A large-scale allosteric transition in cytochrome P450 3A4 revealed by luminescence resonance energy transfer (LRET)

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Sineva, Elena V ^a,b   Rumfeldt, Jessica A O ^a,c   Halpert, James R ^a   Davydov, Dmitri R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1-PYRENEBUTANOL; BROMOCRIPTINE; CYTOCHROME P450 3A; HEME; LIGAND; PYRENE DERIVATIVE;

ALLOSTERISM; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; LUMINESCENCE; METABOLISM; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ALLOSTERIC REGULATION; BROMOCRIPTINE; CYTOCHROME P-450 CYP3A; HEME; LIGANDS; LUMINESCENT MEASUREMENTS; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PYRENES;

EID: 84893466286     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083898     Document Type: Article

References (50)

1. Wilderman PR, Halpert JR (2012) Plasticity of CYP2B enzymes: Structural and solution biophysical methods. Curr Drug Metab 13: 167-176.
2. Pochapsky TC, Kazanis S, Dang M (2010) Conformational plasticity and structure/function relationships in cytochromes P450. Antioxid Redox Signal 13: 1273-1296.
3. Gay SC, Roberts AG, Halpert JR (2010) Structural features of cytochromes P450 and ligands that affect drug metabolism as revealed by x-ray crystallography and NMR. Future Med Chem 2: 1451-1468.
4. Otyepka M, Berka K, Anzenbacher P (2012) Is there a relationship between the substrate preferences and structural flexibility of cytochromes P450? Curr Drug Metab 13: 130-142.
5. Ma Q, Lu AYH (2008) The challenges of dealing with promiscuous drug-metabolizing enzymes, receptors and transporters. Curr Drug Metab 9: 374-383. (Pubitemid 352025192)
6. Atkins WM, Qian H (2011) Stochastic ensembles, conformationally adaptive teamwork, and enzymatic detoxification. Biochemistry 50: 3866-3872.
7. Davydov DR, Halpert JR (2008) Allosteric P450 mechanisms: multiple binding sites, multiple conformers or both? Expert Opin Drug Metab Toxicol 4: 1523-1535.
8. Davydov DR (2011) Microsomal monooxygenase as a multienzyme system: the role of P450-P450 interactions. Expert Opin Drug Metab Toxicol 7: 543-558.
9. Fernando H, Davydov DR, Chin CC, Halpert JR (2007) Role of subunit interactions in P450 oligomers in the loss of homotropic cooperativity in the cytochrome P450 3A4 mutant L211F/D214E/F304W. Arch Biochem Biophys 460: 129-140. (Pubitemid 46482417)
10. Williams PA, Cosme J, Vinkovic DM, Ward A, Angove HC, et al. (2004) Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 305: 683-686. (Pubitemid 39006760)
11. Roberts AG, Atkins WM (2007) Energetics of heterotropic cooperativity between alpha-naphthoflavone and testosterone binding to CYP3A4. Arch Biochem Biophys 463: 89-101. (Pubitemid 46879710)
12. Davydov DR, Rumfeldt JAO, Sineva EV, Fernando H, Davydova NY, et al. (2012) Peripheral ligand-binding site in cytochrome P450 3A4 located with fuorescence resonance energy transfer (FRET). J Biol Chem 287: 6797-6809.
13. Davydov DR, Davydova NY, Sineva EV, Kufareva I, Halpert JR (2013) Pivotal role of P450-P450 interactions in CYP3A4 allostery: the case of α-naphthoflavone. Biochem J 453: 219-230.
14. Atkins WM, Wang RW, Lu AYH (2001) Allosteric behavior in cytochrome P450-dependent in vitro drug-drug interactions: A prospective based on conformational dynamics. Chem Res Toxicol 14: 338-347. (Pubitemid 32367465)
