Chain length-dependent cooperativity in fatty acid binding and oxidation by cytochrome P450BM3 (CYP102A1)

Protein and Cell

Volumn 2, Issue 8, 2011, Pages 656-671

  Rowlatt, Benjamin ^a   Yorke, Jake A ^a   Strong, Anthony J ^a   Whitehouse, Christopher J C ^a   Bell, Stephen G ^a   Wong, Luet Lok ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

allosteric effect; cooperativity; CYP102A1; fatty acid; monooxygenase

Indexed keywords

CYTOCHROME P450 BM3; HEME; LAURIC ACID; MYRISTIC ACID; PALMITIC ACID; PHOSPHATE; QUERCETIN;

ARTICLE; BACILLUS MEGATERIUM; BINDING SITE; CONTROLLED STUDY; ELECTRON TRANSPORT; FATTY ACID BINDING; FATTY ACID METABOLISM; FATTY ACID OXIDATION; IONIC STRENGTH; MICHAELIS MENTEN KINETICS; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

BACILLUS MEGATERIUM;

EID: 80053090303     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-011-1082-6     Document Type: Article

References (53)

1. Baas, B. J., Denisov, I. G., and Sligar, S. G. (2004). Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch Biochem Biophys 430, 218-228.
2. Bell, S. G., Dale, A., Rees, N. H., and Wong, L. L. (2010a). A cytochrome P450 class I electron transfer system from Novosphingobium aromaticivorans. Appl Microbiol Biotechnol 86, 163-175.
3. Bell, S. G., Hoskins, N., Whitehouse, C. J. C., and Wong, L.-L. (2007). Design and Engineering of Cytochrome P450 Systems. Metal Ions Life Sci 3, 437-476.
4. Bell, S. G., Tan, A. B., Johnson, E. O., and Wong, L. L. (2010b). Selective oxidative demethylation of veratric acid to vanillic acid by CYP199A4 from Rhodopseudomonas palustris HaA2. Mol Biosyst 6, 206-214.
5. Bell, S. G., and Wong, L. L. (2007). P450 enzymes from the bacterium Novosphingobium aromaticivorans. Biochem Biophys Res Commun 360, 666-672.
6. Bell, S. G., Xu, F., Johnson, E. O., Forward, I. M., Bartlam, M., Rao, Z., and Wong, L. L. (2010c). Protein recognition in ferredoxin-P450 electron transfer in the class I CYP199A2 system from Rhodopseudomonas palustris. J Biol Inorg Chem 15, 315-328.
7. Brewer, C. B., and Peterson, J. A. (1988). Single turnover kinetics of the reaction between oxycytochrome P-450cam and reduced putidaredoxin. J Biol Chem 263, 791-798.
8. Budde, M., Maurer, S. C., Schmid, R. D., and Urlacher, V. B. (2004). Cloning, expression and characterisation of CYP102A2, a self-sufficient P450 monooxygenase from Bacillus subtilis. Appl Microbiol Biotechnol 66, 180-186.
9. Carmichael, A. B., and Wong, L. L. (2001). Protein engineering of Bacillus megaterium CYP102. The oxidation of polycyclic aromatic hydrocarbons. Eur J Biochem 268, 3117-3125.
10. Chowdhary, P. K., Alemseghed, M., and Haines, D. C. (2007). Cloning, expression and characterization of a fast self-sufficient P450: CYP102A5 from Bacillus cereus. Arch Biochem Biophys 468, 32-43.
11. Cryle, M. J., Espinoza, R. D., Smith, S. J., Matovic, N. J., and De Voss, J. J. (2006). Are branched chain fatty acids the natural substrates for P450(BM3)? Chem Commun 2353-2355.
12. Davydov, D. R., Botchkareva, A. E., Kumar, S., He, Y. Q., and Halpert, J. R. (2004). An electrostatically driven conformational transition is involved in the mechanisms of substrate binding and cooperativity in cytochrome P450eryF. Biochemistry 43, 6475-6485.
13. 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.
14. Denisov, I. G., Baas, B. J., Grinkova, Y. V., and Sligar, S. G. (2007). Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation. J Biol Chem 282, 7066-7076.
15. Denisov, I. G., Frank, D. J., and Sligar, S. G. (2009). Cooperative properties of cytochromes P450. Pharmacol Ther 124, 151-167.
16. Dietrich, M., Eiben, S., Asta, C., Do, T. A., Pleiss, J., and Urlacher, V. B. (2008). Cloning, expression and characterisation of CYP102A7, a self-sufficient P450 monooxygenase from Bacillus licheniformis. Appl Microbiol Biotechnol 79, 931-940.
