Uncovering the role of hydrophobic residues in cytochrome P450-cytochrome P450 reductase interactions

Biochemistry

Volumn 50, Issue 19, 2011, Pages 3957-3967

  Kenaan, Cesar ^a,b   Zhang, Haoming ^b   Shea, Erin V ^b   Hollenberg, Paul F ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CO FORMATION; COMPLEX FORMATIONS; CYSTEINE RESIDUES; CYTOCHROME P450; CYTOCHROME P450 REDUCTASE; DRUG METABOLISMS; FLUORESCENCE ENHANCEMENT; FLUORESCENCE INTENSITIES; FLUORESCENCE LABELING; HYDROPHOBIC RESIDUES; INTRINSIC KINETICS; REACTIVE CYSTEINE; REDOX PARTNERS; STOPPED FLOW;

AMINO ACIDS; BINDING SITES; FLUORESCENCE; GENETIC ENGINEERING; HYDROPHOBICITY;

DRUG INTERACTIONS;

BENZPHETAMINE; CYSTEINE; CYTOCHROME P450; CYTOCHROME P450 REDUCTASE; ENZYME VARIANT; MUTANT PROTEIN; TERT BUTYL HYDROPEROXIDE;

ARTICLE; CONTROLLED STUDY; DRUG METABOLISM; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME KINETICS; FLUORESCENCE; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; WILD TYPE;

ANIMALS; ARYL HYDROCARBON HYDROXYLASES; CYTOCHROME P-450 ENZYME SYSTEM; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LEUCINE; MUTAGENESIS, SITE-DIRECTED; NADPH-FERRIHEMOPROTEIN REDUCTASE; RATS; SPECTROMETRY, FLUORESCENCE; SURFACE PROPERTIES; VALINE;

EID: 79955833019     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1020748     Document Type: Article

References (49)

