophie ^b   Truan, Gilles ^b   Kranendonk, Michel ^a  

^a NOVA MEDICAL SCHOOL   (Portugal)

^b INSA   (France)

Author keywords

Conformational exchange; Diflavin reductase; Electron transfer; Multidomain proteins; Protein dynamics; Protein protein interaction

Indexed keywords

2,6 DICHLOROPHENOLINDOPHENOL; CYTOCHROME C; FERRICYANIDE; POTASSIUM CHLORIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE FERRIHEMOPROTEIN REDUCTASE; SODIUM CHLORIDE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL PARAMETERS; CONCENTRATION (PARAMETERS); CONFORMATIONAL EQUILIBRIUM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME STRUCTURE; HINGE SEGMENT; IONIC STRENGTH; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; OXIDATION REDUCTION STATE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EID: 85032575755     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2018.00175     Document Type: Erratum

References (52)

1. Aigrain, L., Pompon, D., Moréra, S., and Truan, G. (2009). Structure of the open conformation of a functional chimeric NADPH cytochrome P450 reductase. EMBO Rep. 10, 742-747. doi: 10.1038/embor.2009.82
2. Aigrain, L., Pompon, D., and Truan, G. (2011). Role of the interface between the FMN and FAD domains in the control of redox potential and electronic transfer of NADPH-cytochrome P450 reductase. Biochem. J. 435, 197-206. doi: 10.1042/BJ20101984
3. Bridges, A., Gruenke, L., Chang, Y.-T., Vakser, I. A., Loew, G., and Waskell, L. (1998). Identification of the binding site on cytochrome P450 2B4 for cytochrome b 5 and cytochrome P450 reductase. J. Biol. Chem. 273, 17036-17049. doi: 10.1074/jbc.273.27.17036
4. Coon, M. J. (2005). Cytochrome P450: nature's most versatile biological catalyst. Annu. Rev. Pharmacol. Toxicol. 45, 1-25. doi: 10.1146/annurev.pharmtox.45.120403.100030
5. Davydov, D. R., Kariakin, A. A., Petushkova, N. A., and Peterson, J. A. (2000). Association of cytochromes P450 with their reductases: opposite sign of the electrostatic interactions in P450BM-3 as compared with the microsomal 2B4 system. Biochemistry 39, 6489-6497. doi: 10.1021/bi992936u
6. Davydov, D. R., Knyushko, T. V., Kanaeva, I. P., Koen, Y. M., Samenkova, N. F., Archakov, A. I., et al. (1996). Interactions of cytochrome P450 2B4 with NADPH-cytochrome P450 reductase studied by fluorescent probe. Biochimie 78, 734-743. doi: 10.1016/S0300-9084(97)82531-X
7. Duarte, M. P., Palma, B. B., Laires, A., Oliveira, J. S., Rueff, J., and Kranendonk, M. (2005). Escherichia coli BTC, a human cytochrome P450 competent tester strain with a high sensitivity towards alkylating agents: involvement of alkyltransferases in the repair of DNA damage induced by aromatic amines. Mutagenesis 20, 199-208. doi: 10.1093/mutage/gei028
8. Ellis, J., Gutierrez, A., Barsukov, I. L., Huang, W.-C., Grossmann, J. G., and Roberts, G. C. K. (2009). Domain motion in cytochrome P450 reductase: conformational equilibria revealed by NMR and small-angle x-ray scattering. J. Biol. Chem. 284, 36628-36637. doi: 10.1074/jbc.M109.054304
9. Frances, O., Fatemi, F., Pompon, D., Guittet, E., Sizun, C., Pérez, J., et al. (2015). A well-balanced preexisting equilibrium governs electron flux efficiency of a multi-domain diflavin reductase. Biophys. J. 108, 1527-1536. doi: 10.1016/j.bpj.2015.01.032
10. Gopal, D., Wilson, G. S., Earl, R. A., and Cusanovich, M. A. (1988). Cytochrome c: ion binding and redox properties. Studies on ferri and ferro forms of horse, bovine, and tuna cytochrome c. J. Biol. Chem. 263, 11652-11656
11. Grunau, A., Geraki, K., Grossmann, J. G., and Gutierrez, A. (2007). Conformational dynamics and the energetics of protein-ligand interactions: role of interdomain loop in human cytochrome P450 reductase. Biochemistry 46, 8244-8255. doi: 10.1021/bi700596s
12. 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. doi: 10.1021/bi052115r
13. Guengerich, F. P. (2007). Mechanisms of cytochrome P450 substrate oxidation: MiniReview. J. Biochem. Mol. Toxicol. 21, 163-168. doi: 10.1002/jbt.20174
