Conformational dynamics of the cytochrome P450 BM3/N-palmitoylglycine complex: The proposed "proximal-distal" transition probed by temperature-jump spectroscopy

Journal of Physical Chemistry B

Volumn 111, Issue 27, 2007, Pages 7879-7886

  Brenner, Sibylle ^a   Hay, Sam ^a   Girvan, Hazel M ^a   Munro, Andrew W ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CONFORMATIONS; MOLECULAR DYNAMICS; PHASE EQUILIBRIA; RATE CONSTANTS; RELAXATION PROCESSES; THERMAL EFFECTS;

MUTANTS; N-PALMITOYLGLYCINE (NPG)-BOUND ENZYME SPECIE; SUBSTRATE-FREE ENZYME; TEMPERATURE-JUMP SPECTROSCOPY;

PROTEINS;

EID: 34547442056     PISSN: 15206106     EISSN: None     Source Type: Journal    
DOI: 10.1021/jp073036n     Document Type: Article

References (58)

1. Ortiz de Montellano, P. R. Cytochrome P450: Structure, Mechanism and Biochemistry, 3rd ed.; Kluwer Academic/Plenum Press: New York, 2005; pp 377-530.
2. Denisov, I. G.; Makris, T. M.; Sligar, S. G.; Schlichting, I. Structure and chemistry of cytochrome P450. Chem. Rev. 2005, 105, 2253-2277.
3. Pylypenko, O.; Schlichting, I. Structural aspects of ligand binding to and electron transfer in bacterial and fungal P450s. Annu. Rev. Biochem. 2004. 75, 991-1018.
4. Schenkman, J. B.; Remmer, H.; Estabrook, R. W. Spectral studies of drug interaction with hepatic microsomal cytochrome. Mol. Pharmacol. 1967, 3, 113-123.
5. Schenkman, J. B. Effect of substrates on hepatic microsomal cytochrome P-450. Hoppe-Seylers Z. Physiol. Chem. 1968, 349, 1624-1628.
6. Schenkman, J. B.; Sligar, S. G.; Cinti, D. L. Substrate interaction with cytochrome P-450. Pharmacol. Ther. 1981, 12, 43-71.
7. Jefcoate, C. R.; Gaylor, J. L. Ligand interactions with hemoprotein P-450. II. Influence of phenobarbital and methylcholanthrene induction processes on P-450 spectra, Biochemistry 1969, 5, 3464-3472.
8. Jefcoate, C. R.; Gaylor, J. L.; Calabrese, R. L. Ligand interactions with cytochrome P-450. I. Binding of primary amines. Biochemistry 1969, 8, 3455-3463.
9. Griffin, B.; Peterson, J. A. Ethyl isocyanide complexes of bacterial cytochrome P-450. Arch. Biochem. Biophys. 1971, 145, 220-229.
10. Raag, R.; Poulos, T. L. The structural basis for substrate-induced changes in redox potential and spin equilibrium in cytochrome P-450CAM. Biochemistry'1999, 28, 917-922.
11. Daff, S. N.; Chapman, S. K.; Turner, K. L.; Holt, R. A.; Govindaraj, S.; Poulos, T. L.; Munro, A. W. Redox control of the catalytic cycle of flavocytochrome P-450 BM3. Biochemistry 1997, 36, 13816-13823.
12. Dawson, J. H. Probing structure-function relations in heme-containing oxygenases and peroxidases. Science 1988, 240, 433-439.
13. Fisher, M. T.; Sligar, S. Control of heme protein redox potential and reduction rate: Linear free energy relation between potential and ferric spin state equilibrium. J. Am. Chem. Soc. 1985, 107, 5018-5019.
14. Sligar, S. Coupling of spin, substrate, and redox equilibria in cytochrome P450. Biochemistry 1976, 15, 5399-5406.
15. Sligar, S. G.; Gunsalus, I. C. A thermodynamic model of regulation: modulation of redox equilibria in camphor monoxygenase. Proc. Natl. Acad. Sci. U.S.A. 1976, 73, 1078-1082.
16. Wilson, G. S.; Tsibris, J. C.; Gunsalus, I. C. Electrochemical studies of putidaredoxin and its selenium analog. J. Biol. Chem. 1973, 245, 6059-6061.
17. Schwarze, W.; Blanek, J.; Ristau, O.; Janig, G. R.; Pommerening, K.; Rein, H.; Ruckpaul, K. Spin state control of cytochrome P-450 reduction and catalytic activity in a reconstituted P-450 LM2 system as induced by a series of benzphetamine analogues. Chem. Biol. Interact. 1985, 54, 127-141.
18. Rein, H.; Ristau, O.; Misselwitz, R.; Buder, E.; Ruckpaul, K. The importance of the spin equilibrium in cytochrome P-450 for the reduction rate of the heme iron. Acta Biol. Med. Ger. 1979, 38, 187-200.