15. Isin EM, Guengerich FP (2006) Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4. J Biol Chem 281: 9127-9136. (Pubitemid 43864626)
16. Isin EM, Guengerich FP (2008) Substrate binding to cytochromes P450. Anal Bioanal Chem 392: 1019-1030.
17. Davydov DR, Botchkareva AE, Davydova NE, Halpert JR (2005) Resolution of two substrate-binding sites in an engineered cytochrome P450eryF bearing a fluorescent probe. Biophys J 89: 418-432. (Pubitemid 41098297)
18. Tsalkova TN, Davydova NY, Halpert JR, Davydov DR (2007) Mechanism of interactions of alpha-naphthoflavone with cytochrome p450 3A4 explored with an engineered enzyme bearing a fluorescent probe. Biochemistry 46: 106-119. (Pubitemid 46075020)
19. Fernando H, Halpert JR, Davydov DR (2006) Resolution of multiple substrate binding sites in cytochrome P450 3A4: The stoichiometry of the enzymesubstrate complexes probed by FRET and Job's titration. Biochemistry 45: 4199-4209.
20. Fernando H, Rumfeldt JA, Davydova NY, Halpert JR, Davydov DR (2011) Multiple substrate-binding sites are retained in cytochrome P450 3A4 mutants with decreased cooperativity. Xenobiotica 41: 281-289.
21. Nakajima M, Kobayashi K, Oshima K, Shimada N, Tokudome S, et al. (1999) Activation of phenacetin O-deethylase activity by alpha-naphthoflavone in human liver microsomes. Xenobiotica 29: 885-898. (Pubitemid 29454382)
22. Koley AP, Buters JTM, Robinson RC, Markowitz A, Friedman FK (1997) Differential mechanisms of cytochrome P450 inhibition and activation by alpha-naphthoflavone. J Biol Chem 272: 3149-3152. (Pubitemid 27066801)
23. Nakamura H, Nakasa H, Ishii I, Ariyoshi N, Igarashi T, et al. (2002) Effects of endogenous steroids on CYP3A4-mediated drug metabolism by human liver microsomes. Drug Metab Disp 30: 534-540. (Pubitemid 34456975)
24. Kenworthy KE, Clarke SE, Andrews J, Houston JB (2001) Multisite kinetic models for CYP3A4: Simultaneous activation and inhibition of diazepam and testosterone metabolism. Drug Metab Disp 29: 1644-1651. (Pubitemid 33111598)
25. Shinkyo R, Guengerich FP (2011) Inhibition of human cytochrome P450 3A4 by cholesterol. J Biol Chem 286: 18426-18433.
26. Harlow GR, Halpert JR (1998) Analysis of human cytochrome P450 3A4 cooperativity: Construction and characterization of a site-directed mutant that displays hyperbolic steroid hydroxylation kinetics. Proc Natl Acad Sci USA 95: 6636-6641. (Pubitemid 28278032)
27. Davydov DR, Baas BJ, Sligar SG, Halpert JR (2007) 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: 7852-7864. (Pubitemid 47016068)
28. +-ATPase as monitored using fluorescence energy-transfer. Biophys J 61: 553-568.
29. Hunziker PE, Hughes GJ, Wilson KJ (1980) Peptide fragmentation suitable for solid-phase microsequencing - use of N-bromosuccinimide and BNPS-skatole {3-bromo-3-methyl-2-[(2-nitrophenyl)thio]-3H-indole}. Biochem J 187: 515-519.
30. Vestling MM, Kelly MA, Fenselau C (1994) Optimization by mass-spectrometry of a tryptophan-specific protein cleavage reaction. Rapid Commun Mass Spectr 8: 786-790. (Pubitemid 2139499)
31. Davydov DR, Femando H, Halpert JR (2006) Variable path length and counterflow continuous variation methods for the study of the formation of high-affinity complexes by absorbance spectroscopy. An application to the studies of substrate binding in cytochrome P450. Biophys Chem 123: 95-101. (Pubitemid 44279169)
