Cytochrome P450 from photobacterium profundum SS9, a piezophilic bacterium, exhibits a tightened control of water access to the active site

Biochemistry

Volumn 49, Issue 50, 2010, Pages 10636-10646

  Sineva, Elena V ^a   Davydov, Dmitri R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; COMMON FEATURES; CONFINED WATER; CONFORMATIONAL EQUILIBRIUM; CYTOCHROME P450; CYTOCHROMES P450; EXPRESSION IN ESCHERICHIA COLI; HEME POCKETS; HIGH HYDROSTATIC PRESSURE; HIGH SPIN STATE; HIGH SPINS; LIGAND BINDING; LIGAND-FREE; MYRISTIC ACID; PHOTOBACTERIUM PROFUNDUM; PRESSURE PERTURBATION; PRESSURE-INDUCED TRANSITIONS; PROTEIN HYDRATION; REACTION VOLUME; REDOX STATE; SATURATED FATTY ACID; SPIN STATE; UNSATURATED FATTY ACIDS;

ACCESS CONTROL; CLONING; COMPLEXATION; ESCHERICHIA COLI; HYDRATION; HYDROSTATIC PRESSURE; LIGANDS; PORPHYRINS; PROTEINS; SPIN DYNAMICS;

FATTY ACIDS;

ARACHIDONIC ACID; ARACHIDONOYLGLYCINE; CYTOCHROME P450; FATTY ACID DERIVATIVE; HEMOPROTEIN; LIGAND; MYRISTIC ACID; PALMITIC ACID; PARINARIC ACID; SATURATED FATTY ACID; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID;

ACCELERATION; ADAPTATION; ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CLONING; CONFORMATIONAL TRANSITION; ENZYME BINDING; ESCHERICHIA COLI; HABITAT; HYDRATION; HYDROSTATIC PRESSURE; LIGAND BINDING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOBACTERIUM PHOSPHOREUM; PRIORITY JOURNAL; REDOX STRESS; WATER AVAILABILITY;

BACTERIAL PROTEINS; CATALYTIC DOMAIN; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; FATTY ACIDS; PHOTOBACTERIUM; PROTEIN BINDING; WATER;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PHOTOBACTERIUM PROFUNDUM;

EID: 78650400632     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101466y     Document Type: Article

References (51)