14. 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. doi: 10.1074/jbc.M807868200
15. Haque, M. M., Bayachou, M., Tejero, J., Kenney, C. T., Pearl, N. M., Im, S.-C., et al. (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. doi: 10.1111/febs.13073
16. 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. doi: 10.1074/jbc.M112.339697
17. Haque, M. M., Panda, K., Tejero, J., Aulak, K. S., Fadlalla, M. A., Mustovich, A. T., et al. (2007). A connecting hinge represses the activity of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 104, 9254-9259. doi: 10.1073/pnas.0700332104
18. Haque, M. M., Tejero, J., Bayachou, M., Wang, Z.-Q., Fadlalla, M., and Stuehr, D. J. (2013). Thermodynamic characterization of five key kinetic parameters that define neuronal nitric oxide synthase catalysis. FEBS J. 280, 4439-4453. doi: 10.1111/febs.12404
19. Hay, S., Brenner, S., Khara, B., Quinn, A. M., Rigby, S. E. J., 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. doi: 10.1021/ja1016206
20. Hlavica, P., Schulze, J., and Lewis, D. F. V. (2003). Functional interaction of cytochrome P450 with its redox partners: a critical assessment and update of the topology of predicted contact regions. J. Inorg. Biochem. 96, 279-297. doi: 10.1016/S0162-0134(03)00152-1
21. Huang, W.-C., Ellis, J., Moody, P. C. E., Raven, E. L., and Roberts, G. C. K. (2013). Redox-linked domain movements in the catalytic cycle of cytochrome P450 reductase. Structure 21, 1581-1589. doi: 10.1016/j.str.2013.06.022
22. Kranendonk, M., Marohnic, C. C., Panda, S. P., Duarte, M. P., Oliveira, J. S., Masters, B. S. S., et al. (2008). Impairment of human CYP1A2-mediated xenobiotic metabolism by Antley-Bixler syndrome variants of cytochrome P450 oxidoreductase. Arch. Biochem. Biophys. 475, 93-99. doi: 10.1016/j.abb.2008.04.014
23. Lamb, D. C., Kim, Y., Yermalitskaya, L. V., Yermalitsky, V. N., Lepesheva, G. I., Kelly, S. L., et al. (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. doi: 10.1016/j.str.2005.09.015
24. Lamb, D. C., and Waterman, M. R. (2013). Unusual properties of the cytochrome P450 superfamily. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368:20120434. doi: 10.1098/rstb.2012.0434
25. Marohnic, C. C., Panda, S. P., McCammon, K., Rueff, J., Masters, B. S. S., and Kranendonk, M. (2010). Human cytochrome P450 oxidoreductase deficiency caused by the Y181D mutation: molecular consequences and rescue of defect. Drug Metab. Dispos. 38, 332-340. doi: 10.1124/dmd.109.030445
26. McCammon, K. M., Panda, S. P., Xia, C., Kim, J.-J. P., Moutinho, D., Kranendonk, M., et al. (2016). Instability of the human cytochrome P450 reductase A287P variant is the major contributor to its antley-bixler syndrome-like phenotype. J. Biol. Chem. 291, 20487-20502. doi: 10.1074/jbc.M116.716019
27. Miyazaki, K., and Takenouchi, M. (2002). Creating random mutagenesis libraries using megaprimer PCR of whole plasmid. BioTechniques 33, 1036-1038
28. Munro, A. W., Girvan, H. M., Mason, A. E., Dunford, A. J., and McLean, K. J. (2013). What makes a P450 tick? Trends Biochem. Sci. 38, 140-150. doi: 10.1016/j.tibs.2012.11.006
29. Murataliev, M. B., Ariño, A., Guzov, V. M., and Feyereisen, R. (1999). Kinetic mechanism of cytochrome P450 reductase from the house fly (Musca domestica). Insect. Biochem. Mol. Biol. 29, 233-242. doi: 10.1016/S0965-1748(98)00131-3
30. Nadler, S. G., and Strobel, H. W. (1988). Role of electrostatic interactions in the reaction of NADPH-cytochrome P-450 reductase with cytochromes P-450. Arch. Biochem. Biophys. 261, 418-429. doi: 10.1016/0003-9861(88)90358-X
31. Nadler, S. G., and Strobel, H. W. (1991). Identification and characterization of an NADPH-cytochrome P450 reductase derived peptide involved in binding to cytochrome P450. Arch. Biochem. Biophys. 290, 277-284. doi: 10.1016/0003-9861(91)90542-Q