32. Xiao M, Selvin PR (2001) Quantum yields of luminescent lanthanide chelates and far-red dyes measured by resonance energy transfer. J Am Chem Soc 123: 7067-7073. (Pubitemid 32879497)
33. Dixon JM, Taniguchi M, Lindsey JS (2005) PhotochemCAD-2: A refined program with accompanying spectral databases for photochemical calculations. Photochem Photobiol 81: 212-213. (Pubitemid 40327582)
34. Segel IH (1975) Enzyme kinetics: Behavior and analysis of rapid equilibrium and steady-state enzyme systems. New York: Wiley-Interscience.
35. Davydov DR, Deprez E, Hoa GHB, Knyushko TV, Kuznetsova GP, et al. (1995) High-pressure-induced transitions in microsomal cytochrome P450 2B4 in solution - evidence for conformational inhomogeneity in the oligomers. Arch Biochem Biophys 320: 330-344.
36. Selvin PR (2002) Principles and biophysical applications of lanthanide-based probes. Annual Review of Biophysics and Biomolecular Structure 31: 275-302.
37. Faulkner S, Pope SJA, Burton-Pye BP (2005) Lanthanide complexes for luminescence imaging applications. Applied Spectroscopy Reviews 40: 1-31. (Pubitemid 40168225)
38. Bowers PG, Porter G (1967) Triplet state quantum yields for some aromatic hydorcarbons and xanthene dyes in dilute solution. Proc Roy Soc A299: 348.
39. Duchowicz R, Ferrer ML, Acuna AU (1998) Kinetic spectroscopy of erythrosin phosphorescence and delayed fluorescence in aqueous solution at room temperature. Photochem Photobiol 68: 494-501. (Pubitemid 128471984)
40. Yu XF, Cojocaru V, Wade RC (2013) Conformational diversity and ligand tunnels of mammalian cytochrome P450s. Biotechnol Appl Biochem 60: 134-145.
41. Turro NJ, Scaiano JC (2010) Modern Molecular Photochemistry. Sausalito, CA: University Science Books.
42. Lettinga MP, Han ZH, van Zandvoort MAMJ (2000) Phosphorescence and fluorescence characterization of fluorescein derivatives immobilized in various polymer matrices. Phys Chem Chem Phys 2: 3697-3707.
43. Haas E, Katchalski-Katzir E, Steinberg IZ (1978) Effect of Orientation of Donor and Acceptor on Probability of Energy-Transfer Involving Electronic-Transitions of Mixed Polarization. Biochemistry 17: 5064-5070.
44. dos Remedios CG, Moens PDY (1999) Resonance energy transfer in proteins. In: Andrews DL, Demidov AA, editors. Resonance Energy Transfer. New York: Willey. pp. 1 - 64.
45. Ma BY, Shatsky M, Wolfson HJ, Nussinov R (2002) Multiple diverse ligands binding at a single protein site: A matter of pre-existing populations. Protein Sci 11: 184-197. (Pubitemid 34075781)
46. del Sol A, Tsai CJ, Ma BY, Nussinov R (2009) The Origin of Allosteric Functional Modulation: Multiple Pre-existing Pathways. Structure 17: 1042-1050.
47. Sevrioukova IF, Poulos TL (2012) Structural and mechanistic insights into the interaction of cytochrome P4503A4 with bromoergocryptine, a type I ligand. J Biol Chem 287: 3510-3517.
48. Sevrioukova IF, Poulos TL (2013) Understanding the mechanism of cytochrome P450 3A4: recent advances and remaining problems. Dalton Trans 42: 3116-3126.
49. Graham-Lorence S, Peterson JA (1996) P450s: Structural similarities and functional differences. FASEB J 10: 206-214. (Pubitemid 26079940)
50. Baylon JL, Lenov IL, Sligar SG, Tajkhorshid E (2013) Characterizing the membrane-bound state of cytochrome P450 3A4: structure, depth of Insertion, and orientation. J Am Chem Soc 135: 8542-8551.