1. Kornblatt, J. A. and Kornblatt, M. J. (2002) The effects of osmotic and hydrostatic pressures on macromolecular systems Biochim. Biophys. Acta 1595, 30-47
2. Rupley, J. A. and Careri, G. (1991) Protein hydration and function Adv. Protein Chem. 41, 37-172
3. Rand, R. P. (2004) Probing the role of water in protein conformation and function Philos. Trans. R. Soc. London, Ser. B 359, 1277-1285
4. Pal, S. K. and Zewail, A. H. (2004) Dynamics of water in biological recognition Chem. Rev. 104, 2099-2123
5. Scorciapino, M. A., Robertazzi, A., Casu, M., Ruggerone, P., and Ceccarelli, M. (2010) Heme proteins: the role of solvent in the dynamics of gates and portals J. Am. Chem. Soc. 132, 5156-5163
6. Akasaka, K. (2006) Probing conformational fluctuation of proteins by pressure perturbation Chem. Rev. 106, 1814-1835
7. Chalikian, T. V. and Macgregor, R. B., Jr. (2009) Origins of pressure-induced protein transitions J. Mol. Biol. 394, 834-842
8. Kharakoz, D. P. (1997) Partial volumes and compressibilities of extended polypeptide chains in aqueous solution: additivity scheme and implication of protein unfolding at normal and high pressure Biochemistry 36, 10276-10285
9. Weber, G. and Drickamer, H. G. (1983) The effect of high pressure upon proteins and other biomolecules Q. Rev. Biophys. 16, 89-112
10. Hui Bon Hoa, G., McLean, M. A., and Sligar, S. G. (2002) High pressure, a tool for exploring heme protein active sites Biochim. Biophys. Acta 1595, 297-308
11. Heremans, K. and Smeller, L. (1998) Protein structure and dynamics at high pressure Biochim. Biophys. Acta 1386, 353-370
12. Macgregor, R. B. (2002) The interactions of nucleic acids at elevated hydrostatic pressure Biochim. Biophys. Acta 1595, 266-276
13. Occhipinti, E., Bec, N., Gambirasio, B., Baietta, G., Martelli, P. L., Casadio, R., Balny, C., Lange, R., and Tortora, P. (2006) Pressure and temperature as tools for investigating the role of individual non-covalent interactions in enzymatic reactions Sulfolobus solfataricus carboxypeptidase as a model enzyme Biochim. Biophys. Acta 1764, 563-572
14. Loida, P. J. and Sligar, S. G. (1993) Molecular recognition in cytochrome P-450: mechanism for the control of uncoupling reactions Biochemistry 32, 11530-11538
15. Di Primo, C., Hui Bon Hoa, G., Douzou, P., and Sligar, S. G. (1992) Heme-pocket-hydration change during the inactivation of cytochrome P-450camphor by hydrostatic pressure Eur. J. Biochem. 209, 583-588
16. Cojocaru, V., Winn, P. J., and Wade, R. C. (2007) The ins and outs of cytochrome P450s Biochim. Biophys. Acta 1770, 390-401
17. Hamdane, D., Zhang, H., and Hollenberg, P. (2008) Oxygen activation by cytochrome P450 monooxygenase Photosynth. Res. 98, 657-666
18. Di Primo, C., Deprez, E., Hui Bon Hoa, G., and Douzou, P. (1995) Antagonistic effects of hydrostatic pressure and osmotic pressure on cytochrome P-450cam spin transition Biophys. J. 68, 2056-2061
19. Bancel, F., Bec, N., Ebel, C., and Lange, R. (1997) A central role for water in the control of the spin state of cytochrome P-450scc Eur. J. Biochem. 250, 276-285
20. Fisher, M. T., Scarlata, S. F., and Sligar, S. G. (1985) High-pressure investigations of cytochrome P-450 spin and substrate binding equilibria Arch. Biochem. Biophys. 240, 456-463
21. Davydov, D. R., Deprez, E., Hui Bon Hoa, G., Knyushko, T. V., Kuznetsova, G. P., Koen, Y. M., and Archakov, A. I. (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
22. Davydov, D. R., Hui Bon Hoa, G., and Peterson, J. A. (1999) Dynamics of protein-bound water in the heme domain of P450BM3 studied by high-pressure spectroscopy: comparison with P450cam and P450 2B4 Biochemistry 38, 751-761
23. Tschirret-Guth, R. A., Koo, L. S., Hoa, G. H., and Ortiz De Montellano, P. R. (2001) Reversible pressure deformation of a thermophilic cytochrome P450 enzyme (CYP119) and its active-site mutants J. Am. Chem. Soc. 123, 3412-3417
24. Davydov, D. R., Knyushko, T. V., and Hui Bon Hoa, G. (1992) High pressure induced inactivation of ferrous cytochrome P-450 LM2 (IIB4) CO complex: evidence for the presence of two conformers in the oligomer Biochem. Biophys. Res. Commun. 188, 216-221
25. Davydov, D. R., Baas, B. J., Sligar, S. G., and Halpert, J. R. (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
26. Davydov, D. R., Davydova, N. Y., and Halpert, J. R. (2008) Allosteric transitions in cytochrome P450eryF explored with pressure-perturbation spectroscopy, lifetime FRET, and a novel fluorescent substrate, Fluorol-7GA Biochemistry 47, 11348-11359
27. Davydov, D. R. and Halpert, J. R. (2008) Allosteric P450 mechanisms: multiple binding sites, multiple conformers or both? Expert Opin. Drug Metab. Toxicol. 4, 1523-1535
28. Hui Bon Hoa, G. and Marden, M. C. (1982) The pressure dependence of the spin equilibrium in camphor-bound ferric cytochrome P-450 Eur. J. Biochem. 124, 311-315