17. Girvan, H. M., Dunford, A. J., Neeli, R., Ekanem, I. S., Waltham, T. N., Joyce, M. G., Leys, D., Curtis, R. A., Williams, P., Fisher, K., et al. (2011). Flavocytochrome P450 BM3 mutant W1046A is a NADH-dependent fatty acid hydroxylase: implications for the mechanism of electron transfer in the P450 BM3 dimer. Arch Biochem Biophys 507, 75-85.
18. Guengerich, F. P. (2001). Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chem Res Toxicol 14, 611-650.
19. Gustafsson, M. C., Roitel, O., Marshall, K. R., Noble, M. A., Chapman, S. K., Pessegueiro, A., Fulco, A. J., Cheesman, M. R., von Wachenfeldt, C., and Munro, A. W. (2004). Expression, purification, and characterization of Bacillus subtilis cytochromes P450 CYP102A2 and CYP102A3: flavocytochrome homologues of P450 BM3 from Bacillus megaterium. Biochemistry 43, 5474-5487.
20. Haines, D. C., Chen, B., Tomchick, D. R., Bondlela, M., Hegde, A., Machius, M., and Peterson, J. A. (2008). Crystal structure of inhibitor-bound P450BM-3 reveals open conformation of substrate access channel. Biochemistry 47, 3662-3670.
21. Haines, D. C., Sevrioukova, I. F., and Peterson, J. A. (2000). The FMNbinding domain of cytochrome P450BM-3: resolution, reconstitution, and flavin analogue substitution. Biochemistry 39, 9419-9429.
22. Haines, D. C., Tomchick, D. R., Machius, M., and Peterson, J. A. (2001). Pivotal role of water in the mechanism of P450BM-3. Biochemistry 40, 13456-13465.
23. Hasemann, C. A., Kurumbail, R. G., Boddupalli, S. S., Peterson, J. A., and Deisenhofer, J. (1995). Structure and function of cytochromes P450: a comparative analysis of three crystal structures. Structure 3, 41-62.
24. Hegde, A., Haines, D. C., Bondlela, M., Chen, B., Schaffer, N., Tomchick, D. R., Machius, M., Nguyen, H., Chowdhary, P. K., Stewart, L., et al. (2007). Interactions of substrates at the surface of P450s can greatly enhance substrate potency. Biochemistry 46, 14010-14017.
25. Huang, W. C., Westlake, A. C., Maréchal, J. D., Joyce, M. G., Moody, P. C., and Roberts, G. C. (2007). Filling a hole in cytochrome P450 BM3 improves substrate binding and catalytic efficiency. J Mol Biol 373, 633-651.
26. Ingelman-Sundberg, M., and Johansson, I. (1980). Catalytic properties of purified forms of rabbit liver microsomal cytochrome P-450 in reconstituted phospholipid vesicles. Biochemistry 19, 4004-4011.
27. Jovanovic, T., Farid, R., Friesner, R. A., and McDermott, A. E. (2005). Thermal equilibrium of high- and low-spin forms of cytochrome P450 BM-3: repositioning of the substrate? J Am Chem Soc 127, 13548-13552.
28. Joyce, M. G., Girvan, H. M., Munro, A. W., and Leys, D. (2004). A single mutation in cytochrome P450 BM3 induces the conformational rearrangement seen upon substrate binding in the wild-type enzyme. J Biol Chem 279, 23287-23293.
29. Kitazume, T., Haines, D. C., Estabrook, R. W., Chen, B., and Peterson, J. A. (2007). Obligatory intermolecular electron-transfer from FAD to FMN in dimeric P450BM-3. Biochemistry 46, 11892-11901.
30. Lentz, O., Urlacher, V., and Schmid, R. D. (2004). Substrate specificity of native and mutated cytochrome P450 (CYP102A3) from Bacillus subtilis. J Biotechnol 108, 41-49.
31. Li, H., and Poulos, T. L. (1997). The structure of the cytochrome p450BM-3 haem domain complexed with the fatty acid substrate, palmitoleic acid. Nat Struct Biol 4, 140-146.
32. Li, Q. S., Ogawa, J., Schmid, R. D., and Shimizu, S. (2005). Indole hydroxylation by bacterial cytochrome P450BM-3 and modulation of activity by cumene hydroperoxide. Biosci Biotechnol Biochem 69, 293-300.
33. Malik, W. U., and Jain, A. K. (1967). Electrometric determination of critical micelle concentrations of soap solutions. J Electroanal Chem 14, 37-41.
34. Maurer, S. C., Kuhnel, K., Kaysser, L. A., Eiben, S., Schmid, R. D., and Urlacher, V. B. (2005). Catalytic hydroxylation in biphasic systems using CYP102A1 mutants. Adv Synth Catal 347, 1090-1098.
35. Maves, S. A., Yeom, H., McLean, M. A., and Sligar, S. G. (1997). Decreased substrate affinity upon alteration of the substratedocking region in cytochrome P450BM-3. FEBS Lett 414, 213-218.