19. Backes, W. L.; Tamburini, P. P.; Jansson, I.; Gibson, G. G.; Sligar, S. G.; Schenkman, J. B. Kinetics of cytochrome P-450 reduction: evidence for faster reduction of the high-spin ferric state. Biochemistry 1985, 24, 5130-5136.
20. Honeychurch, M. J.; Hill, A. O.; Wong, L. L. The thermodynamics and kinetics of electron transfer in the cytochrome P450cam enzyme system. FEBS Lett. 1999, 451, 351-353.
21. Loida, P. J.; Sligar, S. G. Molecular recognition in cytochrome P-450: mechanism for the control of uncoupling reactions. Biochemistry 1993, 52, 11530-11538.
22. Rein, H.; Ristau, O.; Friedrich, J.; Janig, G. R.; Ruckpaul, K. Evidence for the existence of a high spin-low spin equilibrium in liver microsomal cytochrome P-450. FEBS Lett. 1977, 75, 19-22.
23. Cinti, D. L.; Sligar, S. G.; Gibson, G. G.; Schenkman, J. B. Temperature-dependent spin equilibrium of microsomal and solubilized cytochrome P-450 from rat liver. Biochemistry 1979, 18, 36-42.
24. Cole, P. E.; Sligar, S. G. Temperature-jump measurement of the spin state relaxation rate of cytochrome P450cam. FEBS Lett. 1981, 133, 252-254.
25. Fisher, M. T.; Sligar, S. G. Temperature jump relaxation kinetics of the P-450cam spin equilibrium. Biochemistry 1987, 26, 4797-4803.
26. Narasimhulu, S. Substrate-induced spin-state transition in cytochrome P450LM2: a temperature-jump relaxation study. Biochemistry 1993, 32, 10344-10350.
27. Narasimhulu, S.; Willcox, J. K. Temperature-jump relaxation kinetics of substrate-induced spin-state transition in cytochrome P450 (comparison of the wild-type and C334A mutant P450(CAM) and P450-(2B4)). Arch. Biochem. Biophys. 2001, 388, 198-206.
28. Tsong, T. Y.; Yang, C. S. Rapid conformational changes of cytochrome P-450: effect of dimyristoyl lecithin, Proc. Natl. Acad. Sci. U.S.A. 1978, 75, 5955-5959.
29. Narasimhulu, S. Differential behavior of the sub-sites of cytochrome 450 active site in binding of substrates, and products (implications for coupling/uncoupling). Biochim. Biophys. Acta 2007, 1770, 360-375.
30. Ziegler, M.; Blanek, J.; Greschner, S.; Lenz, K.; Lau, A.; Ruckpaul, K. 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 1983, 42, 641-649.
31. Narasimhulu, S. Significance of the steroid-induced type I spectral change in steroid C-21 hydroxylase system of bovine adrenocortical microsomes. Arch. Biochem. Biophys. 1971, 147, 391-404.
32. Narasimhulu, S. Uncoupling of oxygen activation from hydroxylation in the steroid C-21 hydroxylase of bovine adrenocortical microsomes. Arch. Biochem. Biophys. 1971, 147, 384-390.
33. Marden, M. C.; Hoa, G. H. P-450 binding to substrates camphor and linalool versus pressure. Arch. Biochem. Biophys. 1987, 253, 100-107.
34. Narasimhulu, S. On the model controversy for substrate-induced spin-state transition in cytochrome P450: (a new perspective). Endocr. Res. 1993, 19, 223-258.
35. Bell, S. G.; Chen, X.; Sowden, R. J.; Xu, F.; Williams, J. N.; Wong, L. L.; Rao, Z. Molecular recognition in (+)-α-pinene oxidation by cytochrome P450cam. J. Am. Chem. Soc. 2003, 125, 705-714.
36. Poulos, T. L.; Finzel, B. C.; Howard, A. J. High-resolution crystal structure of cytochrome P450cam. J. Mol. Biol. 1987, 195, 687-700.
37. Schlichting, I.; Jung, C.; Schulze, H. Crystal structure of cytochrome P-450cam complexed with the (1S)-camphor enantiomer. FEBS Lett. 1997, 415, 253-257.
38. Wester, M. R.; Johnson, E. F.; Marques-Soares, C.; Dansette, P. M.; Mansuy, D.; Stout, C. D. Structure of a substrate complex of mammalian cytochrome P450 2C5 at 2.3 Å resolution: evidence for multiple substrate binding modes. Biochemistry 2003, 42, 6370-6379.
39. Wester, M. R.; Johnson, E. F.; Marques-Soares, C.; Dijols, S.; Dansette, P. M.; Mansuy, D.; Stout, C. D. Structure of mammalian cytochrome P450 2C5 complexed with diclofenac at 2.1 Å resolution: evidence for an induced fit model of substrate binding. Biochemistry 2003, 42, 9335-9345.