29. Renaud, J. P., Davydov, D. R., Heirwegh, K. P., Mansuy, D., and Hui Bon Hoa, G. H. (1996) Thermodynamic studies of substrate binding and spin transitions in human cytochrome P-450 3A4 expressed in yeast microsomes Biochem. J. 319, 675-681
30. Davydov, D. R., Halpert, J. R., Renaud, J. P., and Hui Bon Hoa, G. (2003) Conformational heterogeneity of cytochrome P450 3A4 revealed by high pressure spectroscopy Biochem. Biophys. Res. Commun. 312, 121-130
31. Segel, I. H. (1975) Enzyme Kinetics. Behavior and Analysis of Rapid Equilibrium and Steady-State Systems, Wiley, New York.
32. Weber, G. (1991) Protein Interactions, Chapman and Hall, New York.
33. Vezzi, A., Campanaro, S., D'Angelo, M., Simonato, F., Vitulo, N., Lauro, F. M., Cestaro, A., Malacrida, G., Simionati, B., Cannata, N., Romualdi, C., Bartlett, D. H., and Valle, G. (2005) Life at depth: Photobacterium profundum genome sequence and expression analysis Science 307, 1459-1461
34. Brinkhoff, T., Giebel, H. A., and Simon, M. (2008) Diversity, ecology, and genomics of the Roseobacter clade: a short overview Arch. Microbiol. 189, 531-539
35. Yayanos, A. A. (1986) Evolutional and ecological implications of the properties of deep-sea barophilic bacteria Proc. Natl. Acad. Sci. U.S.A. 83, 9542-9546
36. Nogi, Y., Masui, N., and Kato, C. (1998) Photobacterium profundum sp. nov., a new, moderately barophilic bacterial species isolated from a deep-sea sediment Extremophiles 2, 1-7
37. Campanaro, S., Vezzi, A., Vitulo, N., Lauro, F. M., D'Angelo, M., Simonato, F., Cestaro, A., Malacrida, G., Bertoloni, G., Valle, G., and Bartlett, D. H. (2005) Laterally transferred elements and high pressure adaptation in Photobacterium profundum strains BMC Genomics 6, 122
38. Martens, T., Gram, L., Grossart, H. P., Kessler, D., Muller, R., Simon, M., Wenzel, S. C., and Brinkhoff, T. (2007) Bacteria of the Roseobacter clade show potential for secondary metabolite production Microb. Ecol. 54, 31-42
39. McLean, K. J., Lafite, P., Levy, C., Cheesman, M. R., Mast, N., Pikuleva, I. A., Leys, D., and Munro, A. W. (2009) The structure of Mycobacterium tuberculosis CYP125: molecular basis for cholesterol binding in a P450 needed for host infection J. Biol. Chem. 284, 35524-35533
40. Jung, C., Hui Bon Hoa, G., Davydov, D., Gill, E., and Heremans, K. (1995) Compressibility of the heme pocket of substrate analogue complexes of cytochrome P-450cam-CO. The effect of hydrostatic pressure on the Soret band Eur. J. Biochem. 233, 600-606
41. Macdonald, I. D., Smith, W. E., and Munro, A. W. (1996) Inhibitor/fatty acid interactions with cytochrome P-450 BM3 FEBS Lett. 396, 196-200
42. Narhi, L. O. and Fulco, A. J. (1986) Characterization of a catalytically self-sufficient 119,000-dalton cytochrome P-450 monooxygenase induced by barbiturates in Bacillus megaterium J. Biol. Chem. 261, 7160-7169
43. Kitazume, T., Tanaka, A., Takaya, N., Nakamura, A., Matsuyama, S., Suzuki, T., and Shoun, H. (2002) Kinetic analysis of hydroxylation of saturated fatty acids by recombinant P450foxy produced by an Escherichia coli expression system Eur. J. Biochem. 269, 2075-2082
44. Chaurasia, C. S., Alterman, M. A., Lu, P., and Hanzlik, R. P. (1995) Biochemical characterization of lauric acid omega-hydroxylation by a CYP4A1/NADPH-cytochrome P450 reductase fusion protein Arch. Biochem. Biophys. 317, 161-169
45. Tamburini, P. P., Gibson, G. G., Backes, W. L., Sligar, S. G., and Schenkman, J. B. (1984) Reduction kinetics of purified rat liver cytochrome P-450. Evidence for a sequential reaction mechanism dependent on the hemoprotein spin state Biochemistry 23, 4526-4533
46. Helms, V., Deprez, E., Gill, E., Barret, C., Hui Bon Hoa, G., and Wade, R. C. (1996) Improved binding of cytochrome P450cam substrate analogues designed to fill extra space in the substrate binding pocket Biochemistry 35, 1485-1499
47. Blanck, J., Ristau, O., Zhukov, A. A., Archakov, A. I., Rein, H., and Ruckpaul, K. (1991) Cytochrome P-450 spin state and leakiness of the monooxygenase pathway Xenobiotica 21, 121-135
48. Schwarze, W., Blanck, J., Ristau, O., Janig, G. R., Pommerening, K., Rein, H., and Ruckpaul, K. (1985) 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. 54, 127-141
49. Sineva, E. V. and Davydov, D. R. (2010) Constrained water access to the active site of cytochrome P450 from the piezophilic bacterium Photobacterium profundum, High Presure Res. (in press).
50. Rydberg, P., Rod, T. H., Olsen, L., and Ryde, U. (2007) Dynamics of water molecules in the active-site cavity of human cytochromes P450 J. Phys. Chem. B 111, 5445-5457
51. Schulze, H., Hui Bon Hoa, G., Helms, V., Wade, R. C., and Jung, C. (1996) Structural changes in cytochrome P-450cam effected by the binding of the enantiomers (1R)-camphor and (1S)-camphor Biochemistry 35, 14127-14138