1. Denisov, I. G., Makris, T. M., Sligar, S. G., and Schlichting, I. (2005) Structure and Chemistry of Cytochrome P450 Chem. Rev. 105, 2253-2277 (Pubitemid 40951784)
2. Rittle, J. and Green, M. T. (2010) Cytochrome P450 Compound I: Capture, Characterization, and C-H Bond Activation Kinetics Science 330, 933-937
3. 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
4. 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
5. 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)
6. Cawley, G. F., Batie, C. J., and Backes, W. L. (1995) Substrate-dependent competition of different P450 isozymes for limiting NADPH-cytochrome P450 reductase Biochemistry 34, 1244-1247
7. Backes, W. L. and Kelley, R. W. (2003) Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes Pharmacol. Ther. 98, 221-233 (Pubitemid 36513776)
8. Enoch, H. G. and Strittmatter, P. (1979) Cytochrome b5 reduction by NADPH-cytochrome P-450 reductase J. Biol. Chem. 254, 8976-8981
9. Williams, C. H., Jr. and Kamin., H. (1962) Microsomal triphosphopyridine nucleotide-cytochrome c reductase of liver J. Biol. Chem. 237, 587-595
10. Kikuchi, G., Yoshida, T., and Noguchi, M. (2005) Heme oxygenase and heme degradation Biochem. Biophys. Res. Commun. 338, 558-567 (Pubitemid 41540603)
11. Ono, T. and Bloch, K. (1975) Solubilization and partial characterization of rat liver squalene epoxidase J. Biol. Chem. 250, 1571-1579
12. Jang, H. H., Jamakhandi, A. P., Sullivan, S. Z., Yun, C. H., Hollenberg, P. F., and Miller, G. P. (2010) Beta sheet 2-alpha helix C loop of cytochrome P450 reductase serves as a docking site for redox partners Biochim. Biophys. Acta 1804, 1285-1293
13. 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
14. Shimizu, T., Tateishi, T., Hatano, M., and Fujii-Kuriyama, Y. (1991) Probing the role of lysines and arginines in the catalytic function of cytochrome P450d by site-directed mutagenesis. Interaction with NADPH-cytochrome P450 reductase J. Biol. Chem. 266, 3372-3375 (Pubitemid 21909220)
15. 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 b5 and cytochrome P450 reductase J. Biol. Chem. 273, 17036-17049 (Pubitemid 28311737)
16. Gao, Q., Doneanu, C. E., Shaffer, S. A., Adman., E. T., Goodlett, D. R., and Nelson, S. D. (2006) Identification of the interactions between cytochrome P450 2E1 and cytochrome b5 by mass spectrometry and site-directed mutagenesis J. Biol. Chem. 281, 20404-20417 (Pubitemid 44065814)
17. Bumpus, N. N. and Hollenberg, P. F. (2010) Cross-linking of human cytochrome P450 2B6 to NADPH-cytochrome P450 reductase: Identification of a potential site of interaction J. Inorg. Biochem. 104, 485-488
18. Sevrioukova, I. F. and Poulos, T. L. (2011) Structural biology of redox partner interactions in P450cam monooxygenase: A fresh look at an old system Arch. Biochem. Biophys. 501, 66-74
19. Sevrioukova, I. F., Li, H., Zhang, H., Peterson, J. A., and Poulos, T. L. (1999) Structure of a cytochrome P450-redox partner electron-transfer complex Proc. Natl. Acad. Sci. U.S.A. 96, 1863-1868 (Pubitemid 29117833)
20. Sevrioukova, I. F., Poulos, T. L., and Churbanova, I. Y. (2010) Crystal structure of the putidaredoxin reductase x putidaredoxin electron transfer complex J. Biol. Chem. 285, 13616-13620
21. 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
22. Voznesensky, A. I. and Schenkman, J. B. (1994) Quantitative analyses of electrostatic interactions between NADPH-cytochrome P450 reductase and cytochrome P450 enzymes J. Biol. Chem. 269, 15724-15731
23. Hassan, A. Q., Wang, Y., Plate, L., and Stubbe, J. (2008) Methodology to probe subunit interactions in ribonucleotide reductases Biochemistry 47, 13046-13055
24. Drees, B. L., Rye, H. S., Glazer, A. N., and Nelson, H. C. (1996) Environment-sensitive labels in multiplex fluorescence analyses of protein-DNA complexes J. Biol. Chem. 271, 32168-32173 (Pubitemid 26422249)
25. Sevrioukova, I. F., Hazzard, J. T., Tollin, G., and Poulos, T. L. (1999) The FMN to heme electron transfer in cytochrome P450BM-3. Effect of chemical modification of cysteines engineered at the FMN-heme domain interaction site J. Biol. Chem. 274, 36097-36106
26. Zhang, H., Im, S. C., and Waskell, L. (2007) Cytochrome b5 increases the rate of product formation by cytochrome P450 2B4 and competes with cytochrome P450 reductase for a binding site on cytochrome P450 2B4 J. Biol. Chem. 282, 29766-29776 (Pubitemid 350035259)
27. Omura, T. and Sato, R. (1964) The Carbon Monoxide-Binding Pigment of Liver Microsomes. II. Solubilization, Purification, and Properties J. Biol. Chem. 239, 2379-2385