40. Wester, M. R.; Yano, J. K.; Schoch, G. A.; Yang, C.; Griffin, K. J.; Stout, C. D.; Johnson, E. F. The structure of human cytochrome P450 2C9 complexed with flurbiprofen at 2.0-̊ resolution. J. Biol. Chem. 2004, 279, 35630-35637.
41. Williams, P. A.; Cosme, J.; Vinkovic, D. M.; Ward, A.; Angove, H. C.; Day, P. J.; Vonrhein, C.; Tickle, I. J.; Jhoti, H. Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 2004, 305, 683-686.
42. Li, H.; Poulos, T. L. The structure of the cytochrome P450BM-3 haem domain complexed with the fatty acid substrate, palmitoleic acid. Nat. Struct. Biol. 1997, 4, 140-146.
43. Modi, S.; Primrose, W. U.; Boyle, J. M.; Gibson, C. F.; Lian, L. Y.; Roberts, G. C. NMR studies of substrate binding to cytochrome P450 BM3: comparisons to cytochrome P450 cam. Biochemistry 1995, 34, 8982-8988.
44. Ravindranathan, K. P.; Gallicchio, E.; Friesner, R. A.; McDermott, A. E.; Levy, R. M. Conformational equilibrium of cytochrome P450 BM-3 complexed with N-palmitoylglycine: a replica exchange molecular dynamics study. J. Am. Chem Soc. 2006, 128, 5786-5791.
45. Haines, D. C.; Tomchick, D. R.; Machius, M.; Peterson, J. A. Pivotal role of water in the mechanism of P450BM-3. Biochemistry 2001, 40, 13456-13465.
46. Modi, S.; Sutcliffe, M. J.; Primrose. W. U.; Lian, L. Y.; Roberts, G. C. The catalytic mechanism of cytochrome P450 BM3 involves a 6 Å movement of the bound substrate on reduction. Nat. Struct. Biol. 1996, 3, 414-417.
47. Ravindranathan, K. P.; Gallicchio, E.; McDermott, A. E.; Levy, R. M. Conformational dynamics of substrate in the active site of cytochrome P450 BM-3/NPG complex: insights from NMR order parameters. J. Am. Chem. Soc. 2007, 129, 474-475.
48. Jovanovic, T.; McDermott, A. E. Observation of ligand binding to cytochrome P450 BM-3 by means of solid-state NMR spectroscopy. J. Am. Chem. Soc. 2005, 127, 13816-13821.
49. Jovanovic, T.; Farid, R.; Friesner, R. A.; McDermott, A. E. Thermal equilibrium of high- and low-spin forms of cytochrome P450 BM-3: repositioning of the substrate? J. Am. Chem. Soc. 2005, 127, 13548-13552.
50. Miles, J. S.; Munro, A. W.; Rospendowski, B. N.; Smith, W. E.; McKnight, J.; Thomson, A. J. Domains of the catalytically self-sufficient cytochrome P-450 BM-3. Genetic construction, overexpression, purification and spectroscopic characterization. Biochem. J. 1992, 255, 503-509.
51. Noble, M. A.; Miles, C. S.; Chapman, S. K.; Lysek, D. A.; MacKay, A. C.; Reid, G. A.; Hanzlik, R. P.; Munro, A. W. Roles of key active-site residues in flavocytochrome P450 BM3. Biochem. J. 1999, 339, 371-379.
52. Quaroni, L. C.; Seward, H. E.; McLean, K. J.; Girvan, H. M.; Ost, T. W.; Noble, M. A.; Kelly, S. M.; Price, N. C.; Cheesman, M. R.; Smith, W. E.; Munro, A. W. Interaction of nitric oxide with cytochrome P450 BM3. Biochemistry 2004, 43, 16416-16431.
53. Brenner, S.; Hay, S.; Scrutton, N. S. Application Note AN.019. T64. Hi-Tech Scientific 2006.
54. Sayed, Y.; Hornby, J. A.; Lopez, M.; Dirr, H. Thermodynamics of the ligandin function of human class Alpha, glutathione transferase A1-1: energetics of organic anion ligand binding. Biochem. J. 2002, 363, 341-346.
55. Protasevich, I. I.; Brouillette, C. G.; Snow, M. E.; Dunham, S.; Rubin, J. R.; Gogliotti, R.; Siegel, K. Role of inhibitor aliphatic chain in the thermodynamics of inhibitor binding to Escherichia coli enoyl-ACP reductase and the Phe203Leu mutant: a proposed mechanism for drug resistance. Biochemistry 2004, 43, 13380-13389.
56. Noy, N.; Xu, Z. J. Interactions of retinol with binding proteins: implications for the mechanism of uptake by cells. Biochemistry 1990, 29, 3878-3883.
57. Bernasconi, C. F. Relaxation kinetics; Academic Press: New York, 1976.
58. Fersht, A. Structure and mechanism in protein science: A guide to enzyme catalysis and protein folding; W. H. Freeman and Company: New York, 1999.