36. Mizushima, S., Ishida, M., and Kitahara, K. (1966). Chemical composition of the protoplast membrane of Bacillus megaterium. J Biochem 59, 374-381.
37. Modi, S., Primrose, W. U., Lian, L. Y., and Roberts, G. C. (1995). Effect of replacement of ferriprotoporphyrin IX in the haem domain of cytochrome P-450 BM-3 on substrate binding and catalytic activity. Biochem J 310, 939-943.
38. Munro, A. W., Daff, S., Coggins, J. R., Lindsay, J. G., and Chapman, S. K. (1996). Probing electron transfer in flavocytochrome P-450 BM3 and its component domains. Eur J Biochem 239, 403-409.
39. 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.
40. Narhi, L. O., and Fulco, A. J. (1987). Identification and characterization of two functional domains in cytochrome P-450BM-3, a catalytically self-sufficient monooxygenase induced by barbiturates in Bacillus megaterium. J Biol Chem 262, 6683-6690.
41. Neeli, R., Girvan, H. M., Lawrence, A., Warren, M. J., Leys, D., Scrutton, N. S., and Munro, A. W. (2005). The dimeric form of flavocytochrome P450 BM3 is catalytically functional as a fatty acid hydroxylase. FEBS Lett 579, 5582-5588.
42. Noble, M. A., Miles, C. S., Chapman, S. K., Lysek, D. A., MacKay, A. C., Reid, G. A., Hanzlik, R. P., and Munro, A. W. (1999). Roles of key active-site residues in flavocytochrome P450 BM3. Biochem J 339, 371-379.
43. Ost, T. W., Clark, J., Mowat, C. G., Miles, C. S., Walkinshaw, M. D., Reid, G. A., Chapman, S. K., and Daff, S. (2003). Oxygen activation and electron transfer in flavocytochrome P450 BM3. J Am Chem Soc 125, 15010-15020.
44. Roberts, A. G., Campbell, A. P., and Atkins, W. M. (2005). The thermodynamic landscape of testosterone binding to cytochrome P450 3A4: ligand binding and spin state equilibria. Biochemistry 44, 1353-1366.
45. Rock, D. A., Perkins, B. N. S., Wahlstrom, J., and Jones, J. P. (2003). A method for determining two substrates binding in the same active site of cytochrome P450BM3: an explanation of high energy omega product formation. Arch Biochem Biophys 416, 9-16.
46. Urlacher, V. B., and Eiben, S. (2006). Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol 24, 324-330.
47. van Vugt-Lussenburg, B. M., Damsten, M. C., Maasdijk, D. M., Vermeulen, N. P., and Commandeur, J. N. (2006). Heterotropic and homotropic cooperativity by a drug-metabolising mutant of cytochrome P450 BM3. Biochem Biophys Res Commun 346, 810-818.
48. Whitehouse, C. J., Bell, S. G., Tufton, H. G., Kenny, R. J., Ogilvie, L. C., and Wong, L. L. (2008). Evolved CYP102A1 (P450BM3) variants oxidise a range of non-natural substrates and offer new selectivity options. Chem Commun 966-968.
49. Whitehouse, C. J., Bell, S. G., Yang, W., Yorke, J. A., Blanford, C. F., Strong, A. J., Morse, E. J., Bartlam, M., Rao, Z., and Wong, L. L. (2009). A highly active single-mutation variant of P450BM3 (CYP102A1). Chembiochem 10, 1654-1656.
50. Whitehouse, C. J., Yang, W., Yorke, J. A., Rowlatt, B. C., Strong, A. J., Blanford, C. F., Bell, S. G., Bartlam, M., Wong, L. L., and Rao, Z. (2010). Structural basis for the properties of two single-site proline mutants of CYP102A1 (P450BM3). Chembiochem 11, 2549-2556.
51. Whitehouse, C. J. C., Yang, W., Yorke, J. A., Tufton, H. G., Ogilvie, L. C. I., Bell, S. G., Zhou, W., Bartlam, M., Rao, Z., and Wong, L. L. (2011). Structure, electronic properties and catalytic behaviour of an activity-enhancing CYP102A1 (P450BM3) variant. Dalton Trans May 20. [Epub ahead of print] DOI: 10. 1039/C1DT10098J.
52. Yang, W., Bell, S. G., Wang, H., Zhou, W., Hoskins, N., Dale, A., Bartlam, M., Wong, L. L., and Rao, Z. (2010). Molecular characterization of a class I P450 electron transfer system from Novosphingobium aromaticivorans DSM12444. J Biol Chem 285, 27372-27384.
53. Yeom, H. Y., and Sligar, S. G. (1997). Oxygen activation by cytochrome P450BM-3: effects of mutating an active site acidic residue. Arch Biochem Biophys 337, 209-216.