28. Vermilion, J. L. and Coon, M. J. (1978) Purified liver microsomal NADPH-cytochrome P-450 reductase. Spectral characterization of oxidation-reduction states J. Biol. Chem. 253, 2694-2704 (Pubitemid 8328429)
29. Miwa, G. T., West, S. B., Huang, M. T., and Lu, A. Y. (1979) Studies on the association of cytochrome P-450 and NADPH-cytochrome c reductase during catalysis in a reconstituted hydroxylating system J. Biol. Chem. 254, 5695-5700
30. French, J. S., Guengerich, F. P., and Coon, M. J. (1980) Interactions of cytochrome P-450, NADPH-cytochrome P-450 reductase, phospholipid, and substrate in the reconstituted liver microsomal enzyme system J. Biol. Chem. 255, 4112-4119
31. Davydov, D. R., Knyushko, T. V., Kanaeva, I. P., Koen, Y. M., Samenkova, N. F., Archakov, A. I., and Hui Bon Hoa, G. (1996) Interactions of cytochrome P450 2B4 with NADPH-cytochrome P450 reductase studied by fluorescent probe Biochimie 78, 734-743 (Pubitemid 27025963)
32. Nash, T. (1953) The colorimetric estimation of formaldehyde by means of the Hantzech reaction Biochem. J. 55, 416-421
33. Coon, M. J., Hoeven, T. A., Kaschnitz, R. M., and Strobel, H. W. (1973) Biochemical studies on cytochrome P-450 solubilized from liver microsomes: partial purification and mechanism of catalysis Ann. N.Y. Acad. Sci. 212, 449-457
34. Scott, E. E., White, M. A., He, Y. A., Johnson, E. F., Stout, C. D., and Halpert, J. R. (2004) Structure of mammalian cytochrome P450 2B4 complexed with 4-(4-chlorophenyl)imidazole at 1.9-A resolution: insight into the range of P450 conformations and the coordination of redox partner binding J. Biol. Chem. 279, 27294-27301 (Pubitemid 38812569)
35. Lehnerer, M., Schulze, J., Achterhold, K., Lewis, D. F., and Hlavica, P. (2000) Identification of key residues in rabbit liver microsomal cytochrome P450 2B4: importance in interactions with NADPH-cytochrome P450 reductase J Biochem. 127, 163-169 (Pubitemid 30094106)
36. Hermanson, G. T. (1996) Bioconjugate Techniques, Academic Press, San Diego, CA.
37. Backes, W. L. and Eyer, C. S. (1989) Cytochrome P-450 LM2 reduction. Substrate effects on the rate of reductase-LM2 association J. Biol. Chem. 264, 6252-6259 (Pubitemid 19106700)
38. Scott, E. E., He, Y. A., Wester, M. R., White, M. A., Chin, C. C., Halpert, J. R., Johnson, E. F., and Stout, C. D. (2003) An open conformation of mammalian cytochrome P450 2B4 at 1.6-A resolution Proc. Natl. Acad. Sci. U.S.A. 100, 13196-13201 (Pubitemid 37444718)
39. Zhang, H., Kenaan, C., Hamdane, D., Hoa, G. H., and Hollenberg, P. F. (2009) Effect of conformational dynamics on substrate recognition and specificity as probed by the introduction of a de novo disulfide bond into cytochrome P450 2B1 J. Biol. Chem. 284, 25678-25686
40. Gray, H. B. and Winkler, J. R. (1996) Electron transfer in proteins Annu. Rev. Biochem. 65, 537-561 (Pubitemid 26250619)
41. Jones, S. and Thornton, J. M. (1996) Principles of protein-protein interactions Proc. Natl. Acad. Sci. U.S.A. 93, 13-20 (Pubitemid 26038096)
42. Clackson, T., Ultsch, M. H., Wells, J. A., and de Vos, A. M. (1998) Structural and functional analysis of the 1:1 growth hormone:receptor complex reveals the molecular basis for receptor affinity J. Mol. Biol. 277, 1111-1128 (Pubitemid 28190850)
43. http://www.ebi.ac.uk/Tools/emboss/align/index.html.
44. Rodgers, K. K. and Sligar, S. G. (1991) Mapping electrostatic interactions in macromolecular associations J. Mol. Biol. 221, 1453-1460 (Pubitemid 121003465)
45. Black, S. D., French, J. S., Williams, C. H., Jr., and Coon, M. J. (1979) Role of a hydrophobic polypeptide in the N-terminal region of NADPH-cytochrome P-450 reductase in complex formation with P-450LM Biochem. Biophys. Res. Commun. 91, 1528-1535
46. Stayton, P. S. and Sligar, S. G. (1990) The cytochrome P-450cam binding surface as defined by site-directed mutagenesis and electrostatic modeling Biochemistry 29, 7381-7386 (Pubitemid 20251786)
47. Selzer, T., Albeck, S., and Schreiber, G. (2000) Rational design of faster associating and tighter binding protein complexes Nat. Struct. Biol. 7, 537-541 (Pubitemid 30445907)
48. Xiong, P., Nocek, J. M., Griffin, A. K., Wang, J., and Hoffman, B. M. (2009) Electrostatic redesign of the [myoglobin, cytochrome b5] interface to create a well-defined docked complex with rapid interprotein electron transfer J. Am. Chem. Soc. 131, 6938-6939
49. Guengerich, F. P. (2002) Cytochrome P450 enzymes in the generation of commercial products Nat. Rev. Drug Discovery 1, 359-366 (Pubitemid 37361465)