32. Nishino, H., and Ishibashi, T. (2000). Evidence for requirement of NADPH-cytochrome P450 oxidoreductase in the microsomal NADPH-sterol Delta7-reductase system. Arch. Biochem. Biophys. 374, 293-298. doi: 10.1006/abbi.1999.1602
33. Ono, T., and Bloch, K. (1975). Solubilization and partial characterization of rat liver squalene epoxidase. J. Biol. Chem. 250, 1571-1579
34. O'Reilly, J. E. (1973). Oxidation-reduction potential of the ferro-ferricyanide system in buffer solutions. Biochim. Biophys. Acta 292, 509-515. doi: 10.1016/0005-2728(73)90001-7
35. Oshino, N., Imai, Y., and Sato, R. (1971). A function of cytochrome b5 in fatty acid desaturation by rat liver microsomes. J. Biochem. 69, 155-167. doi: 10.1093/oxfordjournals.jbchem.a129444
36. Palma, B. B., Silva, E., Sousa, M., Urban, P., Rueff, J., and Kranendonk, M. (2013). Functional characterization of eight human CYP1A2 variants: the role of cytochrome b5. Pharmacogenet. Genomics 23, 41-52. doi: 10.1097/FPC.0b013e32835c2ddf
37. 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
38. Rendic, S., and Guengerich, F. P. (2015). Survey of human oxidoreductases and cytochrome P450 enzymes involved in the metabolism of xenobiotic and natural chemicals. Chem. Res. Toxicol. 28, 38-42. doi: 10.1021/tx500444e
39. Roman, L. J., Miller, R. T., de la Garza, M. A., Kim, J.-J. P., and Masters, B. S. S. (2000). The C terminus of mouse macrophage inducible nitric-oxide synthase attenuates electron flow through the flavin domain. J. Biol. Chem. 275, 21914-21919. doi: 10.1074/jbc.M002449200
40. Sadeghi, S. J., Valetti, F., Cunha, C. A., Romão, M. J., Soares, C. M., and Gilardi, G. (2000). Ionic strength dependence of the non-physiological electron transfer between flavodoxin and cytochrome c553 from D. vulgaris. J. Biol. Inorg. Chem. 5, 730-737. doi: 10.1007/s007750000162
41. Schacter, B. A., Nelson, E. B., Marver, H. S., and Masters, B. S. (1972). Immunochemical evidence for an association of heme oxygenase with the microsomal electron transport system. J. Biol. Chem. 247, 3601-3607
42. Schrödinger (2015). The PyMOL Molecular Graphics System, Version 1.8. New York, NY: Schrödinger
43. Scott, E. E., Wolf, C. R., Otyepka, M., Humphreys, S. C., Reed, J. R., Henderson, C. J., et al. (2016). The role of protein-protein and protein-membrane interactions on P450 function. Drug Metab. Dispos. 44, 576-590. doi: 10.1124/dmd.115.068569
44. 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. doi: 10.1074/jbc.270.46.27475
45. Sündermann, A., and Oostenbrink, C. (2013). Molecular dynamics simulations give insight into the conformational change, complex formation, and electron transfer pathway for cytochrome P450 reductase. Protein Sci. 22, 1183-1195. doi: 10.1002/pro.2307
46. 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
47. Vermilion, J. L., Ballou, D. P., Massey, V., and Coon, M. J. (1981). Separate roles for FMN and FAD in catalysis by liver microsomal NADPH-cytochrome P-450 reductase. J. Biol. Chem. 256, 266-277
48. Vincent, B., Morellet, N., Fatemi, F., Aigrain, L., Truan, G., Guittet, E., et al. (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. doi: 10.1016/j.jmb.2012.03.022
49. Voznesensky, A. I., and Schenkman, J. B. (1992). The cytochrome P450 2B4-NADPH cytochrome P450 reductase electron transfer complex is not formed by charge-pairing. J. Biol. Chem. 267, 14669-14676
50. Wang, M., Roberts, D. L., Paschke, R., Shea, T. M., Masters, B. S. S., and Kim, J.-J. P. (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. doi: 10.1073/pnas.94.16.8411
51. Xia, C., Hamdane, D., Shen, A. L., Choi, V., Kasper, C. B., Pearl, N. M., et al. (2011a). Conformational changes of NADPH-cytochrome P450 oxidoreductase are essential for catalysis and cofactor binding. J. Biol. Chem. 286, 16246-16260. doi: 10.1074/jbc.M111.230532
52. Xia, C., Panda, S. P., Marohnic, C. C., Martásek, P., Masters, B. S., and Kim, J.-J. P. (2011b). Structural basis for human NADPH-cytochrome P450 oxidoreductase deficiency. Proc. Natl. Acad. Sci. U.S.A. 108, 13486-13491. doi: 10.1073/pnas.1106632108